Minimally invasive surgical biopsy confirms PET findings inesophageal cancer

J. D. Luketich, P. Schauer, K. Urso, D. W. Townsend, C. P. Belani, C. Cidis Meltzer, P. F. Ferson, R. J. Keenan

University of Pittsburgh Medical Center, 300 Kaufmann Building, 3471 Fifth Avenue, Pittsburgh, PA 15213, USA

Received: 6 December 1997/Accepted: 14 January 1997

Abstract. This report describes our initial experience usingpositron emission tomography (PET) scanning in esopha-geal cancer patients. In two patients PET identified distantmetastatic disease missed by conventional staging. Laparo-scopic biopsy provided histological confirmation of metas-tases. In the third patient, locoregional lymph nodes wereidentified by PET and confirmed by surgical staging. In thispreliminary report, PET appears to be a promising newnoninvasive modality for staging patients with esophagealcancer.

Key words: Esophageal Cancer — Positron emission to-mography (PET) — Thoracoscopy — Laparoscopy

Positron emission tomography (PET) is an imaging tech-nology that can be used to assess tissue metabolism. Theincreased metabolic demands of tumors can be visualizedthrough increased focal uptake of the positron-emittingtracer 18F-fluorodeoxyglucose (FDG). The distribution ofFDG has been used to distinguish benign from malignanttissue in various types of cancers [4, 16]. This report de-scribes the results of PET scanning in three patients withesophageal cancer.

Case reports

Case 1

A 59-year-old male was diagnosed with localized adenocarcinoma of thedistal esophagus and received neoadjuvant chemotherapy. Prior to esoph-agectomy, restaging including chest and abdominal CT and a bone scanwhich were negative for distant metastatic disease. A PET scan was per-formed to evaluate possible distant metastatic disease prior to surgery.

The PET scan (Fig. 1) demonstrated unsuspected bone metastases to

the T3 vertebral body and the sacroiliac region of the pelvis and an un-suspected liver metastasis. The presence of metastases was confirmedthrough laparoscopic biopsy. Surgical resection of the esophagus was notundertaken. Subsequently the patient developed a T3 radiculopathy anddied of extensive metastatic disease 3 months later.

Case 2

A 64-year-old male was diagnosed with adenocarcinoma of the distalesophagus. CT scans of the chest and abdomen and a bone scan werenegative for metastases. Endoscopic ultrasound revealed enlarged peri-esophageal and gastrohepatic lymph nodes. A PET scan was ordered toevaluate the extent of disease.

The PET scan (Fig. 2) revealed foci of increased FDG uptake in thedistal esophagus, periesophageal, and gastrohepatic lymph regions, con-sistent with a primary tumor and lymph node metastases. Biopsies taken atvideo-assisted thoracoscopic and laparoscopic staging procedures con-firmed metastases to these lymph nodes. The patient was entered into ataxol-platinum neoadjuvant protocol.

Case 3

A 66-year-old male diagnosed with esophageal cancer underwent a trans-hiatal esophagectomy, gastric pull-up, and a neck anastamosis 6 monthsbefore presenting to our clinic with complaints of dysphagia and a singlepalpable left cervical lymph node. Metastatic esophageal cancer was con-firmed by a fine-needle aspirate of the lymph node, and CT scans of theneck and chest showed no other disease. A PET scan was performed toassess the extent of metastatic recurrence.

The PET image (Fig. 3) showed multiple foci of increased uptake ofFDG in the cervical and supraclavicular nodes which were confirmed byfine-needle aspirate as sites of metastasis. Palliative radiotherapy was suc-cessful in relieving dysphagia.

PET methods

Each patient was requested to fast after midnight the evening prior to thePET study. PET imaging was performed on the ECAT ART tomograph(CTI/Siemens PET Systems; Knoxville, TN), located in the UPMC PETFacility. An intravenous injection of 6–8 mCi of FDG was administeredfollowed by a 45-min delay for tracer uptake, prior to whole-body imagingat six bed positions. Images were evaluated for regions of focally increaseduptake relative to adjacent tissues and compared with CT scans for ana-tomic correlation.

Discussion

Patients with esophageal cancer are frequently diagnosedlate in the course of their disease, and up to 50% alreadyCorrespondence to:J. D. Luketich

Surg Endosc (1997) 11: 1213–1215

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© Springer-Verlag New York Inc. 1997

have metastatic disease at presentation. For those with meta-static disease, the outcome is extremely poor: Most patientsdie within 6 months. For apparently localized disease, sur-gical resection alone has been the traditional approach when

there is a potential for complete resection [2, 7, 8]. Unfor-tunately, surgery alone results in 5-year survival rates ofonly 20–30% in most series, and many patients developdistant metastases within 6 months to 1 year. This suggests

Fig. 1. A PET scan(A) showing three sites of metastatic disease:(a) a thoracic vertebral metastasis,(b) a liver metastasis that was not seen on theabdominal CT scan, and(c) a sacroiliac bone metastasis. The bone scan(B) did not detect either of the two bone metastases.

Fig. 2. A PET scan demonstrating periesophageal and gastrohepatic lymph node metastases in addition to the primary esophageal cancer.

Fig. 3. A PET scan demonstrating multiple bilateral cervical lymph node metastases from esophageal cancer.

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that clinically occult metastases were present at initial pre-sentation. Recently, minimally invasive surgical staging hasbeen employed to more accurately evaluate the extent oflocoregional disease and to rule out clinically occult sites ofmetastases. Positron emission tomography (PET) scanningmay facilitate the staging of esophageal cancer.

Preliminary reports on the use of PET scanning in pa-tients with non–small cell lung cancer (NSCLC) are encour-aging [5]. Up to 90% sensitivity and specificity have beenreported in the detection of mediastinal lymph nodes inNSCLC using PET. However, a false-positive rate of be-tween 13 and 20% has been noted in some series, and theultimate role of PET in staging NSCLC continues to beevaluated [1, 3].

Our results suggest PET scanning could play an impor-tant role as a noninvasive staging modality in patients withesophageal cancer. In this report, PET accurately detectedlocal or distant unsuspected metastatic disease in all threepatients. CT scans, bone scans, and endoscopic ultrasoundfailed to detect lymph node involvement in two patients andliver and bone metastases in one patient. The accurate de-tection of locoregional or distant metastases contributed sig-nificantly to the management of their disease. These pre-liminary results suggest that PET scanning may play a rolein the noninvasive staging of patients with esophageal can-cer and may provide targets for minimally invasive surgicalbiopsy.

References

1. Chin R, Ward R, Keyes JW, Choplin RH, Reed JC, Wallenhaupt S,Hudspeth AS, Haponik EF (1995) Mediastinal staging of non-small celllung cancer with positron emission tomography. Am J Respir Crit CareMed 152: 2090–2096

2. Lerut T, DeLeyn P, Coosemans W, Van Raemdonck D (1992) Surgicalstrategies in esophageal carcinoma with emphasis on radical lymphad-enectomy. Ann Surg 216(5): 583–590

3. Patz EF, Lowe VJ, Goodman PC, Herndon J (1995) Thoracic nodalstaging with PET imaging with FDG in patients with bronchogeniccarcinoma. Chest 108(6): 1617–1621

4. Scott WJ, Schwabe JL, Gupta NC, Dewan NA, Reeb SD, Sugimoto JT(1994) Positron emission tomography of lung tumors and mediastinallymph nodes using F-18-fluorodeoxyglucose. Ann Thorac Surg 58:698–703

5. Valk PE, Pounds TR, Hopkins DM, Haseman MK, Hofer GA, GreissHB, Meyers RW, Lutrin CL (1995) Staging non-small cell lung cancerby whole body PET imaging. Ann Thorac Surg 60: 1573–1582

6. Wahl RL, Hutchins G, Buchsbaum D, Liebert M, Grossman HB, FisherS (1991) F-18-2-deoxy-fluoro-D-glucose (FDG) uptake in human tu-mor xenografts: feasibility studies for cancer imaging with PET. Cancer67: 1544–1550

7. Watson A (1994) Operable esophageal cancer: current results from theWest. World J Surg 18: 361–366

8. Zhang DW, Cheng GU, Huang GJ, Zhang RG, Liu XY, Mao YS, WangYG, Chen SJ, Zhang LZ, Wang LJ, Zhang DC, Yang L, Meng PJ, SunKL (1994) Operable squamous esophageal cancer: current results fromthe East. World J Surg 18: 347–354

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Video-assisted thoracoscopic treatment of spinal lesions in thethoracolumbar junction

T. J. Huang,1 R. W. W. Hsu,1 H. P. Liu,2 K. Y. Hsu,1 Y. S. Liao,1 H. N. Shih,1 Y. J. Chen1

Department of Orthopedic Surgery1 and Thoracic and Cardiovascular Surgery,2 Chang Gung Memorial Hospital, Chang Gung Medical College,Taipei, Taiwan, R.O.C.

Received: 6 February 1997/Accepted: 8 April 1997

AbstractBackground:The endoscopic treatment of spinal lesions inthe thoracolumbar junction (T11–L2) poses a great chal-lenge to the surgeon. From November 1, 1995 to December31, 1996, we successfully used a combination of video-assisted thoracoscopy and conventional spinal instrumentsto treat 38 patients with anterior spinal lesions. Twelve ofthem had lesions in the thoracolumbar junction.Methods: The so-called extended manipulating channelmethod was used to perform vertebral biopsy, discectomy,decompressive corpectomy, interbody fusions, and/or inter-nal fixations in these patients. The size of the thoracoscopicportals was greater than usual in order to allow conventionalspinal instruments and a thoracoscope to enter the chestcavity freely and be manipulated by techniques similar tothose used in standard open surgical procedures. In thisseries, the procedures were performed by using either athree-portal approach (2.5–3.5 cm) or a modified two-portaltechnique involving a 5–6 cm larger incision and a smallone for introducing the scope.Results:None of the operations resulted in injury to thegreat vessels, internal organs, or spinal cord. The total timefor the operation ranged from 1.5 to 4.5 h (average, 3); andthe total blood loss ranged from 50 to 3000 cc (average,1050). One patient was converted to an open procedure dueto severe pleural adhesion. Complications included two in-stances of transient intercostal neuralgia, one superficalwound infection, and one residual pneumothorax.Conclusions:The video-assisted technique with the ex-tended manipulating channel method presented in this re-

port simplifies thoracoscopic spinal surgery in the thoraco-lumbar junction and makes it easier. It avoids division of thediaphragm, removal of the rib, and wide spread of the in-tercostal space, and it allows greater control of intraopera-tive vessel bleeding. Using this technique, the number ofportals required during the procedure can be reduced. Inaddition, the technique reduces the endoscopic materialsrequired, thus lowering overall cost. It is an effective andpromising approach.

Key words: Video-assisted thoracoscopic surgery — Tho-racolumbar junction — Spinal lesions

Standard open surgery techniques for spinal lesions in thethoracolumbar junction (T11–L2) usually require divisionof the diaphragm, resection of the rib, and wide spreading ofthe surgical wounds. These procedures may result in in-creased pain, prolonged postoperative rehabilitation, exten-sive scarring, and longer hospitalization [5, 6, 8, 11].

Endoscopic procedures are widely used in peripheraljoints, as well as thoracic, urologic, gynecologic, and gen-eral surgery. The use of thoracoscopy to treat spinal lesionsis a relatively recent development [7, 8, 12, 13]. Among thevariety of video-assisted thoracoscopic spinal proceduresthat have been reported are biopsy, discectomy, anteriorreleasing procedures in scoliosis surgery, decompressivecorpectomy, interbody fusion, and internal instrumentation[1, 7, 8, 11–13]. However, when this technique is used,many problems and complications can develop due to thelimited trocar spaces and lack of suitability of endoscopicinstruments [1, 6–8, 12, 13]. Problems are particularly likelyto arise when the lesions are located in the thoracolumbarjunction. Under one-lung ventilation, the high-riding dia-phragm may occlude the lesion site; therefore, additionalportals and special endo-equipment are needed to facilitateexposure. As many as four, five, or even more portals arecommon in these procedures [1, 8, 12, 13].

Presented in part at the first combined meeting of the Leading EuropeanSpine Society, Zurich, Switzerland, 16–19 October 1996; the third com-bined meeting of spinal and pediatric sections of West Pacific OrthopedicAssociation, Kochi, Japan, 5–8 November 1996; and the first Asian PacificWorkshop on Minimally Invasive Thoracic Surgery, Hong Kong, 21–23November 1996.

Correspondence to:T. J. Huang, Department of Orthopedic Surgery,Chang Gung Memorial Hospital, Chang Gung Medical College, No. 5,Fu-Hsing St. 333, Kweishan, Taoyuan, Taiwan, R.O.C.

Surg Endosc (1997) 11: 1189–1193

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© Springer-Verlag New York Inc. 1997

We report a new approach that uses the so-called ex-tended manipulating channel method [2] to treat spinal le-sions located in the thoracolumbar junction endoscopically.This method allows for the use of a combination of video-assisted thoracoscopy and conventional spinal instrumentsduring surgery. The series presented here comprises 12 pa-tients.

Patients and methods

From November 1, 1995 to December 31, 1996, we used video-assistedthoracoscopic surgery (VATS) to treat 12 patients with anterior spinallesions in the thoracolumbar junction (T11–L2) (Table 1). There were sixwomen and six men; their ages ranged from 24 to 75 years (average, 52).The patients and their families were informed that an open thoracotomymight be necessary if video-thoracoscopic surgery was not successful.

The location of the pathology in the involved vertebra often determinesthe approach. In this series, either a right- or left-sided approach wasfeasible. For lesions involving the L1 body or L1–L2 disc, we prefer aleft-sided approach because the aorta is located just left to the midline andmore space is available next to the vertebral surface. Using the so-calledextended manipulating channel method [2], the number of incisions wasusually sufficient using either a three-portal (Fig. 1) or a modified two-portal technique (Fig. 2).

Case illustration

A 24-year-old man (case 11) suffered from ankylosing spondylitis of >6years’ duration. Due to severe hip pain and flexion deformity, he under-went bilateral total hip replacements 3 years earlier. He presented to uswith progressive mid-back pain of 3 months’ duration and urine retentionof 1 week’s duration. Plain radiographs demonstrated irregular and scle-rotic changes at the bony endplates adjacent to the T10–T11 disc space(Fig. 3). The urodynamic study revealed a detrusor hyporeflexia, and themagnetic resonance imaging (MRI) showed a widening and decreasedsignal intensity of the T10–T11 disc, with mild cord compression at thatlevel (Fig. 4). Prior to the operation, video-assisted thoracoscopic discec-tomy, interbody fusion, and internal fixation were chosen as the course oftreatment.

Under general anesthesia and following intubation with a double-lumenendotracheal tube, the patient was put in the right lateral decubitus position.The operative table was flexed to open the flank region. Skin was drapedand prepped for a posterolateral thoracotomy, so that in the event of in-traoperative complication or if thoracoscopic surgery was not possible theprocedure could be converted. With selective collapse of the left lung, the

chest was entered carefully through a stab incision. The initial trocar in-cision was located at the seventh intercostal space (ICS) along the anterioraxillary line. An 11-mm trocar was used to introduce the operating thora-coscope (0°, 10 mm; Stryker, Kalamazoo, MI, USA).

The lesion site was identified and displayed on the video monitor. Thena larger manipulating channel measuring 5–6 cm in length was createdunder the guidance of the scope; it was made at the level or slightly behindthe posterior axillary line at the T9–T10 ICS (Fig. 2). The diaphragm wasgrasped and pushed down gently with a traditional sponge forceps (9.59,Foster type; Edward Weck, Research Triangle Park, NC, USA) that hadbeen introduced through the manipulating channel. The lung was alsoremoved from the lesion site with the sponge forceps.

Table 1. Clinical data for 12 patients with lesions involving the thoracolumbar function (T11–L2)

Caseno. Sex

Age(yr)

Final diagnosis(level)

Operativeproceduresa

Totaloperatingtime (h)b

Totalbloodloss (cc)

Incisions inchest (no.)

1 F 40 Thoracic disc herniation (T11–T12) 2 3.5 400 Lt (3)2 M 73 Metastatic hepatoma (T11) Conversion to open — — —3 M 52 Acute burst fracture (T11) 3 + 4a + 5 4.5 1,000 Lt (3)4 M 75 Metastatic laryngeal Ca (T12) 3 + 4b 2.5 1,500 Rt (3)5 F 66 Metastatic adenoca, unknown primary (T12) 3 + 4b + 6 3.0 650 Rt (3)6 F 38 Metastatic breast Ca (T11) 3 + 4b + 6 3.0 1,300 Rt (3)7 M 45 Metastatic renal cell Ca (T11) 3c 2.0 3,000 Rt (3)8 F 65 Metastatic adenoca, unknown primary (T11) 1 1.5 50 Rt (3)9 F 34 Neglected old burst fracture (L1) 3 + 4a + 5 + 6 4.0 1,200 Lt (2)

10 M 64 Osteoporotic burst fracture 3 + 4b + 5 2.5 500 Lt (2)11 M 24 Ankylosing spondylitis with discitis (T10–T11) 3 + 4a + 5 3.5 450 Lt (2)12 F 43 Metastatic adenoca, unknown primary (L1) 3 + 4c + 5 3.5 1,500 Lt (2)

a operative procedures: 1, biopsy; 2, discectomy; 3, corpectomy; 4, interbody fusion: a (autograft), b (allograft), and c (polymethylmethacrylate); 5, anteriorinstrumentation (Reduction-Fixation fixator system, Trifix, San Leandro, CA, USA); 6, posterior instrumentation (Harrington rodding techniques).b total operating time: not including posterior procedures.c partial corpectomy only.

Fig. 1. Video-assisted thoracoscopic surgery for spinal lesions in the tho-racolumbar junction (T11–L2) using the so-called extended manipulatingchannel method with a three-portal approach (2.5–3.5-cm incisionwounds).

Fig. 2. A modified two-portal approach for lesions in the thoracolumbarjunction (T11–L2) using an extended manipulating channel measuring 5–6cm and a small incision (2.5 cm) for introducing the thoracoscope.

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The thoracoscope helped us to identify the lesion and establish itsproximity to the aorta. The lesion site was ascertained by a C-arm inten-sifier. The intercostal arteries and veins were isolated using Debakey rightangle forceps (109; Edward Weck) and ligated with hemoclips. The dis-cectomy at the T10–T11 level was then carefully performed under videomonitoring using conventional disc rongeurs (89; Cushing type; Lawton,Tuttlingen, Germany) and elongated bone curettes (159; Howmedica, Ruth-erford, NJ, USA). With selective use of a 0° or 30° thoracoscope, thediscectomy was performed posteriorly and down to the epidural space.Through another incision, a 2 × 2 × 1.2 cm3 tricoctical iliac bone graft was

harvested from the left iliac crest. The graft was inserted and appliedbetween the 10th and 11th thoracic vertebrae using a conventional boneimpactor (129; Trauma-fix; AST, San Leandro, CA, USA).

After that, a guide pin was introduced through the manipulating chan-nel into the anterolateral aspect of the vertebral body. The direction of thepin was checked by a C-arm intensifier, and a vertebral screw was theninserted with a screw-holding device. The position and depth of the screwwere checked again by the C-arm intensifier at the 10th and 11th instru-mented vertebrae. A length of titanium plate (Reduction-Fixation fixatorsystem; Trifix, San Leandro, CA, USA) was applied. The sandwich con-

Fig. 3. Case 11. A plainantero-posterior radiograph of a24-year-old man with ankylosingspondylitis and discitis at the levelof T10–T11.

Fig. 4. Case 11. Magneticresonance imaging of a 24-year-oldman with ankylosing spondylitisand discitis at the level of T10–T11.MRI revealed a widening anddecreased signal intensity of theT10–T11 disc and slight cordcompression.

Fig. 5. Case 11. A 24-year-old manwith ankylosing spondylitis anddiscitis (T10–T11).A:Antero-posterior andB: lateralradiographs taken aftervideo-assisted thoracoscopicdiscectomy, interbody fusion withleft iliac strut grafting, and internalfixation with the Reduction-Fixationfixator system.

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figuration of the two square-shaped washers between the screw and plateallows a variable angle anchorage. Upon completion of the procedure, a nutwas loaded and tightened on top of the screw head (Fig. 5). Once hemo-stasis was assured, a single 32-F chest tube was inserted through theincision site at the anterior axillary line and guided under direct visualiza-tion to the apex of the chest. During completion of the procedure, theincision wounds were closed in layers using 3-0 nylon and an interruptedsuture. A chest radiograph was taken immediately after the operation tomake sure the lung was reinflated. The chest tube was removed on the 3rdpostoperative day. The patient wore a protective Taylor-Knight brace for aperiod of 3 months.

Results

The total time for the operation ranged from 1.5 to 4.5 h(average, 3); the total blood loss ranged from 50 to 3000 cc(average, 1050). The average number of portals made dur-ing the procedures was less than three (Table 1). There wereno injuries to great vessels or visceral organs, and no furtherneurological deterioration was caused by the procedure.One patient (case 2) was converted to an open proceduredue to a severe pleural adhesion from a previous hepatec-tomy procedure. Complications included two cases of tran-sient intercostal neuralgia, one residual pneumothorax afterchest tube removal, and one superficial wound infection.One patient (case 7) had massive bleeding (3000 cc) duringthe operation due to a metastatic renal cell carcinoma, so theprocedure was limited to partial corpectomy only. Six pa-tients had their surgery via a right-sided approach; the othersix had a left-sided one.

Discussion

Since its use was first reported for the treatment of a varietyof thoracic lesions, VATS has become widespread [5].Many procedural refinements and improvements in videooptics and instrumentation have been developed since theinitial report. VATS has only recently been applied in suchthoracic spine procedures as biopsy, discectomy, anteriorreleases in scoliotics, decompressive corpectomy, and inter-nal instrumentations [1, 7, 8, 11–13], so most spine sur-geons are still somewhat unfamiliar with the technique. Al-though in some respects VATS is superior to open thora-cotomy [3, 4, 6, 9, 10], it also has some disadvantages. First,the technique requires a learning curve to acquire the hand-eye coordination necessary to perform remote bone andsoft-tissue dissection, as well as to establish proper orien-tation under the angled endoscope [1, 13]. Second, success-ful one-lung ventilation is required for the operation. Thecomplete assistance of an experienced anesthesiologist is aprerequisite for proper ventilation. Third, high riding of thedome of the diaphragm to the eighth ICS may occur whilethe lung is collapsed [8]. Therefore, the initial portal forintroducing the thoracoscope must be made at the sixth orseventh ICS. Fourth, many spinal lesions, including traumacases, frequently occur in the thoracolumbar junction (T11–L2). It is far more difficult and a technically demanding toperform endoscopic surgery in this sensitive location.

The traditional trocar method in VATS surgery is time-consuming and fraught with difficulties in manipulating theinstruments. Many problems arise due to limited trocarspace and a lack of suitable endoscopic equipment. In thisseries, we used a technique known as the ‘‘extended ma-

nipulating channel method.’’ This method allowed us to usea combination of video-assisted thoracoscopy and conven-tional spinal instruments [2]. Using this approach, the in-struments can be passed freely through the channels andmanipulated in ways similar to the techniques familiar tosurgeons accustomed to standard open procedures.

In the thoracolumbar junction (T11–L2), the endoscopictechnique is complicated by the high riding of the dome ofthe diaphragm. With the VATS approach, the spine can beaccessed as far as the T12–L1 disc space. Although endo-scopic T12 corpectomy is no more difficult to perform thanan open procedure, additional portals are required for thediaphragm’s retraction [8]. Therefore, a total of four, five,or more incisional wounds must be made [1, 8, 13].

Anatomically, the diaphragm originates in three loca-tions: a sternal, a costal, and a vertebral part arise by meansof crura and from the arcuate ligaments. The right crusarises from the sides of the bodies of L1–L3; the left crusarises from the sides of L1 and L2 bodies. The medialarcuate ligament extends from the side of L2 body to the tipof the transverse process of the first lumbar vertebra. Thelateral arcuate ligament extends from the tip of the trans-verse process of the L1 vertebra to the lower border of the12th rib. Therefore, both the crura and arcuate ligaments ofthe diaphragm are inserted below the T12–L1 disc space.When the lesion is located above the T12–L1 disc, it isusually unnecessary to dissect the diaphragm. However, inlesions below the T12–L1 disc, the spine is surrounded bythe diaphragmatic crura, arcuate ligaments, and psoasmuscles. This lower location of the lesion may increasetechnical difficulties for the surgeon when VATS is usedand the instruments are manipulated from the diaphragmabove the lesion. Regan and Ben-Yisbay recommend a com-bined thoracoscopic and laparoscopic method to approachlesions below the T12–L1 disc [12]. However, because ofthe potential hazard of penetration of the peritoneum, thisapproach requires both the exploration and transection ofthe diaphragm [12].

In this paper, we have reported the successful use of acombination of video-assisted thoracoscopy and conven-tional spinal instruments to perform endoscopic spine sur-gery at the thoracolumbar junction (T11–L2). Our techniquedecreases the number of portals required for the procedure.Using the ‘‘extended manipulating channel method,’’ wefound that either a three-portal or a modified two-portalapproach was sufficient. This technique makes thoraco-scopic spinal surgery simpler and easier in this region. Inmost cases, there is no need to transect the diaphragm. Forlesions below the T12–L1 disc level, the diaphragm can bedetached easily from its lumbar origins, the crura, and thearcuate ligaments following ligation of the segmental ves-sels. We have no experience with Regan and Ben-Yisbay’scombined laparoscopic method [12]; however, it seems lesslikely to compromise the surgical objective in our patients.In addition, very few endoscopic materials were required forthe procedure, resulting in a reduction of overall costs.

References

1. Dickman CA, Rosenthal D, Karahalios DG, Paramore CG, Mican CA,Apostolides PJ, Lorenz R, Sonntag VKH (1996) Thoracic vertebrec-tomy and reconstruction using a microsurgical thoracoscopic ap-proach. Neurosurgery 38: 279–293

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2. Huang TJ, Liu HP, Liao YS, Hsu KY, Hsu RWW (1996) Video-assisted thoracoscopic surgery for the spine: preliminary results. ProcJ Endosc Laparosc Surgeons Asia 2: s33–34

3. Kaiser LR, Bavaria JE (1993) Complications of thoracoscopy. AnnThorac Surg 56: 796–798

4. Landreneau RJ, Mack MJ, Mazelhjg SR (1992) Video-assisted tho-racic surgery: basic technical concepts and intercostal approach strat-egies. Ann Thorac Surg 54: 800–807

5. Lewis RJ, Caccavale RJ, Sisler GE (1991) Special report: video-endoscopic thoracic surgery. NJ Med 88: 473–475

6. Liu HP, Chang CH, Lin PJ, Hsieh HC, Chang JP, Hsieh MJ (1994)Video-assisted thoracic surgery. The Chang Gung experience. J Tho-rac Cadiovasc Surg 108: 834–840

7. Mack MJ, Regan JJ, Bobechko WP, Acuff TE (1993) Application ofthoracoscopy for diseases of the spine. Ann Thorac Surg 56: 736–738

8. McAfee PC, Regan JR, Zdeblick T, Zuckerman J, Picetti GD, Heim S,Geis WP, Fedder IL (1995) The incidence of complications in endo-scopic anterior thoracolumbar spinal reconstructive surgery. A pro-

spective multicenter study comprising the first 100 consecutive cases.Spine 14: 1624–1632

9. McCormack PM, Martini N (1979) The changing role of surgery formetastatic pulmonary metastasis. Ann Thorac Surg 28: 139–145

10. Miller JI, Hatcher CR Jr (1978) Thoracoscopy: a useful tool in thediagnosis of thoracic disease. Ann Thorac Surg 26: 68–72

11. Regan JJ, Mack MJ, Picetti GD (1995) A technical report on video-assisted thoracoscopy in thoracic spinal surgery—preliminary descrip-tion. Spine 20: 831–837

12. Regan JJ, Ben-Yisbay A (1995) Thoracolumbar discectomy. In: ReganJJ, McAfee PC, Mack MJ (eds) Atlas of endoscopic spine surgery.Quality Medical Publishing, St Louis

13. Rosenthal D, Sutterlin CE III, Corbin TP, Connolly J, Yuan HA,Kolata RJ, Clem MF, Regan JJ, Mack MJ (1995) Newer applicationsof spinal instrumentation. In: Regan JJ, McAfee PC, Mack MJ (eds)Atlas of endoscopic spine surgery. Quality Medical Publishing, StLouis

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The author replies

It is true that the TAPP and Shouldice techniques differsignificantly. Their similarities are limited to their goal,namely, to cure groin hernias surgically. The differencescomprise the anesthesia, the anatomic approach, the tech-nique itself, the materials used, the difficulty, the cost,and—in our hands—the results. However, a new techniqueshould be compared to the gold standard which—in Swit-zerland—surely is the Shouldice procedure. The aim of thestudy was to compare the results of both techniques in thehands of the same surgeons. It could not be to show thesuperiority of one technique over the other. In that case theresults would have been biased. In fact, to tell the truth, Iinitially doubted very much that the results would be infavor of laparoscopy. The reason for this was that wequickly realized how difficult the TAPP procedure is andthat the learning curve takes longer than we first assumed.The complication rate has dropped since, as have the oper-ating times and thus the costs. The early recurrence rate hasbeen low in the laparoscopic group from the beginning [9].

Open tension-free hernia repairs indeed give promisingresults. Where these techniques are established it seemsreasonable to compare them to the laparoscopic procedure.The common feature being the use of prostheses to reinforcethe groin, the comparison will be between an anterior ap-proach with the mesh in onlay position [4] or in a sublayposition [3] with a second onlay mesh as reinforcement [6]and the laparoscopic posterior sublay approach ultimatelyreferring to the Stoppa technique [7] either transabdomi-nally or extraperitoneally. The solely onlay open techniquewill be prone to miss associated femoral components, whichshould theoretically not be the case in the transinguinalpreperitoneal approach either with or without onlay rein-forcement. The difference compared to the laparoscopictechnique will be that the latter allows a visual control of thewhole inguinal floor and thus a precise diagnosis of allhernias including the very rare obturator hernia [2, 8]. Theplacement of the mesh occurs under vision and even verylarge meshes of 15 × 13 cm, e.g., can be placed withoutfolds and fixed securely, which I find more difficult toachieve in the transinguinal approach. I wonder, too, wheth-er a double buttress onlay-sublay technique does not stiffenthe abdominal wall too much and cause some discomfort tothe patient.

The pain the patients experience postoperatively deter-mines the moment when they resume their usual activities,as most patients do not strain a painful groin even whenencouraged to do so. I have no doubt that open tension-freetechniques are less painful than a conventional herniorrha-phy. There still seems, however, to remain a difference infavor of laparoscopy, especially when perioperative exer-cise testing is used as an adjunct to return to work in thecomparison of methods [5]. The Shouldice Clinic [1] hasshown that the key to preventing technical errors with ananterior approach is experience. We must assume that thiswill be the case for laparoscopic techniques, too. To restrictlaparoscopy to difficult cases like recurrences and bilateralhernias may be dangerous, as it needs a lot of experience toperform a perfect laparoscopic procedure in these cases.

The ease of repair, low cost, low complication rate, andshort time of rehabilitation strongly favor open tension-freemethods. The ultimate standard by which any hernioplastyis judged will nevertheless be the recurrence rate, for in theend the incidence of recurrence determines the true cost ofthe procedure [2]. If we assume that open tension-free her-nioplasties give the same or better results than the laparo-scopic techniques we will need many more trials with largenumbers of patients and at least 2-year results to get theanswer, as most recurrencies in hernioplasties occur withinthe first 2 years [2]. It will be of uttermost importance tohave a high percentage of clinical follow-up of the patientsof more than 90% in order to validate these studies. Herniacenters all over the world seem ideally suited to perform thistask.

References

1. Ben David R (1989) New techniques in hernia repair. World J Surg 13:522–531

2. Felix EL, Michas CA, Gonzalez MH Jr (1997) Laparoscopic hernio-plasty: why does it work? Surg Endosc 11: 36–41

3. Gilbert AI (1991) Inguinal hernia repair: biomaterials and suturelessrepair. Perspect Gen Surg 2: 113–129

4. Lichtenstein IL, Shulman AG (1974) Ambulatory outpatient hernia sur-gery, including a new concept, introducing tension-free repair. Int Surg71: 1–7

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5. Payne JH Jr, Grininger LM, Izawa MT, Podoll EF, Lindahl PJ, BalfourJ (1994) Laparoscopic or open inguinal herniorrhaphy? A randomizedprospective trial. Arch Surg 129: 973–981

6. Rutkow IM (1994) Open tension-free mesh plug versus laparoscopicgroin herniorrhaphy: economic practicalities. In: Bu¨chler MW, Farth-mann EH (eds) Laparoscopic hernia repair: a new standard? Progress inSurgery vol 21. Karger, Basel Freiburg Paris London New York, pp105–112

7. Stoppa R (1989) The treatment of complicated groin and incisionalhernias. World Surg 23: 545–554

8. Tschudi J, Wagner M, Klaiber Ch (1993) Laparoskopische Operationeiner incarcerierten Obturatoriushernie mit assistierter Darmresektion.Chirurg 64: 827–828

9. Tschudi J, Wagner M, Klaiber Ch, Brugger JJ, Frei E, Kra¨henbuhl L,Inderbitzi R, Husler J, Hsu Schmitz S (1996) Controlled multicentertrial of laparoscopic transabdominal preperitoneal hernioplasty vsShouldice herniorrhaphy: early results. Surg Endosc 10: 845–847

J. Tschudi

Bahnhofstr. 39CH-2502 BielSwitzerland

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Letters to the editor

Tumor dissemination during laparoscopic cholecystectomy forgallbladder carcinoma

Port site and peritoneal tumor seeding is a lethal complica-tion following laparoscopic cholecystectomy (LC) for gall-bladder carcinoma. Since the first report by Drouard et al.[4] in 1991, many other cases of seeding have been pub-lished. The number of previous articles appearing inSurgi-cal Endoscopy[2, 3, 5, 8, 10–12, 14, 15] suggests thatreaders of the journal are very interested in this problem.We attempt here to obtain answers from the literature as towhether LC promotes tumor seeding more than open cho-lecystectomy, and by what mechanisms.

The true incidence of port site and peritoneal seedingafter LC for gallbladder cancer is not known, as cases with-out this complication typically are not reported. Only afew small studies allow an estimate of incidence. Wibben-meyer et al. [16] reported that three of six patients under-going LC for unsuspected cancer developed seeding. Fonget al. [6] reported that four of 10 patients with laparoscopi-cally resected cancer developed tumor implants from seed-ing soon after LC. Sandor and associates [12] reported thattwo of three patients undergoing LC for unsuspected cancerdeveloped port site recurrences. In our experience, one oftwo LC patients with unsuspected cancer developed perito-neal seeding (unpublished data). Considering these foursmall series, the incidence of tumor seeding after LC isconsiderable. In contrast, we previously have reported thatnone of 98 patients with unsuspected gallbladder carcinomadeveloped wound metastases after open cholecystectomy[13].

A recent study in rats [9] revealed that port site seedingoccurred more frequently after laparoscopic tumor ma-nipulation than after an open procedure; seeding developedequally in ‘‘contaminated’’ ports from which a tumor-la-den instrument was withdrawn and ‘‘clean’’ ports fromwhich a tumor-free laparoscope was retrieved. Clinically,also, seeding may occur at ports which had no evidentcontact with tumor [8, 9]; pneumoperitoneum with carbondioxide may explain seeding at apparently clean port sites[2, 9].

Another unresolved question is whether laparoscopic re-section could enhance hematogeneous or lymphatic dis-semination. Fong et al. [6] and Nishizaki et al. [10] havereported hepatic metastases appearing soon after LC.

Finally, many anecdotal reports of seeding after LC

have omitted critical information such as the incidence ofcancer in the surgeons’ LC experience, the incidence ofseeding in their cancer cases, the TNM stage [1, 7] of thetumor, whether bile spillage occurred, and whether a gall-bladder bag was used. The follow-up period also is short inmost reports. Future authors should ensure that such data isincluded, especially since prospective randomized trials re-garding this complication are largely precluded by ethicalissues and tumor rarity.

In conclusion, LC risks tumor dissemination more thanopen cholecystectomy, not only by direct contact but also bymetastatic spread. Well-documented clinical reports andwell-designed animal studies are needed to better under-stand this lethal complication.

References

1. Beahrs OH, Henson DE, Hutter RVP, Kennedy BJ (eds) (1992)Manual for staging of cancer. 4th ed. JB Lippincott, Philadelphia

2. Birkett DH (1995) Spilled cells, spilled clips, spilled stones: new prob-lems or old challenges. Surg Endosc 9: 269–271

3. Copher JC, Rogers JJ, Dalton ML (1995) Trocar-site metastasis fol-lowing laparoscopic cholecystectomy for unsuspected carcinoma ofthe gallbladder: case report and review of the literature. Surg Endosc9: 348–350

4. Drouard F, Delamarre J, Capron J (1991) Cutaneous seeding of gall-bladder cancer after laparoscopic cholecystectomy. N Engl J Med 325:1316

5. Ferzli GS, Daou R (1994) Laparoscopic cholecystectomy and gall-bladder cancer. Surg Endosc 8: 1357

6. Fong Y, Brennan MF, Turnbull A, Colt DG, Blumgart LH (1993)Gallbladder cancer discovered during laparoscopic surgery: potentialfor iatrogenic tumor dissemination. Arch Surg 128: 1054–1056

7. Hermanek P, Sobin LH (eds) (1992) UICC TNM classification ofmalignant tumours. 4th ed. 2nd rev. Springer-Verlag, Berlin

8. Jacobi CA, Keller H, Mo¨nig S, Said S (1995) Implantation metastasisof unsuspected gallbladder carcinoma after laparoscopy. Surg Endosc9: 351–352

9. Mathew G, Watson DI, Rofe AM, Baigrie CF, Ellis T, Jamieson GG(1996) Wound metastases following laparoscopic and open surgery forabdominal cancer in a rat model. Br J Surg 83: 1087–1090

10. Nishizaki T, Matsumata T, Hashizume M, Maeda T, Otsuka K, Sugi-machi K (1994) Hepatic metastasis after laparoscopic cholecystectomyfor polypoid gallbladder cancer followed by radical surgery. Surg En-dosc 8: 1436–1438

11. Sailer M, Debus S, Fuchs KH, Thiede A (1995) Peritoneal seeding ofgallbladder cancer after laparoscopic cholecystectomy. Surg Endosc 9:1298–1300Correspondence to:Y. Shirai

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12. Sandor J, Ihasz M, Fazekas T, Rego¨ly-Merei J, Batorfi J (1995) Un-expected gallbladder cancer and laparoscopic surgery. Surg Endosc 9:1207–1210

13. Shirai Y, Yoshida K, Tsukada K, Muto T (1992) Inapparent carcinomaof the gallbladder: an appraisal of a radical second operation aftersimple cholecystectomy. Ann Surg 215: 326–331

14. Targarona EM, Pons MJ, Viella P, Trı´as M (1994) Unsuspected car-cinoma of the gallbladder: a laparoscopic dilemma. Surg Endosc 8:211–213

15. Wade TP, Comitalo JB, Andrus CH, Goodwin MN Jr, Kaminski DL(1994) Laparoscopic cancer surgery: lessons from gallbladder cancer.Surg Endosc 8: 698–701

16. Wibbenmeyer LA, Wade TP, Chen RC, Meyer RC, Turgeon RP, An-

drus CH (1995) Laparoscopic cholecystectomy can disseminate in situcarcinoma of the gallbladder. J Am Coll Surg 181: 504–510

Y. ShiraiT. OhtaniK. Hatakeyama

Department of SurgeryNiigata University School of Medicine1 Asahimachi-doriNiigata City 951Japan

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Ambulatory laparoscopic fundoplication

M. A. Milford, T. A. Paluch

Department of Surgery, Kaiser Foundation Medical Center, 4647 Zion Avenue, San Diego, CA 92120, USA

Received: 1 April 1996/Accepted: 29 May 1997

AbstractBackground:Increasingly larger series of laparoscopic fun-doplications (LF) are being reported. A well-documentedadvantage of the laparoscopic approach is shortened hospi-tal stay. Most centers report typical lengths of stay (LOS)for LF of 2–3 days. Our success with LF with a LOS of 1day led to an attempt at performing LF on an ambulatorybasis.Methods:Sixty-one consecutive patients with appropriatecriteria for LF underwent surgery at our institution. Patientswere counseled by the authors as to the usual postop courseand progression of diet. All patients received preemptiveanalgesia (PEA) consisting of perioperative ketorolac andpreincisional local infiltration with bupivicaine. Anestheticmanagement included induction with propofol, high-doseinhalational anesthetics, minimizing administration of par-enteral narcotics, and avoidance of reversal of neuromuscu-lar blockade. Immediate postop pain management includedparenteral ketorolac and oral hydro- or oxycodone. All pa-tients were given oral fluids and soft solids after transferfrom the recovery room to the postoperative observationunit. Two patients were excluded from ambulatory consid-eration due to excessive driving distance from our hospital.Another two were hospitalized for observation after expe-riencing intraoperative technical problems.Results:Of 57 patients in whom same-day discharge wasattempted, there were three failures requiring overnight hos-pitalization: All were due to pain and nausea; one patientalso suffered transient urinary retention. There were no ad-verse outcomes related to early discharge, and there were noreadmissions. One patient returned to the emergency roomafter delayed development of urinary retention. Mediantime from conclusion of operation to discharge was lessthan 5 h. No patients expressed dissatisfaction with earlydischarge on follow-up interview.Conclusions:LF can be safely performed as an ambulatoryprocedure. Analgesic and anesthetic management should betailored to minimize nausea and provide adequate pain con-trol.

Key words: Laparoscopic fundoplication — Ambulatorysurgery — Preemptive analgesia — Propofol — Ketorolac— Bupivicaine

Minimally invasive surgical techniques have created a revo-lution in the management of gastroesophageal reflux disease(GERD). The ability to combine the time-tested efficacyand durability of total and partial fundoplications with themore rapid recovery afforded by laparoscopic techniques isat the cornerstone of this change. As increasingly largerseries of laparoscopic fundoplications (LF) are reported, aclear and favorable picture of both outcomes and costs isemerging. Although the cost of surgical therapy hinges onmany variables, length of hospital stay (LOS) is a primecontributor. Published American series of LF, ranging up-ward to nearly 300 patients, have reported average LOS of2–4 days [3, 4]. Against concurrent controls, this wouldappear to afford a greater than 5-day improvement in LOScompared with fundoplication via laparotomy [6].

In our own series of LF, a gradual evolution in analgesicand anesthetic techniques combined with improving patientcare strategies resulted in a more predictable recovery andprogressively shorter LOS. This was accomplished withoutcompromise in safety, efficacy, or patient satisfaction. Afterfirst establishing a consistent and reproducible experiencewith overnight hospitalization for LF, we embarked on atrial of same-date discharge, i.e., true ambulatory surgery.

Patients and methods

From May 1995 to January 1997, a consecutive series of 61 patients withdocumented GERD were referred from our Gastroenterology Unit for LFby the authors. The patients, 26 women and 35 men, ranged in age from 30to 77 years, with a median of 47 years. Only one patient was over 65 yearsof age. Age distribution is shown in Fig. 1. The women ranged in weightfrom 56 to 109 kg (123–240 pounds), with Body Mass Indices (BMI)(calculated as weight in kilograms, divided by height in meters, squared)ranging from 23.9 to 38.1. The men ranged from 68 to 130 kg (150–286pounds), with BMI ranging from 23.4 to 37.7. BMI distribution for allpatients is shown in Fig. 2. All had met criteria for operability on the basisof endoscopically documented esophagitis, and dependence upon omepra-Correspondence to:M. A. Milford

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zole (Prilosec) for symptom control. Esophageal motility was routinelyassessed by preoperative esophageal manometry. In 51 patients, esopha-geal body motility was normal, and laparoscopic Nissen fundoplicationwas performed. In 10 patients, esophageal motility was diminished, andpartial (modified Toupet) fundoplication was performed. Patients were notexcluded from operative candidacy due to age, weight, or prior upperabdominal operative history. Comorbidities were relatively rare, althoughseven patients (11%) were under treatment for asthma/reactive airwaydisease. Patients were counseled regarding the common postoperative ex-perience, anticipated hospitalization period, and criteria and conditions fordischarge. All patients were agreeable to this approach.

Patients were electively admitted for same-day surgery approximately2 h prior to anticipated anesthetic induction. Preoperative parenteral met-oclopramide (Reglan) was administered as prophylaxis against aspiration.In the operating room, all patients received a standard combination ofagents as preemptive analgesia (PEA), after anesthetic induction. All wereadministered a total of 50 ml of bupivicaine (Marcaine) with epinephrine,a long-acting local anesthetic, at the five pre-marked port sites, by theoperating surgeon. Patients also received a preincisional dose of 30 mg ofparenteral ketorolac (Toradol), a nonsteroidal antiinflammatory drug(NSAID) that has shown analgesic effects comparable to that of commonlyused doses of narcotics. This was followed in most cases by another iden-tical dose at the time of fascial closure. Adults greater than 65 years of agereceived half of this dose.

Anesthetic technique was tailored to minimize immediate postoperativeanesthetic side effects Propofol (Diprivan) was used as the induction agent,in contrast to barbiturates, which have some nausea-inducing properties.Isoflurane (Forane) was used, without nitrous oxide, for maintenance ofanesthetic depth. Fentanyl (Sublimaze), a short-acting parenteral narcotic,was selectively used to complement the inhalation agent, but in minimaldoses. Intermediate-acting neuromuscular relaxants such as vecuronium(Norcuron) were utilized in order to avoid the use of neuromuscular re-versal regimens and their autonomic side effects. An orogastric tube wasutilized in the first half of the procedure only, and it was not replaced afterconstruction of the fundoplication. Urinary catheters were not utilized.

The procedure was performed with the patient in modified lithotomy,reverse Trendelenburg position. A standard five-puncture technique wasused, typically with 10–12-mm ports. In 51 patients, a (360°) sutured

Nissen-style fundoplication was created, 2.0 cm long. In 10 patients, apartial (270°) modified Toupet-style fundoplication was created using in-terrupted sutures and Teflon felt pledgets. The fundoplications were con-structed over a 60-French (Maloney) dilator. In all instances, the dilatorswere placed by the assisting surgeon under strict video observation. Theshort gastric vessels were divided by either laparoscopic intestinal staplingdevices or by use of an ultrasonic scalpel. Crural closure was routinelyperformed. Fascia was routinely closed at 10- and 12-mm sites. An attemptwas made to evacuate all CO2 at the conclusion of the procedure.

Additional planned procedures were performed as medically or tech-nically indicated. Seven patients, with histories of prior upper laparoto-mies, underwent adhesiolysis/enterolysis to allow exposure of the left up-per quadrant. One of these patients had previously undergone an (open)Nissen fundoplication, which had failed. Two patients underwent synchro-nous cholecystectomy. One patient each underwent paraesophageal herniarepair with prosthetic mesh and incisional hernia repair.

In the recovery room, standard monitoring and techniques were uti-lized. Parenteral narcotics and antiemetics were used as needed under thedirection of the supervising anesthesiologist. Once directed to the postop-erative observation unit, patients were offered liquids and soft solids bymouth. Analgesics were provided, when needed, in the form of parenteralketorolac and/or oral hydrocodone or oxycodone. Once diet and oral an-algesic tolerance were demonstrated, patients were required to meet stan-dard criteria prior to consideration for discharge. Discharge criteria areitemized in Table 1. Patients were routinely contacted by telephone on theday after operation by a registered nurse experienced in perioperative care.Patients were routinely seen back in the office within 10 days.

Results

Of the 59 patients who were considered ambulatory candi-dates at the outset of the procedure, two were admitted tohospital after operation for technical reasons. One suffereda splenic capsular tear, which required additional hemo-static maneuvers. The other suffered an esophageal tearfrom passage of the Maloney dilator. This patient had ahistory of prior stricture and dilatation, which may havecontributed to this problem. Both problems were correctedlaparoscopically, and both patients were discharged un-eventfully on the following day. No other complicationsoccurred. No patients were converted to laparotomy. Nodifficulties with hemostasis were ascribed to the use of ke-torolac. Mean operating time for all 61 patients was 87 min(1 h, 27 min), ranging from 53 to 160 min.

Of the 57 patients who were directed to the postopera-tive observation unit, 54 (95%) successfully met dischargecriteria that date and left hospital at a median interval of 290min (4 h, 50 min) after completion of operation (range140–607 min). In this group, 21 patients (39%) required noadditional parenteral narcotic after leaving the operatingroom. An additional 24 patients (44%) required 1.0 mg or

Fig. 2. Body Mass Index distribution of the same 61 patients.

Fig. 1. Age distribution of 61 consecutive patients undergoing laparoscop-ic fundoplication.

Table 1. Standard ambulatory surgery discharge criteria at Kaiser Foun-dation Medical Center, San Diego

Medical:Alert and orientedVital signs stableNo evidence of active bleedingAmbulation without nausea or dizzynessTolerating oral fluids wellFree of excessive painAble to voidSocial:Escort available to transport patient to homeHome care instructions explained, copy givenPatient/family verbalized understanding of home care instructions

1151

less of parenteral hydromorphone (Dilaudid), which wasadministered in the recovery room. Only 12 patients (22%)requested antiemetic agents while in the recovery room.Their complaints of nausea did not recur in the observationarea, prior to discharge. Three patients failed to meet dis-charge criteria, all due to complaints of unresolved nauseaand inadequate pain control. One of these patients, a 50-year-old man, also had initial urinary retention, which re-solved after a single catheterization. All three patients re-quired additional doses of both ketorolac and Dilaudid foradequate analgesic effect. All three were improved and ableto be discharged on the following day. Patients who failedto meet discharge criteria did not differ from those who didin regard to length of operation, age, obesity, or extent ofprocedure (fundoplication alone vs fundoplication with ad-ditional procedures). No patients required readmission aftersuccessfully meeting discharge criteria. Only one patient, a56-year-old man, returned to office or emergency room forunanticipated postoperative problems during the follow-upperiod, this being due to delayed presentation of urinaryretention. At scheduled clinic follow-up, no patients ex-pressed any dissatisfaction with the conduct of their post-operative care or their readiness for discharge.

Discussion

Many series of LF have recently been published, attesting tothe popularity of this approach. Excellent records of safetyand efficacy have been established, paralleling that of theopen procedure. Typically, however, little detail is providedregarding analgesic or anesthetic methods or dietary pro-gression. As a result, it is unclear why LF patients havesignificantly longer hospital stays than other laparoscopicprocedures currently performed on an ambulatory basis,such as cholecystectomy.

In our own series of LF, dating to 1993, early cases weremanaged with emphasis on those mechanical aspects ofpostoperative care that might minimize the potential fornausea, retching, and/or gastric distension. As a conse-quence, patients were subjected to a mandatory period ofnasogastric tube decompression and bowel rest. These mea-sures were largely ineffective, however, in prevention ortreatment of complaints of nausea. As a result, neuroleptic-class antiemetics were commonly prescribed, which thencontributed to sedation and lethargy. In contrast, during thissame period, it was observed that nausea and failure ofdietary tolerance were rare in those patients who had post-operative analgesia with parenteral ketorolac rather than tra-ditional parenteral narcotics. This suggested that medicationside effects, rather than ileus or gastroparesis, contributed tothese complaints, which is consistent with the known side-effect profiles of the two respective classes of analgesic(NSAID vs opiate). Additionally, patients who had receivedpreincisional ketorolac required less total analgesic thanthose who received it after operation was complete, sug-gesting what has been termed a preemptive effect [7].

Preemptive analgesia is a concept that has not yet gainedwidespread clinical acceptance. There is ample laboratoryevidence to show that noxious stimuli, even when experi-enced under general anesthetic, create alterations in periph-eral and spinal cord pathways that heighten the sensitivity ofthese channels to pain [8]. If these stimuli are blocked, thesubsequent pain experienced when conscious may be less-ened. Ketorolac and bupivicaine appear to be ideal agentsfor PEA in an ambulatory setting, since the former hassystemic efficacy comparable to potent narcotics, but withlessened propensity for nausea, and both have durations ofaction sufficient to cover the time from incision to postop-erative observation unit. Ketorolac has been shown to haveclinically measurable preemptive analgesic effect in pro-spective studies on both total hip replacement [2] and hys-terectomy patients [5]. Similarly, the use of preincisional vspostincisional bupivicaine has been shown to lessen earlypostoperative analgesic requirements in pediatric hernia pa-tients [1].

Once ketorolac/bupivicaine PEA was adopted as ourstandardized technique for pain management, the rarity ofnausea led to the abandonment of postoperative nasogastrictubes and progressively earlier feeding. The final step in thetransition from overnight hospitalization to true ambulatorystatus was minimizing both length of recovery and sideeffects from anesthesia, particularly within the first 6 h afterthe operation concluded. We empirically selected a schemethat minimizes or excludes those agents with prolonged,emetogenic and/or adverse autonomic activities. The result-ing series of patients shows consistently shorter LOS thanpreviously reported series.

We believe that this combination of preoperative coun-seling, ketorolac-bupivicaine PEA, and a tailored anestheticmethod is a simple, effective, and reproducible technique.The resulting improvement in patient comfort and func-tional status has led to a significant reduction in hospitalstay for laparoscopic fundoplication.

References

1. Dahl V, Raeder JC, Erno PE, Kovdal A (1996) Pre-emptive effect ofpre-incisional versus post-incisional infiltration of local anesthesia onchildren undergoing hernioplasty. Acta Anesth Scand 40: 847–851

2. Fletcher D, Zetlaoui P, Monin S, Bombart M, Samii K (1995) Influenceof timing on the analgesic effect of intravenous ketorolac after ortho-pedic surgery. Pain 61: 291–297

3. Hinder RA, Filipi CJ, Wetscher G, Neary P, DeMeester TR, Perdikis G(1994) Laparoscopic Nissen fundoplication is an effective treatment forgastroesophageal reflux disease. Ann Surg 220: 472–483

4. McKernan JB, Champion JK (1995) Laparoscopic antireflux surgery.Am Surg 61: 530–536

5. Parke TJ, Lowson SM, Uncles DR, Daugherty MO, Sitzman BT (1995)Pre-emptive versus post-surgical administration of ketorolac for hys-terectomy. Eur J Anaesth 12: 549–553

6. Peters JH, Heimbucher J, Kauer WKH, Incarbone R, Bremmer, De-Meester TR (1995) Clinical and physiologic comparison of laparoscop-ic and open Nissen fundoplication. J Am Coll Surg 180: 385–392

7. Wall PD (1988) The prevention of postoperative pain. Pain 33: 289–2908. Woolf CJ (1989) Recent advances in the pathophysiology of acute pain.

Br J Anesth 63: 139–146

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Editorial

Day-case (ambulatory) laparoscopic surgery

Let us sing from the same hymn sheet

This issue ofSurgical Endoscopycontains three reports onambulatory laparoscopic surgery: two on laparoscopic cho-lecystectomy and one on laparoscopic fundoplication. Therehave been a number of reports on ambulatory LC with themajority verdict based on these reports, including the twopublished in the current issue, being in favor of same-daydischarge for the majority of patients [1–6]. The substantialreduction in hospital charges is self-evident. The seminalquestion centers on the safety of such an approach, espe-cially if careful selection of patients for ambulatory care isnot practiced. A minority has been criticized [7] for advisingcaution against outpatient cholecystectomy on the sensiblebut unproven assumption that day-case discharge will in-evitably lead to occasional delays in the diagnosis and man-agement of postoperative complications [8].

The report on ambulatory laparoscopic fundoplication isthe first of its kind and merits special consideration [9].Although there can be no argument about the substantialsavings from the widespread practice of ambulatory lapa-roscopic surgery, we shall never be able to document itssafety unless we conduct and participate in prospective ran-domized studies comparing day-case laparoscopic surgeryversus short stay (overnight) practice. There are also certainconsiderations that require clarification and agreement forus to ensure that in addressing this important change insurgical practice, we are singing from the same hymn sheet.

Nomenclature

One has to raise this issue even at the risk of soundingpedantic.Ambulatory surgery, day-case surgery,and out-patient surgeryare terms used synonymously on both sidesof the Atlantic. By definition, certainly in the NationalHealth Service in the United Kingdom, the terms mean thatthe patient is discharged during the same day. This is notequivalent to a stay of less than 24 hours in a hospital. Thusif a patient has an operation (laparoscopic or otherwise) onthe afternoon of a certain day and is discharged next morn-ing (well within 24 hours), the overnight stay excludes thepatient from being categorized as an ambulatory, day-case,or outpatient. It is obvious from at least two of the reportsin the current issue and others reported previously that thisstandard definition of ambulatory (day-case) care is not ad-hered to, and indeed, one report specifically refers to ‘‘dis-

charge in 24 hours.’’ Perhaps future reports on the subjectshould specifically indicate the patients who for any reasonrequired an overnight stay in the hospital.

Anaesthesia/gasless techniques

Many surgeons may not be fully aware of the need forspecialized anaesthetic techniques and the importance ofpreemptive analgesia (PEA), particularly in the preventionof postoperative nausea and vomiting that have been devel-oped for day-case surgery. In this and other respects, thereport by Milford and Paluch on ‘‘Ambulatory Laparoscop-ic Fundoplication’’ [9] is both instructive and exemplary.There is good evidence, which is strengthened by this re-port, that avoidance of opiate administration by PEA virtu-ally abolishes the postoperative complaints of nausea andvomiting that preclude oral intake of fluids soon after theoperation. There is, however, a need for standardization ofboth anaesthetic and preemptive analgesic techniques usedfor ambulatory laparoscopic surgery and perhaps theE.A.E.S. and SAGES ought to set up a consensus confer-ence on this subject with active involvement of expert an-aesthesiologists. My impression on reading the literature onthe subject is that various techniques are used in differentinstitutions. Gasless and abdominal wall lift techniqueshave been shown to reduce postoperative nausea and vom-iting and CO2 narcosis [10, 11]. This approach merits seri-ous consideration.

Selection of patients

Some surgeons believe that comorbid disease, old age, andphysical status do not preclude safe ambulatory surgery.This assumption is largely based on retrospective reportsthat ignore the precise definition of day-case (ambulatory)surgery. There is no doubt, at least in my mind, that thesehigher-risk patients require a longer period of observationafter their surgery. Indeed, many can often be dischargedearly after an overnight stay and within 24 hours, but, bydefinition, this is not ambulatory surgery. Patients’ relatedfactors go beyond comorbid factors and old age, and includehome support, distance and access between the patient’shome and the hospital, personality type, and regional envi-ronment. Day-case discharge of an otherwise fit patient who

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lives alone in a region where the winters are harsh, the daysare short, and the roads are often impassable after heavysnowfalls cannot be regarded as an exercise of good clinicaljudgment. Perhaps colleagues who live and practice inwarmer and kinder environments never encounter this situ-ation; they are blessed even though they may not be awareof it.

Ambulatory discharge criteria

The standard ambulatory discharge medical and social cri-teria at the Kaiser Foundation Medical Center, San Diego,quoted in the article by Milford and Paluch, seem fine but,in my view, require fine tuning. It is not clear from this andother reports as to who is responsible (by documented sig-nature) for the ambulatory discharge of these patients whenall these criteria are met. ‘‘Free of excessive pain’’ worriesme as being insufficiently precise and the legal professionwould have a field day in the event of an adverse outcome.A more objective assessment based on a linear analoguescale should be agreed upon.

Follow-up

If surgeons are convinced that patients can be dischargedsafely as day cases after laparoscopic surgery, and the vastmajority of patients obviously do well at considerable costsavings to the hospital, why is it necessary that they are allseen at the office ten days later? The point is that if we areto change drastically our surgical practice, why should wenot also consider changes in the follow-up policy, especiallyin this digital age with unsurpassed means of efficient, in-

expensive, and real time communication between patientand surgeon or his staff?

References

1. Arregui ME, Davis CI, Arkush A, Nagan RF (1991) In selected pa-tients outpatient cholecystectomy is safe and significantly reduces hos-pitalization charges. Surg Laprosc Endosc 1: 240–245

2. Reddick EJ (1992) Laparoscopic cholecystectomy in free-standingoutpatient centres. J Laparoendosc 2: 65–67

3. Llorente J (1992) Laparoscopic cholecystectomy in the ambulatorysetting. J Laparoendosc 2: 23–26

4. Voitk AJ (1996) Routine outpatient laparoscopic cholecystectomy.Can J Surg 6: 262–265

5. Hargreaves R (1996) Is outpatient laparoscopic cholecystectomy wise?(letter) Surg Endosc 10: 950

6. Saunders CJ, Leary BF, Wolfe BM (1995) Is outpatient laparoscopiccholecystectomy safe? Surg Endosc 9: 1263–1268

7. Voyles R, Berch BR (1997) Selection criteria for laparoscopic chole-cystectomy in an ambulatory care setting. Surg Endosc 11: 1145–1146

8. Voitk AJ (1997) Is outpatient cholecystectomy safe for the higher-riskelective patient? Surg Endosc 11: 1147–1149

9. Milford MA, Paluch TA (1997) Ambulatory laparoscopic fundoplica-tion. Surg Endosc 11: 1150–1152

10. Koivusalo A-M, Kellokumpu I, Lindgren L (1997) Postoperativedrowsiness and emetic sequelae correlate to total amount of carbondioxide during laparoscopic cholecystectomy. Surg Endosc 11: 42–44

11. Koivusalo A-M, Kellokumpu I, Lindgren L (1996) Gasless laparo-scopic cholecystectomy: comparison of postoperative recovery withconventional technique. Br J Anaesth 77: 576–580

A. Cuschieri

Department of SurgeryNinewells Hospital and Medical SchoolDundee DD1 9SY, UK

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Laparoscopic vs open hernioplasty

Which open technique for a correct comparison of outcomes?

We read with interest the article by J. Tschudi et al. entitled‘‘Controlled multicenter trial of laparoscopic transabdomi-nal preperitoneal hernioplasty vs Shouldice herniorrhaphy:Early Results,’’ published in the August 1996 issue ofSur-gical Endoscopy[13].

Patients treated by the open technique left the hospitallater (6.3 vs 4.9 days), had more postoperative complica-tions (26 vs 16%), and had double the rate of recurrence (4.6vs 2.3%) experienced by patients treated by laparoscopy.Moreover, the open technique caused more postoperativepain and more delayed return to full work and usual activi-ties.

If the main aim of the authors was to demonstrate thesuperiority of laparoscopic transabdominal preperitonealhernioplasty (LTAPPH) compared to the Shouldice herni-orrhaphy, we do believe that they reached their goal, sup-ported by the same conclusion reached by other similarrandomized studies [6, 11].

If, on the other hand, the aim was to demonstrate thesuperiority of LTAPPH compared to ‘‘open’’ hernioplasty,we do not agree with the authors. We do think that it is notcorrect at all to compare LTAPPH to an open repair such asthe Shouldice technique. Relying solely on the traditionalopen techniques, the advocates of laparoscopic hernia repairconcluded that this offers a better outcome (less postopera-tive pain, shorter recovery period, and lower recurrencerate) [2]. This comparison is not appropriate, a more suit-able approach to the problem being to compare it to a mod-ern, tension-free and prosthetic repair such as the Lichten-stein repair [1], the Gilbert sutureless technique [5], and theRutkow-Robbins mesh-plug repair [9]. The results of thesetechniques are significantly better than those recorded in arecent multicenter trial on LTAPPH [4]—namely, a loweroverall rate of complications, a lower rate of postoperativeadmissions, a lower rate of recurrence, and lower costs.Recently, a prospective randomized trial demonstrated thesuperiority of open plug repairs (Gilbert and Rutkow-Robbins) compared to LTAPPH [3]. Actually, the lattertook longer operative time, required more postoperative ad-missions, showed the same rate and length of postoperativepain/discomfort, and was more expensive than the former.Patients undergoing LTAPPH returned to full work 4 dayssooner than did patients submitted to open repair, but bothgroups were unusually quick to resume normal workingactivities compared to the commonly held notion of a 4-week recuperation for hernia repair. The evidence that

LTAPPH enables patients to return earlier to work couldappear more theorethical than actual when comparing itwith tension-free open repairs. Moreover, determinants ofreturn to work are strongly subjective and influenced by theattitudes of patients, surgeons, and general practitioners. Forexample, in a recently reported randomized single-blindcomparison of laparoscopic vs small-incision open chole-cystectomy, in which patients were left free to decide theirown time off-work, all the patients returned to work at thesame time [7].

We are not surprised at all that LTAPPH induced lesspain than the Shouldice technique in the study by Tschudi etal. This appears quite obvious when the comparison is madewith techniques under tension with division of the hernialsac, because such maneuvers are the main determinants ofpostoperative pain [10]. Moreover, the degree of postopera-tive pain is very difficult to measure, and current criteria(postoperative consumption of analgesics, visual analoguescales, time off-work) appear unsufficient to cover the tre-mendous variations among different subjects. Anyway, inour personal series of about 700 open tension-free herniarepairs, only few patients required a mild analgesic duringthe first 10 postoperative h, prolonged administration hav-ing been anedoctal.

In any case, less pain and more rapid resumption ofworking activities cannot overcome the disadvantages ofLTAPPH: the need for general anesthesia, higher rate ofpostoperative complications, especially major ones, longerand difficult training, higher costs. Concerning laparoscopichernia repair, on one hand, Rutkow [8] stated that ‘‘simplybecause an operation can be done laparoscopically does notmean that is necessarily the most expedient method.’’ Onthe other hand, Swanstrom [12] recently concluded that‘‘laparoscopic repair can be emphasized for bilateral her-nias, recurrent hernias and, rarely, for patients undergoingunilateral, first-time hernia repairs who absolutely must re-sume normal activity at the earliest possible moment.’’ Wedo agree that there is a place for laparoscopic hernioplastyin the treatment of groin hernia, but its indications should bedetermined by a careful and controlled comparison withprosthetic tension-free open hernioplasty.

References

1. Amid PK, Shulman AG, Lichtenstein IL (1993) Critical scrutiny of theopen ‘‘tension-free’’ hernioplasty. Am J Surg 165: 369–371

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2. Amid PK, Shulman AG, Lichtenstein IL (1994) A critical comparisonof laparoscopic hernia repair with Lichtenstein tension-free hernio-plasty. Med J Aust 161: 239–240

3. Brooks DC (1994) A prospective comparison of laparoscopic andtension-free open herniorraphy. Arch Surg 129: 361–366

4. Fitzgibbons RJ, Camps J, Cornet DA (1995) Laparoscopic inguinalherniorrhaphy. Results of multicenter trial. Ann Surg 221: 3–13

5. Gilbert AI (1992) Sutureless repair of inguinal hernia. Am J Surg 163:331–335

6. Maddern JG, Rudkin G, Bessel JR, Devitt P, Ponte L (1994) A com-parison of laparoscopic and open hernia repair as a day surgical pro-cedure. Surg Endosc 8: 1404–1408

7. Majeed AW, Troy G, Nicholl JP, Smythe A, Reed MWR, Peacock J,Johnson AG (1996) Randomized prospective single-blind comparisonof laparoscopic versus small-incision cholecystectomy. Lancet 347:989–994

8. Rutkow IM (1995) Open tension-free mesh plug versus laparoscopicherniorrhaphy: economic practicalities. Prog Surg 21: 105–112

9. Rutkow IM, Robbins AW (1995) Mesh plug hernia repair: a follow upreport. Surgery 117: 597–598

10. Smedberg SGC, Broome´ AEA, Gullmo A (1984) Ligation of the her-nial sac? Surg Clin North Am 64: 299–306

11. Stoker DL, Spiegel H, Alter DJ, Singh R, Wellwood JM (1994) Lap-aroscopic versus open inguinal hernia repair: randomised prospectivetrial. Lancet 343: 1243–1245

12. Swanstrom LL (1996) Laparoscopic herniorrhaphy. Surg Clin NorthAm 76: 483–491

13. Tschudi J, Wagner M, Klaiber CH, et al (1996) Controlled multicentertrial of laparoscopic transabdominal preperitoneal hernioplasty vsShouldice herniorrhaphy. Early results. Surg Endosc 10: 845–847

P. NegroF. GossettiM. Catarci

2nd Surgical Clinic, University of Rome ‘‘La Sapienza’’and Hernia Center of RomeV.le del Policlinico, 15500161 RomeItaly

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The author replies

We thank Dr. Zornig, Hamburg, Germany, for his interest inour recent article. The following topics were addressed inhis letter.

First he criticizes us in the laparoscopic procedures forneglecting local ulcer excision and describes that as a com-promise of surgical standard. Regarding this point, we haveto admit that the paper inSurgical Endoscopyreally reflectsour initial experience with laparoscopic ulcer closure. At thevery beginning we were not yet able to completely excise anulcer and close the duodenal wall. Today in 1997 this tech-nique would of course be feasible; still, we would performonly simple closure of the ulcer today.

The next topic addresses the problem of carbon dioxidepneumoperitoneum in patients with severe peritonitis andlong interval between onset of peritonitis and treatment.Unfortunately, in our cases we are not able to document theexact time spent between the onset of peritonitis and surgi-cal intervention. However, the concerns which are utteredby Dr. Zornig do not seem to translate into a clinical dis-advantage for the patient.

In their study (Surg. Endosc.1995;9:898–901) Bo¨chleand Zornig show that in rats a pneumoperitoneum aggra-vates the extent and severity of peritonitis when the intervalbetween ulcer perforation and pneumoperitoneum is longerthan 12 h. On the other hand, Gurtner (British Journal ofSurgery1995;82:844–848) could not prove an adverse de-fect of carbon dioxide pneumoperitoneum on bacteremia

and endotoxemia in a rabbit model. Parallel to the latterfindings, clinically relevant disadvantages for the patientshave, to our mind, not yet been proven.

The distribution of patients to the treatment groups wasalso addressed. Of course, the intention to treat principle hasto be followed. However, our number of patients was rathersmall, so we put the three conversion patients the conven-tional closure group. On the other hand, when these patientswere calculated in the laparoscopic group (as was done inthe paper), the rate of uncomplicated causes dropped to 43%of the patients (page 832).

We agree with the authors that further sound experimen-tal and clinical data focusing on the risk of laparoscopicmanagement of peritonitis are needed. However, a furtherimportant piece of evidence has been collected by the studyof Lau and others in theAnnals of Surgery(1996;224:131–138). The authors report findings similar to those we haveshown in our preliminary paper inSurgical Endoscopy.

E. Eypasch

2nd Department of SurgeryUniversity of CologneOstmerheimer Strabe 20051109 KolnGermany

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First trimester of pregnancy laparoscopic procedures

B. S. Schwartzberg, J. A. Conyers, J. A. Moore

Department of Surgery, Rose Medical Center, 4500 East 9th Avenue, Suite 710, Denver, CO 80220, USA

Received: 25 March 1996/Accepted: 24 January 1997

Abstract. Laparoscopic procedures are being performedduring pregnancy with increasing frequency; however, fewfirst-trimester operations have been published. Two first-trimester procedures are here reported, both performed withuneventful recoveries.

Key words: Laparoscopy — Pregnancy — Appendectomy— Cholecystectomy — Twins

First-trimester pregnancy laparoscopic procedures remaincontroversial due to the potential impact of carbon dioxidepneumoperitoneum on fetal organogenesis. Traditionalfirst-trimester open procedures are, however, associatedwith a fetal loss of 1.1% with appendectomy [7] and 12%with cholecystectomy [3]. Initial first-trimester laparoscopicreports have been encouraging [2, 4, 5, 8]. The operationshave been successfully accomplished without fetal loss andsubsequent delivery of healthy normal infants. We wouldlike to present two first-trimester cases, an appendectomyand cholecystectomy, the second involving a twin preg-nancy.

Case reports

Case report I

A 30-year-old woman (gravida 3, para 1, abortus 1) presented at 8 weeksof gestation with sudden acute right lower quadrant pain. Her medicalhistory was pertinent for recurrent symptomatic Crohn’s disease. Physicalexamination revealed a temperature of 99.0°F and significant localizedabdominal pain. WBC was 4,600/mm3. Appendicitis was the primary pre-operative diagnosis. Surgical options were discussed. These included eithera standard open surgical approach with known organogenesis anestheticrisk and a 2% risk of fetal loss, or a laparoscopic approach which could

provide a more complete diagnostic evaluation, treatment, and quickerrecovery, but with less known risk of organogenesis and fetal loss as aresult of carbon dioxide pneumoperitoneum. Informed consent was ob-tained for laparoscopy. ASA class was 3E. Cefotetan was given as antibi-otic prophylaxis. Sequential compression stockings were placed. Laparos-copy was initiated following general endotracheal anesthesia (GETA) us-ing propofol, succinylcholine, fentanyl, mivacurium, and isoflurane. AHassan port was placed with an open cutdown technique due to previousabdominal procedures. Pneumoperitoneum was maintained with carbondioxide for an average intraabdominal pressure of 15 mmHg and an end-tidal carbon dioxide of 28–33 mmHg. O2 saturation was 96–99%. Arterialgases were not obtained. Laparoscopy revealed a recent right ovarian cystrupture. Active Crohn’s disease was not noted. The appendix was removedvia a suprapubic port placed under direct vision. It was normal on finalpathology. The procedure lasted 1 h. Transvaginal ultrasound fetal evalu-ation performed preoperatively and 48 h postoperatively documented acontinued viable intrauterine pregnancy. Droperidol, ketorolac, morphine,and acetaminophen were given in the initial postoperative period. Thepatient was transitioned to oral oxycodone and hydrocodone. The patientwas discharged on the 1st postoperative day. She had an uneventful preg-nancy and delivered at 37 weeks’ gestation by elective cesarean section.The baby was healthy, weighing 7 lb 0 oz and having Apgar scores of 7 at1 min and 9 at 5 min. Mother and child enjoy good health.

Case report II

A 31-year-old woman (gravida 6, para 3, abortus 2) was referred at 8.5weeks’ gestation with symptomatic cholelithiasis. This was causing nauseaand weight loss, threatening her twin pregnancy. She was afebrile withonly minimal right upper quadrant pain. Laboratory values were normal.Multiple gallstones were documented by ultrasound. Informed consentincluded discussion of open surgical technique, with known anesthetic riskand 10% risk of fetal loss, or a laparoscopic approach with benefits of ashort procedure and quick recovery but with less known risk of effect ofcarbon dioxide pneumoperitoneum on organogenesis or fetal loss. ASAclass was 3, cefotetan was administered, and pneumatic stockings wereplaced preoperatively. GETA was initiated using fentanyl, thiopental, atra-curium and isoflurane. Laparoscopic cholecystectomy was performed us-ing a Veress needle to create a pneumoperitoneum (average insufflation—12 mmHg, O2 saturation 96–99%; average endtidal CO2—30 mmHg).Arterial gases were not obtained. A cholangiogram was not performed asthe biliary anatomy was straightforward; the procedure took 0.5 h. Post-operative medications were droperidol, demerol, and hydrocodone. Preop-erative and 48-h postoperative transvaginal ultrasound fetal evaluation wasunremarkable. The patient was discharged on the 2nd postoperative day;her appetite improved and she gained 30 lb over the next 23 weeks. Anemergency cesarean section was performed at 31 weeks’ gestation for ableeding placenta previa. Twin ‘‘A’’ was born weighing 3 lb 15 oz and hadApgar scores of 7 at 1 min and 8 at 5 min. He required ventilator support

Presented at the 5th World Congress of Endoscopic Surgery of the Societyof American Gastrointestinal Endoscopic Surgeons (SAGES), Philadel-phia, Pennsylvania, USA, 13–17 March 1996Correspondence to:B. S. Schwartzberg

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for 1 week following delivery. Twin ‘‘B,’’ weighing 4 lb 0 oz, had Apgarscores of 7 at 1 min and 8 at 5 min and needed continuous positive airwaypressure after birth. All are now well.

Discussion

Pregnancy is no longer considered an absolute contraindi-cation to laparoscopic procedures. Laparoscopy is now be-ing used cautiously for nonobstetrical emergent and urgentindications despite potential adverse complications. Al-though most frequently performed in the second trimester,first-trimester-pregnancy operations have been reported.First-trimester gynecologic procedures have included treat-ment of adnexal torsion [5], and treatment of an ectopicpregnancy complicating a concomitant intrauterine one (B.Albrecht, personal communication). Laparoscopy was alsoused to diagnose appendicitis in first-trimester patients [8].Open appendectomies were then successfully performed. Afirst-trimester laparoscopic appendectomy is now being de-scribed. Three cases of first-trimester laparoscopic chole-cystectomies have been published, including one success-fully treating acute cholecystitis [2, 4, 6]. Increased fetalloss has been reported following nonobstetric second- andthird-trimester laparascopic procedures [1]. Abnormal fetalorganogenesis has not been observed.

Most surgeons employed a Veress needle for first-trimester insufflation. Intraoperative fetal monitoring wasnot performed during the first trimester, although transvagi-nal ultrasound fetal heart monitoring could be used afterapproximately 8 weeks’ gestation. End-tidal carbon dioxidemeasurements were used to monitor maternal, and therebyindirectly fetal, carbon dioxide levels during each proce-dure. More precise arterial gas monitoring was not utilized.

The abnormal fetal heart rhythms and excessive maternalend-tidal carbon dioxide levels which would mandate lap-aroscopic procedure termination have yet to be determined.

During the first trimester of pregnancy laparoscopic pro-cedures may have undetermined complications; however,most initial case reports reveal safe outcome. Long-termsafety needs to be established. Further study should includeboth experimental animal models to better understand thefetal physiologic effects of laparoscopy and formation of alaparoscopy-in-pregnancy registry.

References

1. Amos JD, Schorr SJ, Norman PF, Poole GV, Thomae KR, MancinoAT, Hall TJ, Scott-Conner CEH (1996) Laparoscopic surgery duringpregnancy. Am J Surg 171: 435–437

2. Chandra M, Shapiro SJ, Gordan LA (1994) Laparoscopic cholecys-tectomy in the first trimester pregnancy. Surg Laparosc Endosc 4:68–69

3. Curet MJ, Allen D, Josloff RK, Pitcher DE, Curet LB, Miscall BG,Zucher KA (1996) Laparoscopy during pregnancy. Arch Surg 131:546–551

4. Elerding SC (1993) Laparoscopic cholecystectomy in pregnancy. AmJ Surg 165: 625–627

5. Garzarelli S, Mazuca N (1994) One laparoscopic puncture for treat-ment of ovarian cysts with adnexal torsion in early pregnancy. A reportof two cases. J Reprod Med 39: 985–986

6. Hart RO, Tamadon A, Fitzgibbons RJ, Fleming A (1993) Open lapa-roscopic cholecystectomy in pregnancy. Surg Laparosc Endosc 3: 13–16

7. Mazze RI, Kallen B (1991) Appendectomy during pregnancy: a Swed-ish registry study of 778 cases. Obstet Gynecol 77: 835–840

8. Spirtos NM, Eisenkop SM, Spirtos TW, Poliakin RI, Hibbard LT(1987) Laparoscopy—a diagnostic aid in cases of suspected appendi-citis. Its use in women of reproductive age. Am J Obstet Gynecol 156:9000–9094

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Laparoscopic cecal ligation and puncture in the rat

Surgical technique and preliminary results

R. Berguer,1 A. Alarcon,2 S. Feng,1 C. Gutt3

1 Department of Surgery, University of California Davis Medical Center, 4301 X. Street, Room 2310, Sacramento, CA 85917, USA2 Central University of Ecuador, Calle Sodiro y 12 de Octubre, Quito, Ecuador3 Johann-Wolfgang-Goethe Universitat Frankfurt, Theodor-Stern-Kai 7, 60590 Frankfurt, Germany

Received: 3 July 1996/Accepted: 7 January 1997

AbstractBackground:We describe a technique of laparoscopic cecalligation and puncture (CLP) in the rat analogous to openCLP which may facilitate the study of minimally invasivesurgery (MIS) and peritonitis.Methods:Forty-four rats were randomized to either laparo-scopic or open CLP and their 3-day mortality was recorded.Autopsies were performed for peritoneal fluid cultures,measurement of the length of ligated cecum, and scoring ofthe degree of cecal necrosis.Results:Laparoscopic CLP required slightly longer operat-ing times compared to open CLP (average 15.6 vs 13.1 min,p 4 0.002). Three-day postoperative mortality was 36.4%and 22.7% for open and laparoscopic CLP, respectively (p4 NS). There were no differences in the length of ligatedcecum or the cecal necrosis score between the open andlaparoscopic CLP groups.Conclusion:Laparoscopic CLP is feasible and produces afecal peritonitis with similar characteristics to those of tra-ditional open CLP.

Key words: Laparoscopy — Cecal ligation and puncture —Peritonitis — Rats

The application of minimally invasive surgery (MIS) tech-niques to a wide variety of operations has demonstrated thatthis technique causes less postoperative pain, a more rapidrecovery [1, 12], and possibly less stress-induced postop-erative immune impairment than open surgery [2, 5, 8, 13,14], although the evidence for the latter remains controver-sial [11]. The study of potential benefits of MIS in thetreatment peritonitis as well as the understanding of the hostreaction to visceral perforation at the time of laparoscopy

would be facilitated by the development of a good MISanimal model of peritonitis.

Cecal ligation and puncture (CLP) is a simple andwidely used model of severe peritonitis [11, 15]. We haveadapted the technique of open CLP to our rat model oflaparoscopic surgery [3, 4] and herein report our prelimi-nary results with this technique.

Methods

The research protocol was approved by the Animal Care and Use Com-mittee at the University of California Davis. Male Lewis rats weighing250–300 g (Charles River Laboratories) were housed individually in plasticcages and fed standard rat chow. Rats were not fasted prior to CLP so asto maintain the maximum amount of stool in the gastrointestinal tract.Following CLP rats were given ad lib water and rat chow. No antibioticsor pain medications were administered to avoid confounding effects onimmune function. Animals who died during the first 3 postoperative dayswere stored at 20°C in plastic bags until necropsy on day 4. On postop-erative day 4 all surviving animals were euthanized by CO2 inhalation perAALAC guidelines and necropsies were performed on all animals. Atnecropsy, the peritoneal cavity was examined and the gross appearance ofthe cecum was graded as Normal, Red, or Black/gray (author’s classifica-tion). In order to assess the adequacy of the laparoscopic placement of thececal ligature, the distance from this ligature to the tip of the necroticcecum was measured in all animals. In animals that survived to postop-erative day 4, necropsy also included a swab of peritoneal fluid for aerobicand anaerobic culture.

Rats were anesthetized with 1.5–2.0% isoflurane and 50% nitrous ox-ide at gas flow rates of 2 l/min via tight-fitting masks in order to providerapid induction and reversal of anesthesia without the need for intraperi-toneal injection. The animals’ body temperature was monitored with arectal probe and maintained between 37 and 38°C during surgery with anelectric heating pad. Five ml per 100 g body weight of 0.9% saline fluidresuscitation was given subcutaneously in the neck to all animals prior toawakening.

Our laparoscopic surgical technique used a specialized small-animaloperating table (Kaps Co., Frankfurt, Germany) (Fig. 1) with an attachedflexible arm to hold the laparoscope. Rats were placed supine on theoperating table over an electric heating pad and with the head and anes-thesia mask facing the surgeon. The abdomen was shaved, sprayed with70% isopropyl alcohol, and covered with a sterile paper drape. All instru-ments were sterilized in solution and cleansed with 70% isopropyl alcohol.Correspondence to:R. Berguer

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We employed a 2.9-mm arthroscopic sheath with a blunt obturator (Dyon-ics Inc., Andover, MA) held by the flexible arm on the operating table andintroduced into the abdomen via a 2-mm subxyphoid midline abdominalpuncture. A 2.7-mm-diameter 30° wide-angle arthroscope (Dyonics Inc.)was inserted through the sheath into the peritoneal cavity and connected toa laparoscopic light source and video camera (Karl Storz Endoscopy, Ger-many) to visualize the peritoneal cavity on a 13-inch color video monitor(Sony Corp., Japan). We created a 2–3 mmHg CO2 pneumoperitoneumusing a standard laparoscopic insufflator (Karl Storz Endoscopy, Germany)connected to the side port of the arthroscopic sheath. Micro-alligator for-ceps (Weck Endoscopy, Largo, FL) were placed directly into the peritonealcavity through right and left abdominal wall punctures for dissection andknot tying. The cecum in the rat is large and easy to identify and usuallylies in the left lower abdomen with the ileocecal junction nearest thesurgeon when viewed from a cephalad direction. The ileocecal peritonealreflection is divided bluntly to free the tip of the cecum for ligation. A 3-cm4.0 silk ligature is inserted into the peritoneal cavity through the lumen ofan 18-gauge needle which is introduced and left in alongside the left-sidedforceps. The ligature is grasped from the inside with the right-sided forcepsand placed around the tip of the cecum as near to the ileocecal junction aspossible. Using two-handed intracorporeal knot-tying technique, a sur-geon’s knot and two more squared throws were used to ligate the cecum.The tip of the same 18-gauge needle is then easily used to puncture theantimesenteric surface of the cecum distal to the ligature in three differentlocations. At the end of the procedure the instruments, needle, and thearthroscope are removed and the three abdominal wall puncture sites areclosed with skin staples (Davis and Geck, Danbury, CT).

For the purpose of exact comparison 44 rats were randomized to eitherlaparoscopic CLP or open CLP. Open CLP was carried out via a 4-cmmidline incision using the same steps and instruments as described for thelaparoscopic approach. Statistical comparison of the length of ligated ce-cum and operative times was performed by Student’st-test. The compari-son of the cecal necrosis score and the number of positive peritonealcultures was performed by chi-square analysis. The survival rats for thetwo groups were compared using a Kaplan-Meier survival curve and thelog-rank test. Statistical significance was set atp < 0.05.

Results

There were no intraoperative deaths or differences in bodyweight or rectal temperature between animals undergoinglaparoscopic or open CLP. Laparoscopic CLP requiredslightly longer operating times than open CLP (average 15.6vs 13.1 min,p 4 0.002). The 3-day postoperative mortalitywas 36.4% for open CLP and 22.7% for laparoscopic CLP(Fig. 2,p 4 NS). There were no differences in the length of

ligated cecum, the cecal necrosis score, or the number ofpositive peritoneal cultures between the two groups (Table1).

Discussion

Laparoscopic surgery in the rat is gaining wider acceptanceamong MIS researchers [5–7, 10, 14]. Our animal model ofperitonitis induced by laparoscopic surgery is simple andeffective and may be most useful for the study of effects ofbowel injury at the time of laparoscopy. This model mayalso allow a comparison of the stress and immune responsesto peritonitis with and without a laparotomy incision.

Our technique is based on previously reported openmethods [15] except that we don’t milk the stool into thececum. In order to maintain uniformity of technique be-tween laparoscopic and open CLP we used the same lapa-roscopic instruments, dissection technique, and knot-tyingmethods during both procedures. The adequacy of our CLPtechnique is attested to by the similar mortality, length ofcecal ligation, and cecal necrosis score compared to openCLP.

Several technical tips may be of help to other investi-gators interested in performing laparoscopic CLP. The sur-geon needs to be careful not to cause bleeding from tearingsmall surface vessels on the cecum during the blunt divisionof the ileocecal ligament. Passing the ligating silk suturethrough the abdominal wall through a needle avoided theneed to remove an instrument to introduce the ligature dur-ing the operation and therefore the need for trocars. Bypassing the needle along the left-sided instrument weavoided an additional abdominal wall puncture and the tipof the needle remained ready for cecal puncture as soon asthe ligature was tied. There is no need to trim the ends of thesilk ligature.

Fig. 1. The small-animal laparoscopic operating table (Kaps Co., Frank-furt, Germany) allows the operator or an assistant to move the table, ratherthan the laparoscope, in order to change the surgeon’s view. Fig. 2. Kaplan-Meier survival curves for rats undergoing laparoscopic or

open cecal ligation and puncture (n 4 22 for each group). The differencesin survival between the two groups are not statistically significant by thelog-rank test. — open, ..... laparoscopy.

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References

1. (1993) National Institutes of Health consensus development confer-ence on gallstones and laparoscopic cholecystectomy. Am J Surg 165:390–396

2. Allendorf J, Kayton M, Libutti S, Trokel M, Whelan R, Treat M,Nowygrod R, Bessler M (1994) The effect of laparotomy versus in-sufflation on tumor establishment and growth. Surg Endosc 8: S38

3. Berguer R, Gutt C, Stiegmann GV (1993) Laparoscopic surgery in therat. Description of a new technique. Surg Endosc 7: 345–347

4. Berguer R, Gutt CN (1994) Laparoscopic colon surgery in a rat model:a preliminary report. Surg Endosc 8: 1195–1197

5. Bouvy ND, Marquet RL, Hamming JF, Jeekel J, Bonjer HG (1996)Laparoscopic surgery in the rat: beneficial effect on body weight andtumor take. Surg Endosc 10: 490–494

6. Crane LH, Martin L (1991)In vivo myometrial activity in the ratduring the oestrous cycle: studies with a novel technique of videolaparoscopy. Reprod Fertil Dev 3: 185–199

7. Filmar S, Gomel V, McComb PF (1987) Operative laparoscopy versusopen abdominal surgery: a comparative study on postoperative adhe-sion formation in the rat model. Fertil Steril 48: 486–489

8. Griffith J, Everitt N, Curley P, McMahon M (1993) Laparoscopicversus ‘‘open’’ cholecystectomy—reduced influence upon immunefunction and the acute phase response. Surg Endosc 7: 123

9. Johnson D, Spencer M, Cerra F, Constatidides F, Tothenberger D,Madoff R (1994) Laparoscopic versus open colectomy. A comparativestudy of the systemic stress response. Surg Endosc 8: S37

10. Kayton M, Morales A, Chen M, Treat M, Nowygrod R (1994) Lapa-roscopic surgery in the rat: a model for teaching laparoscopic suturingtechniques. Surg Endosc 8: 264

11. Martinell S, Falk A, Haglund U, Myrvold H (1985) Peritonitis andseptic shock—an evaluation of two experimental models in the rat. EurSurg Res 17: 160–166

12. Troidl H, Spangenberger W, Langen R, al-Jaziri A, Eypasch E, Neu-gebauer E, Dietrich J (1992) Laparoscopic cholecystectomy: technicalperformance, safety and patient’s benefit. Endoscopy 24: 252–261

13. Trokel M, Allendorf J, Treat M, Whelan R, Nowygrod R, Bessler M(1994) Inflammatory response is better preserved after laparoscopy vslaparotomy. Surg Endosc 8: S30

14. Trokel MJ, Bessler M, Treat MR, Whelan RL, Nowygrod R (1994)Preservation of immune response after laparoscopy. Surg Endosc 8:1385–1387; discussion 1387–1388

15. Wichterman KA, Baue AE, Chaudry IH (1980) Sepsis and septicshock: a review of laboratory models and a proposal. J Surg Res 29:189–201

Table 1. The gross appearance and length of ligated cecum at necropsy inrats 4 days following laparoscopic or open CLP; NS4 nonsignificant

Laparoscopic CLP Open CLP

Length of cecal ligation (mm)a 15.6 13.1 NSCecum normalb 5 3 NSCecum redb 6 10 NSCecum black/grayb 4 4 NS(+) peritoneal cultureb 10 10 NS

a Group average.b Number of animals.

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News and notices

New Address for the European Association forEndoscopic Surgery (E.A.E.S.)

Effective January 1, 1997, the new correspondence, telephone, and faxnumbers of the E.A.E.S. office are:

E.A.E.S. Office, c/o Mrs. Ria Palmen

Luchthavenweg 81Unit 1.425657 EA EindhovenThe Netherlandsor: P.O. Box 3355500 AH VeldhovenThe NetherlandsTel: +31 40 2525288Fax: +31 40 2523102

Volunteer Surgeons NeededNorthwestern Nicaragua LaparoscopicSurgery Teaching Program,Leon, Nicaragua

Volunteer surgeons are needed to tutor laparoscopic cholecystectomy forthis non-profit collaboration between the Nicaraguan Ministry of Health,the National Autonomous University of Nicaragua, and Medical TrainingWorldwide. The program consists of tutoring general surgeons who havealready undergone a basic laparoscopic cholecystectomy course. MedicalTraining Worldwide will provide donated equipment and supplies whenneeded.

For further information, please contact:

Medical Training WorldwideRamon Berguer, MD, ChairmanTel: 707-423-5192Fax: 707-423-7578e-mail: berguer.r@martinez.va.gov

Fellowship in Minimally Invasive SurgeryGeorge Washington Medical CenterWashington, DC USA

A one-year fellowship is being offered at the George Washington Univer-sity Medical Center. Interested candidates will be exposed to a broad rangeof endosurgical Education and Research Center. Active participation inclinical and basic science research projects is also encouraged.

For further information, please contact:

Debbie Moser202-994-8425

or, send curriculum vitae to:

Dr. Jonathan M. SackierDirector, Washington Institute of Surgical EndoscopyGeorge Washington University Medical CenterDepartment of Surgery2150 Pennsylvania Avenue, N.W.6B-417Washington, DC 20037, USA

Essentials of Laparoscopic SurgerySurgical Skills UnitUniversity of DundeeScotland, UK

Under the direction of Professor A. Cuschieri the Surgical Skills Unit isoffering a three-day practical course designed for surgeons who wish toundertake the procedures such as laparoscopic cholecystectomy. This in-tensely practical program develops the necessary operating skills, empha-sizes safe practice, and highlights the common pitfalls and difficultiesencountered when starting out. Each workshop has a maximum of 18participants who will learn both camera and instrument-manipulation skillsin a purpose-built skills laboratory. During the course there is a live dem-onstration of a laparoscopic cholecystectomy. The unit has a large libraryof operative videos edited by Professor Cuschieri, and the latest books onendoscopic surgery are on display in our Resource area. Course fee in-cluding lunch and course materials is $860.

For further details and a brochure please contact:

Julie Struthers, Unit Co-ordinatorSurgical Skills UnitNinewells Hospital and Medical SchoolDundee DD1 9SYTel: +44 382 645857Fax: +44 382 646042

Advanced Endoscopic SkillsSurgical Skills UnitUniversity of DundeeScotland, UK

Each month Professor Cuschieri Surgical Skills Unit offers a 41⁄2 daycourse in Advanced Endoscopic Skills. The course is intensely practicalwith ‘‘hands on’’ experience on a range of simulated models. The programis designed for experienced endoscopic surgeons and covers advanceddissection techniques, extracorporeal knotting techniques, needle control,suturing, internal tying technique, stapling, and anastomotic technique.Individual workstations and a maximum course number of 10 participantsallows for personal tuition. The unit offers an extensive collection of sur-gical videos and the latest books and publications on endoscopic surgery.In addition, participating surgeons will have the opportunity to see liveadvanced laparoscopic and/or thoracoscopic procedures conducted by Pro-fessor Cuschieri and his team. The course is endorsed by SAGES. Coursefee including lunch and course materials is $1850.

For further details and a brochure please contact:

Julie Struthers, Unit Co-ordinatorSurgical Skills UnitNinewells Hospital and Medical SchoolDundee DD1 9SYTel: +44 382 645857Fax: +44 382 646042

The Practical Aspects of Laparoscopic FundoplicationSurgical Skills UnitUniversity of DundeeScotland, UK

A three-day course, led by Professor Cuschieri, designed for experiencedlaparoscopists wishing to include fundoplication in their practice. The

SurgicalEndoscopy

© Springer-Verlag New York Inc. 1997Surg Endosc (1997) 11: 1232–1234

course covers the technical details of total and partial fundoplication usingsmall group format and personal tuition on detailed simulated models.There will be an opportunity to observe one of these procedures live duringthe course. Maximum course number is six. Course fee including lunch is$1850.

For further details and a brochure please contact:

Julie Struthers, Unit Co-ordinatorSurgical Skills UnitNinewells Hospital and Medical SchoolDundee DD1 9SYTel: +44 382 645857Fax: +44 382 646042

Courses at the Royal Adelaide Centre forEndoscopic Surgery

Basic and Advanced Laparoscopic Skills Courses are conducted by theRoyal Adelaide Centre for Endoscopic Surgery on a regular basis. Thecourses are limited to six places to maximize skill development and tuition.Basic courses are conducted over two days for trainees and surgeons seek-ing an introduction to laparoscopic cholecystectomy. Animal viscera insimulators is used to develop practical skills. Advanced courses are con-ducted over four days for surgeons already experienced in laparoscopiccholecystectomy who wish to undertake more advanced procedures. Awide range of procedures are included, although practical sessions can betailored to one or two procedures at the participants request. Practical skillsare developed using training simulators and anaesthetised pigs.

Course fees: $A300 ($US225) for the basic course and $A1,600($US1,200) for the advanced course.

For further details and brochure, please contact:

Dr. D. I. Watson or Professor G. G. JamiesonThe Royal Adelaide Centre for Endoscopic SurgeryDepartment of SurgeryRoyal Adelaide HospitalAdelaide SA 5000 AustraliaTel: +61 8 224 5516Fax: +61 8 232 3471

Advanced Laparoscopic Suturing and SurgicalSkills Courses

MOET InstituteSan Francisco, CA, USA

Courses are offered year-round by individual arrangement. The MOETInstitute is accredited by the Accreditation Council for Continuing MedicalEducation (ACCME) to provide continuing medical education for physi-cians and designates these CME activities for 20–40 credit hours in Cat-egory 1 of the Physician’s Recognition Award of the American MedicalAssociation. These programs are also endorsed by the Society of Gastro-intestinal Endoscopic Surgeons (SAGES).

For further information, please contact:

Wanda Toy, Program AdministratorMicrosurgery & Operative Endoscopy Training (MOET) Institute153 States StreetSan Francisco, CA 94114, USATel: (415) 626-3400Fax: (415) 626-3444

Courses at WISEWashington Institute for Surgical EndoscopyWashington, DC, USA

The Washington Institute of Surgical Endoscopy is pleased to offer thefollowing courses:

Laparoscopic antireflux and hiatal hernia surgery (July 14–15, 1997); Lap-aroscopic management of the common bile duct and difficult cholecystec-

tomy (May 15–16, August 11–12, November 10–11, 1997); Laparoscopiccolon and rectal surgery (June 20–21, September 15–16, December 4–5,1997). Also, courses for operating room nurses and technicians will be runon a monthly basis and personal instruction and preceptorship is available.

For further information, please call:

Debbie MoserWashington Institute of Surgical Endoscopy2150 Pennsylvania Avenue, N.W.Washington, DC 20037Tel: 202-994-9425

Call for AbstractsSociety of American Gastrointestinal Endoscopic Surgeons(SAGES) 1998 Annual MeetingApril 1–4, 1998Seattle, WA, USA

Abstract deadlines: Oral and Poster abstracts: September 12, 1997Video Submissions: September 18, 1997

For further information, or to obtain an abstract form, please contact:

SAGES Program CommitteeSociety of American Gastrointestinal Endoscopic SurgeonsSuite #30002716 Ocean Park BoulevardLos Angeles, CA 90405Tel: (310) 314-2404Fax: (310) 314-2585e-mail: SAGESMail@AOL.com

Second Asian Pacific Symposium and Workshop onMinimally Invasive Thoracic and Cardiac Surgery

December 9–11, 1997Taipei, Taiwan

The main themes are updates and live operative demonstrations of thora-coscopy and video-assisted thoracic surgery, minimally invasive cardiacsurgery, and thoracoscopic spine surgery.

For further information, please contact:

Hui-Ping Liu, MDDivision of Thoracic and Cardiovascular SurgeryChang Gung Memorial Hospital199 Tun-Hwa N Rd.Taipai, Taiwan 10591Tel: 866-3-3281200Fax: 866-3-3285818

Colorectal Disease in 1998February 19–21, 1998Fort Lauderdale, FL, USA

Symposium Director: Steven D. Wexner, MD

Cleveland Clinic Florida presents its ninth annual postgraduate course.Provides an intensive, in-depth, analytical review of all aspects of colo-rectal disease, including laparoscopy; colorectal carcinoma screening and

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genetics, inflammatory bowel disease; and pouch surgery. There will be areview of both basic and advanced principles of diagnosis and managementof disease. Video techniques will be shown as well. The faculty is inter-nationally represented and includes leading experts in the field. Simulta-neous Spanish and Italian translation is available.

For more information, please contact:

Cleveland Clinic FloridaDepartment of Education2950 West Cypress Creek RoadFort Lauderdale, FL 33309-1743Tel: 800-359-6101, ext. 6066Fax: 954-978-5539

6th World Congress of Endoscopy Surgery ‘‘Roma 98’’6th International Congress of European Associationfor Endoscopic Surgery

June 3–6, 1998Rome, Italy

The program will include: the latest, original high quality research; sym-posia; plenary lectures; abstract presentations (video, oral, and posters);EAES and SAGES postgraduate courses, OMED postgraduate course ontherapeutic endoscopy; working team reports; educational center and learn-ing corner; meeting of the International Society of Nurses and Associates;

original and non original scientific reports; and a world expo of newtechnology in surgery.

For further information, please contact:

Congress Secretariat: Studio EGAViale Tiziano, 1900196 Rome, ItalyTel: +39 6 322-1806Fax: +39 6 324-0143

Tenth International Conference of the Society for Mini-mally Invasive TherapySeptember 3–5, 1998London, England

Host Chairman: Mr. J. Wickham

For further information, please contact:

The Society for Minimally Invasive Therapy2nd Floor, New Guy’s HouseGuy’s HospitalSt. Thomas StreetLondon, SE1 9RT, EnglandTel: +44 (0)171 955 4478Fax: +44 (0)171 955 4477email: j.wickham@umds.ac.uk

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Needle and trocar injury during laparoscopic surgery in Japan

M. Hashizume, K. Sugimachi, Study Group of Endoscopic Surgery in Kyushu, Japan

Department of Surgery II, Faculty of Medicine, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka, 812-82, Japan

Received: 10 February 1997/Accepted: 22 May 1997

AbstractBackground:With the growth and sophistication of laparo-scopic surgery, increased attention is now being focused onsafety and complications.Methods:In an attempt to address questions regarding thesafety of laparoscopic surgery, a retrospective study of thetime period from January 1991 to December 1995 was con-ducted by the Study Group of Endoscopic Surgery in Ky-ushu, Japan.Results:The response rate was 84.4% (152 of 180 hospi-tals). During the last 5 years 17,626 patients underwentendoscopic operations and 87.5% (15,422 patients) had lap-aroscopic surgery while 12.5% (2,204 patients) underwentthoracoscopic surgery. In 96.6% of the hospitals a minimalopen laparotomy was used. Among the various operations,a cholecystectomy was performed in the largest number ofpatients (13,787). The total number of complications was415 (2.7%), of which 156 (37.6%) were related to needle ortrocar insertion. Visceral injury was found in 22 patients(0.14%): major vessel injury in 10, gastrointestinal tractinjury in 11, and liver injury in one patient. Abdominal wallinjury was seen in 79 patients (0.52%), bleeding in 70(0.46%), and a hernia in 9 (0.06%). Extraperitoneal insuf-flation occurred in 55 patients (0.36%). There was no mor-tality. The complication rate significantly decreased year byyear after the use of laparoscopic surgery began.Conclusions:The most common complications of laparo-scopic surgery are related to needle and trocar insertion.These are preventable by placement under direct vision withverification of the intraperitoneal location of the needle andtrocar.

Key words: Trocar injury — Complication — Laparoscop-ic surgery

Having achieved vast acceptance following its pioneeringphase, minimally invasive surgery is now exerting a sub-stantial impact on the world of medicine. The use of lapa-roscopy as an alternative to open surgery continues to growdramatically. Along with its growth and sophistication,however, has also come an intensified focus on the need toprevent laparoscopic complications [3, 5, 6, 21].

The potential complications of laparoscopic surgery in-clude those resulting from the insertion of the needle andtrocar, the creation of the pneumoperitoneum, the position-ing of the patient, and the insertion and manipulation of theinstruments [2, 18, 22].

In an attempt to address questions regarding the safetyof laparoscopic surgery, a retrospective study of the timeperiod from January 1991 to December 1995 was conductedby the Study Group of Endoscopic Surgery in Kyushu, Ja-pan.

Materials and methods

In November 1995, we mailed a questionnaire to 180 hospitals that aremembers of the Study Group of Endoscopic Surgery in Kyushu, Japan. Therespondents involved in the collection of data were chiefs of departmentsof the hospitals and the data were collected from medical records. Thequestions referred to the frequencies with which laparoscopic procedureswere carried out during the period of January 1991 to December 1995 andalso to the frequency of complications. The analysis of complication re-lated to needle and trocar insertion was conducted on patients who under-went laparoscopic surgery. The patients who underwent thoracoscopic sur-gery or transanal endoscopic microsurgery (TEM) were excluded from thisstudy. In addition, the preventive measures taken to avoid complicationswere evaluated.

Results

The Study Group survey generated a response rate of 84.4%(152/180). In five (3.3%) of the 152 hospitals that partici-pated in the survey, only thoracoscopic operations wereperformed. Between January 1991 and December 1995,17,626 patients were registered; 87.5% (15,422 patients) ofthe total number of patients underwent laparoscopic surgerywhile 12.5% (2,204 patients) had thoracoscopic surgery. Inall of the hospitals except three, the total number of lapa-

Presented in part at the postgraduate course of the 5th World Congress ofEndoscopic Surgery, Philadelphia, Pennsylvania, USA

Correspondence to:M. Hashizume

Surg Endosc (1997) 11: 1198–1201

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© Springer-Verlag New York Inc. 1997

roscopic operations performed was under 500 cases. In threehospitals more than 1,000 cases were reported.

Table 1 shows the type of operations performed. Thegreat majority of these operations were laparoscopic chole-cystectomies (13,787, 89.4%). The mortality rate was zero.TEM was performed in 143 patients and was excluded fromthis study. The total complication rate was 2.7% (415/15,279). The insertion of needle or trocar was responsiblefor 156 injuries during laparoscopy (Table 2). Of these com-plications, 79 patients had early and late abdominal wallinjuries, 22 patients had visceral injuries, and 55 patientsexperienced extraperitoneal insufflation.

In 142 (96.6%) of the 147 hospitals in the Study Groupopen laparoscopy was performed (except during the 1styear, when endoscopic surgery had just started); only fivehospitals still used the Veress needle to establish a pneu-moperitoneum.

Vascular injury

Vascular injury occurred in 152 patients (Fig. 1), but majorvascular injury related to needle and trocar insertion oc-curred in only 10 patients (0.07%). The aorta was injured inone patient, the left common iliac artery in one patient, rightcommon iliac artery in three patients, the gastroepiploicartery in one patient, the epigastric artery in one patient, theretroperitoneal vessel in one patient, and the superior mes-enteric artery in two patients. The mechanism of injuryinvolved insertion of the primary trocar in seven patients(70%) and insertion of the Veress needle in two patients(20%). Injury was due to placement of the secondary trocarin one patient. A laparotomy was required in nine of 10patients with vascular injury. Suturing was done in fivepatients, ligation in two patients, electrocoagulation in onepatient, and tamponade in one patient. Only one patientrequired no treatment for the bleeding. Figure 1 shows thecomplication rate of vascular injury every year after startingendoscopic surgery. The incidence of vascular injury wasthe highest in the 1st year but thereafter gradually de-creased.

Gastrointestinal tract injury

Gastrointestinal tract injury occurred in 23 patients. Theincidence of gastrointestinal tract injury related to trocarinsertion was 0.07% (11 patients) (Fig. 2). The small intes-tine was injured in 10 patients and the large intestine in onepatient. Injury was caused by insertion of the primary trocarin seven patients (63.6%) and the secondary trocar in fourpatients. No intestinal injuries were related to insertion ofthe Veress needle. A laparotomy was required in two pa-tients and all injuries were successfully sutured. Figure 2shows the rate of gastrointestinal tract injury each year afterstarting endoscopic surgery. The incidence of gastrointesti-nal tract injury decreased over time.

Bleeding from the abdominal wall

Bleeding from the abdominal wall, which was the mostcommon complication, was always caused by trocar inser-tion and occurred in 70 patients (0.46%). The most frequentsources of hemorrhage were the superficial epigastric, infe-rior epigastric, and muscular abdominal wall vessels. In 69patients the bleeding was from the secondary trocar sites. Alaparotomy was required in four patients. Suture ligature ofthe bleeding vessels was done extracorporeally in 20 pa-tients and intracorporeally in three patients. Electrocoagu-lation was done externally in 14 patients and laparoscopi-cally in two patients. Tamponade with the use of a Foleyballoon catheter was successfully applied in one patient.Bleeding from the abdominal wall spontaneously ceasedduring operation without any specific treatment in 30 pa-

Table 1. Type of laparoscopic operations

Cholecystectomy 13,787Repair of inguinal hernia 541Colectomy 197Choledochotomy 150Transanal endoscopic microsurgery (TEM)a 143Partial gastrectomy 113Release of ileus 99Splenectomy 80Repair of duodenal perforation 57Appendectomy 44Drainage of hepatic cyst 14Hepatectomy 8Vagotomy 6Resection of pancreas 5Repair of esophageal hernia 5Esophagectomy 2Others 171Total 15,422

a In this study, 143 patients who underwent TEM were excluded from theanalysis of complication related to needle and trocar insertion.

Table 2. Complications related to needle and trocar insertion

Complication n %

Abdominal wall injury 79 0.52Bleeding 70 0.46Hernia 9 0.06

Visceral injury 22 0.14Major vessel 10 0.07Gastrointestinal tract 11 0.07Liver 1 0.01

Extraperitoneal insufflation 55 0.36Total 156/

15,2791.02

Fig. 1. Rate of vascular injury.

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tients. The rate of bleeding from the abdominal wall de-creased with experience (Fig. 3).

Primary late abdominal wall complications

Hernia formation occurred as a late abdominal wall com-plication in nine patients (0.06%). Hernias were found at theumbilical site of the primary trocar in seven patients and atan extraumbilical site in two patients. All hernias were as-sociated with a port site larger than 10 mm in size. A lap-arotomy was required in five patients and suture repair wasperformed in nine patients. One hernia was repaired lapa-roscopically with the use of a mesh. The incidence of post-operative hernia by each year is shown in Fig. 4.

Complications related to pneumoperitoneum

The complication rate related to the pneumoperitoneum was0.48% (Table 3). Subcutaneous emphysema was the mostcommon of these complications. In 54 of 55 patients inwhom subcutaneous emphysema was found no specifictreatment was necessary. In the remaining patient, evacua-tion of the gas by manual pressure on the abdominal wallwas done.

Discussion

The insertion of the Veress needle or trocars is responsiblefor a substantial number of injuries during laparoscopy. Ithas been reported that the complication rate of Veressneedle or trocar insertion during closed laparoscopy is ap-proximately 0.2–0.3% [14]. The modern technique of openlaparoscopy was first popularized by Hasson in 1974 [8].The primary advantage of this technique is that access to theperitoneal cavity is gained under direct vision. Therefore,bowel and vascular injuries should be virtually nonexistent[4, 13, 16]. However, bowel injuries still occur at the samerate using this technique.

Of our Study Group members, 96.6% changed theirmethod of establishing a pneumoperitoneum from theclosed method to an open laparoscopic technique in order toincrease patient safety during endoscopic surgery. The rateof complications related to needle and trocar insertion sub-

sequently decreased as the surgeon’s experience performingendoscopic surgery increased.

Vascular injuries, which occur in 0.1–0.6% of all pa-tients, may involve abdominal wall vessels, major retroper-itoneal vessels, or other intraabdominal vessels [1, 14, 15].Injury to the major retroperitoneal vessels such as the aorta,inferior vena cava, and iliac artery or vein has a mortalityrate of 9% [4].

Major vascular injuries occur in about 0.03–0.06% ofthe patients [17, 18, 20]. Injury to a major vessel is thesecond most common cause of death during laparoscopy,following anesthesia. A delayed diagnosis is common insuch fatalities. The mechanism of injury involves the Veressneedle in approximately two-thirds of all such cases and theinsertion of the primary trocar in one-third of cases. Ourstudy also showed that in nine of 10 patients the major

Fig. 2. Rate of gastrointestinal tract injury. Fig. 3. Rate of bleeding from the abdominal wall.

Fig. 4. Rate of postoperative hernia.

Table 3. Complications related to pneumoperitoneum

Complications n %

Subcutaneous emphysema 55 0.36Right shoulder or back pain 6 0.04Pneumothorax 4 0.03Hypercarbia 3 0.02Vagotonia 2 0.01Oliguria 1 0.01Pulmonary infarction 1 0.01CO2 gas embolism 1 0.01Total 73/

15,2790.48

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vascular injury was associated with the Veress needle andthe primary trocar. In nine of 10 patients an open laparot-omy was required to control bleeding. The best manage-ment of major vascular injury is prevention. The propertechnique of Veress needle insertion and verification of anintraperitoneal location are the two most important steps [4].If an injury occurs, the Veress needle should be left in placeand an immediate laparotomy should then be performed toobtain vascular control.

Injuries to the vessels of the abdominal wall are a fre-quent source of morbidity, occurring in 0.25–6.0% of cases[14, 15]. Bleeding from abdominal wall vessels is usuallymanifested by troublesome oozing around the trocar, eitherinternally or externally. In 30 of the 70 patients with bleed-ing from the abdominal wall, the bleeding spontaneouslyceased during the operation after merely applying pressurewith the trocar on the abdominal wall. Other initial methodsof management include tamponade with a Foley ballooncatheter or a lever to apply pressure to the posterior aspectof the anterior abdominal wall. Coagulation or ligation ofthe bleeding point externally or internally with a laparo-scopic approach is an alternative method. Finally, if all suchmethods fail, a laparotomy should be done to stop the bleed-ing. Injuries to the abdominal wall vessels may also beavoided in thin patients by transillumination and by inspec-tion of the abdominal wall prior to trocar insertion.

The complications of gastrointestinal injury are secondonly to hemorrhage in frequency. Half of the gastrointesti-nal tract injuries during operation are due to trocar insertion.The incidence in large series has been reported to rangefrom 0.06 to 0.4% [7, 9–12, 15, 19, 20] and has been asso-ciated with a relatively high mortality rate of 5%. The in-juries most frequently involve the small intestine, followedby the colon, duodenum, and stomach [6]. These injuries areoften unrecognized at the time of the laparoscopic proce-dures and are usually only detected later when the patientpresents with peritonitis, sepsis, or intraabdominal abscess.The incidence of gastrointestinal tract injury was the highestin the 1st year after starting endoscopic surgery, but theincidence of such injuries has substantially decreased as theexperience of the surgeons performing endoscopic surgeryhas increased.

The predominate late abdominal wall complication fol-lowing laparoscopic surgery is hernia formation. Herniationthrough laparoscopic entry sites is uncommon, with an in-cidence of less than 0.1% [2]. It is possible that this com-plication has been underreported. Boike et al. [2] offeredseveral guidelines that may reduce the occurrence of thiscomplication. The surgeon should use smaller trocars (5mm), if possible. The use of trocar anchoring devices suchas fascial screws may increase the risk of herniation bywidening the fascial defect. When ports larger than 10 mmare used an attempt should thus be made to suture the defect.If the surgeon elects not to close these incisions, then rec-ommendations include the use of Z-track placement of tro-cars and the slow release of the pneumoperitoneum withdirect visualization of the trocar removal to ensure that thebowel is not drawn into the abdominal wall. Selected casesof herniation may also be managed laparoscopically.

In conclusion, the complications related to needle and

trocar insertion are preventable by placement under directvision. Laparoscopic surgery is safe and effective whenproper techniques are utilized.

Acknowledgments.We wish to express our heartfelt thanks to Drs. Shin-ichiro Migo and Kouji Tsugawa for their kind help in the statistical treat-ment of the data collected in this study.

References

1. Begqvist D, Bergqvist A (1987) Vascular injuries during gynecologicsurgery. Acta Obstet Gynecol Scand 66: 19–23

2. Boike GM, Miller CE, Spirtos NM, Mercer LJ, Fowler JM, Summitt R,Orr JW (1995) Incisional bowel herniations after operative laparosco-py: a series of nineteen cases and review of the literature. Am J ObstetGynecol 172: 1726–1733

3. Deziel DJ (1994) Avoiding laparoscopic complications. Int Surg 79:361–364

4. Deziel DJ, Millikan KW, Economou SG, Doolas A, Ko S-T, Airan MC(1993) Complications of laparoscopic cholecystectomy; a national sur-vey of 4,292 hospitals and an analysis of 77,604 cases. Am J Surg 165:9–14

5. Dubelman A (1994) Complications of laparoscopic surgery: surgicaland anesthetic considerations. Semin Laparosc Surg 1: 219–222

6. Flowers JL, Zucker KA, Bailey RW (1994) Complications. In: Bal-lantyne GH, Leahy PF, Modlin IM (eds) Laparoscopic surgery. Chap-ter 8, WB Saunders, Philadelphia, pp 77–94

7. Grainger DA, Soderstrom RM, Schiff SF, Glickman MG, DeCherneyAH, Diamond MP (1990) Ureteral injuries at laparoscopy; insight intodiagnosis, management and prevention. Obstet Gynecol 75: 839–843

8. Hasson HM (1974) Open laparoscopy: a report of 150 cases. J ReprodMed 12: 234–238

9. Henning H (1985) The Dallas report in laparoscopic complications.Gastrointest Endosc 31: 104–105

10. Ilter T, Bolukoglu MA, Musoglu A (1986) Complication rates of di-agnostic laparoscopy. Gastrointest Endosc 32: 126

11. Kleppinger RK (1977) Laparoscopy at a community hospital: ananalysis of 4300 cases. J Reprod Med 19: 353–363

12. Krebs HB (1986) Intestinal injury in gynecologic surgery: a ten yearexperience. Am J Obstet Gynecol 155: 509–514

13. Larson GM, Vitale GC, Casey J, Evans JS, Gilliam G, Heuser L,McGee G, Rao M, Scherm MJ, Voyles CR (1991) Multipractice analy-sis of laparoscopic cholecystectomy in 1,983 patients. Am J Surg 163:221–226

14. Loffler FD, Pent D (1975) Indications, contraindications, and compli-cations of laparoscopy. Obstet Gynecol Surg 30: 407–427

15. McDonald PT, Rich NM, Collins GJ, Andersen CA, Kozloff L (1978)Vascular trauma secondary to diagnostic and therapeutic procedures:laparoscopy. Am J Surg 135: 651–655

16. The Southern Surgeons Club. (1991) A prospective analysis of 1518laparoscopic cholecystectomies. N Engl J Med 324: 1073–1078

17. Minz M (1977) Risks and prophylaxis in laparoscopy: a survey of100,000 cases. J Reprod Med 18: 269–272

18. Nordestgaaard AG, Bodily KC, Osborne RW Jr, Buttorff JD (1995)Major vascular injuries during laparoscopic procedures. Am J Surg169: 543–545

19. Peterson HB, Hulka J, Phillips JM (1990) American Association ofGynecologic Laparoscopists’ 1988 membership survey on operativelaparoscopy. J Reprod Med 35: 587–589

20. Riedel HH, Lehmann-Willenbrock E, Conrad P, Semm K (1986) Ger-man pelviscopic statistics for the years 1978–1982. Endoscopy 18:219–222

21. Riedel HH, Willenbrock EL, Mecke H, Semm K (1989) The frequencydistribution of various pelviscopic (laparoscopic) operations, includingcomplications rates: statistics of the Federal Republic of Germany inthe years 1983–1985. Zentralbl Gynakol 111: 78–91

22. Yuzpe AA (1990) Pneumoperitoneum needle and trocar injuries inlaparoscopy. A survey on possible contributing factors and prevention.J Reprod Med 35: 485–490

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Diagnostic ultrasound of acute colonic diverticulitis bysurgical residents

A. Zielke,1 C. Hasse,1 Th. Bandorski,1 H. Sitter,2 P. Wachsmuth,1 R. Grobholz,1 M. Rothmund1

1Department of General Surgery and2Institute of Theoretical Surgery, Philipps-University of Marburg, Baldinger Strasse, P.O. Box 100, 35043Marburg, Germany

Received: 3 October 1996/Accepted: 9 May 1997

AbstractBackground:Recent studies have documented the feasibil-ity of ultrasonography (US) to diagnose acute colonic di-verticulitis (ACD). This prospective observational trial de-termined the sonomorphology of ACD and evaluated thediagnostic accuracy of routine US performed on admissionby surgeons in training.Methods:Fifty-seven consecutive patients with a confirmedepisode of ACD were entered into this study, and the sono-morphology of the involved colon was assessed. US find-ings were compared to the results of the clinical evaluationand correlated to the clinicopathological outcome.Results:The sonomorphology of ACD was characterized bysegmental inflammatory transformation of the colon aver-aging 9.9 ± 3.2 cm (range, 6–20) in length and visualized astarget phenomena of a mean 3.5 ± 0.8 cm (range, 2.4–4.8)width. Targets were caused by hypoechogenic thickening ofthe colonic wall of an average 7.7 ± 2.6 mm (range, 4–18).In 40% of cases, a hyperechogenic halo representing peri-diverticulitis (average width, 2.3 ± 0.6; range, 1.2–3 cm)was noted. Diverticula were seen in almost half of the cases.Of the 57 cases with confirmed ACD, the diagnosis wasmade by US in 48, for a global accuracy of 84.2%. US wasfalse negative in nine patients, suggesting perforated appen-dicitis in five cases and acute appendicitis in one (the finaldiagnoses were perforated sigmoid diverticulitis in fivecases and cecal diverticulitis in one case). In three patients,US was nondiagnostic.Conclusion: In the hands of sonographically trained sur-geons, ultrasound is a useful modality to image acute co-lonic diverticulitis. US reveals diagnostic sonomorphologyin most cases of ACD and therefore facilitates early confir-mation of the diagnosis and assessment of severity.

Key words: Ultrasound — Acute colonic diverticulitis

Ultrasound (US) is a new method for imaging acute colonicdiverticulitis (ACD) [10, 14, 16]. If performed by an expertsonographer, it can be very accurate in establishing the di-agnosis [13]. However the diagnostic sonomorphology ofACD is not yet fully established. Moreover, it is unclearwhether surgeons trained in US imaging can successfullyutilize the method to diagnose ACD. We therefore studiedthe sonomorphology as well as the overall diagnostic accu-racy of routine ultrasonography performed by surgeons intraining in patients with confirmed episodes of ACD.

Patients and methods

Over a 4-year period, all patients admitted to the surgical clinic with apossible diagnosis of acute colonic diverticulitis underwent US evaluationand were entered into this study. Patients with generalized peritonitis re-quiring emergent surgery were excluded. Only those patients in whom thediagnosis of ACD was proven by either surgery or at least one establisheddiagnostic modality other than US were accepted for analysis. Ultrasoundwas performed on admission, after the physical examination.

Eleven surgeons in training (2nd- to 6th-year residents) were involvedin this study; all of them had received standardized training in abdominalultrasound, as described in detail elsewhere [6]. Training included an av-erage of 400 supervised investigations of the abdomen, as well as anintroduction to the method of graded compression [6]. ‘‘Graded compres-sion’’ refers to a technique of handling the ultrasound probe in a wayclosely resembling that of a surgeon’s palpating hands during physicalexamination: Gentle compression graded by the patients tolerance for painis applied with the probe, which is then slowly moved. Compression of theabdominal wall reduces the distance between the transducer and bowel,displaces gas and intraluminal residue, interposing bowel or mesentery andeliminates (or at least reduces) interfaces. Graded compression was alsoused in the area of greatest abdominal tenderness.

The US investigator was chosen arbitrarily and had supplied with thedetails of the clinical indications for the study. For the purpose of thisstudy, individual investigators were asked to deliver a definite diagnosis.Sonograms were interpreted immediately at the time of the procedure, andthere was no supervision until a definite ultrasonographic diagnosis wasestablished.

Patients were scanned using commercially available electronic real-time scanners (3.5- and 5.0-MHz transducers; Siemens SL100, Erlangen,Germany). Visualization of a hypoperistaltic segment with hypoechogenicmural thickening, presenting as a poorly compressible target in transverseview, was considered diagnostic of acute diverticulitis and thus recorded as

Offprint requests to:C. Hasse

Correspondence to:A. Zielke

Surg Endosc (1997) 11: 1194–1197

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© Springer-Verlag New York Inc. 1997

a positive finding. Nonvisualization of such a segment was regarded as anegative result. The largest diameter of the segment, its length, and muralthickness were measured by calipers. Diverticula, peridiverticulitis, andother signs of diverticulitis were recorded.

To assess the clinical utility of US in ACD, patients were allocated intoone of the following three clinical categories after the physical examina-tion: group A, highly likely for diverticulitis; group B, equivocal diagnosisof acute diverticulitis pending further investigation; group C, highly un-likely for diverticulitis. This allowed for a grading of the clinical suspicionof ACD. US results were compared to those obtained during the clinicalevaluation and correlated to the discharge diagnoses of the respective pa-tients.

Results

We evaluated 57 patients with a confirmed episode of ACD.This group was comprised of 31 female patients with amean age of 64.9 years (range, 35–89) and 26 male patientswith a mean age of (21–81) 55.6 years (m/f ratio, 1:1.2).The sigmoid colon was the most common site of acutediverticulitis (47/57; 82.4%). Involvement of the descendentcolon and left colonic flexure was found in eight cases

(14.1%). The cecum and ascending colon accounted for twocases (3.5%). The final diagnosis of ACD was confirmed byradio-opaque enemas in 29 patients (50.8%), surgery in 21patients (36.9%), colonoscopy in six patients (10.5%), andcomputed tomography in one patient (1.8%), respectively.Overall, 28 patients underwent operative interventions dur-ing the same hospital stay; ACD was confirmed in all cases.

During US evaluation ACD was characterized by hy-poechogenic thickening of the wall of an average 7.7 ± 2.6mm (range, 4–18) accompanied by luminal narrowing andhypoperistalsis of the involved colonic segment during dy-namic view. This region was usually appreciable as a poorlycompressible segmental target pattern in transverse viewand a rigid tubular structure displaying multiple hypoecho-genic strata in longitudinal view. The average width andlength of the inflamed segments were 3.5 ± 0.8 cm (range,2.4–4.8) and 9.9 ± 3.2 cm (range, 6–20). In 19 of 48(39.6%) cases of ACD with a true positive US investigation,a hyperechogenic halo of an average width of 2.3 ± 0.56 cm(range, 1.2–3) was noted (Figs. 1–4). Diverticula were seenwith a frequency of 47.9%. Abscesses were present in 11patients and visualized by US in nine; they ranged from

Fig. 1. Transverse section in the left lower quadrant exemplifying postin-flammatory sigmoid diverticulosis. Note the target pattern of the sigmoidcolon, revealing marked hypoechogenicity of the wall. Five concentriclayers of the bowel wall can be readily identified: The innermost brightlayer is produced by residue and air present within the lumen of the colon(1); the next layer is representative of the mucosa (2); the next bright layerrepresents an interface between mucosa and muscularis (3); the hypoecho-genic outer layer represents the muscularis (4); the next bright layer [(5)appreciated between 6 and 9 h] is yet another interface between muscularisand serosa. To the right of the target pattern, at 5 h, a small grape-likestructure with a central hyperechogenic reflection and faint dorsal acousticshadowing represents a noninflamed diverticulum.

Fig. 2. Transverse section in the left lower quadrant in a case of uncom-plicated acute sigmoid diverticulitis. Acute diverticulitis is characterized byan asymmetric inflammatory target pattern of the sigmoid colon (T) causedby hypoechogenic thickening of the wall, narrowing of the lumen, anddecreased peristalsis in dynamic view. To the right of the target, at 3 h, atubular structure with a bright apical reflection represents an inflameddiverticulum (D). It is surrounded by a hyperechogenic mass of homog-enous sonolucency, which is caused by inflammatory edema of the peri-colic fat and indicates peridiverticulitis (hyperechogenic halo, H).

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2 × 4 to 12 × 3 cm (Fig. 3). Enterovesicular fistulas wereapparent in two patients; neither was detected by US. Oneenterocutaneous fistula was correctly diagnosed by US(Table 1).

US made the diagnosis of ACD in 48 of the 57 caseswith proven diverticulitis, for an accuracy of 84.2%. Falsenegative results of US were recorded in nine cases (15.8%).The false diagnosis of complicated acute appendicitis wasmade in five patients; in these cases, the inflamed sigmoidcolon was found displaced to the right lower abdominalquadrant. All of these patients underwent surgery for signsof localized peritonitis. Four patients received two-stagesigmoid colectomies and appendectomy for perforated sig-moid diverticulitis, and one patient underwent one-stagesigmoid colectomy without appendectomy. Another caseconcerned a patient with an inflamed solitary cecal diver-ticulum and confined local peritonitis, which was also mis-diagnosed as acute appendicitis. This patient underwent ap-pendectomy and local resection of the cecal diverticulum.The remaining three cases involved a group of clinicallymildly affected patients; in these cases, diagnosis of uncom-plicated ACD was made by water-soluble contrast enemasin two patients and CT scanning in one patient, respectively.

Based on the results of the clinical evaluation on admis-sion, the immediate clinical diagnosis of an ACD was made

in 29 of 57 patients, for a diagnostic accuracy of 50.8%. Ofthe six patients who appeared clinically very unlikely forACD, five cases were misdiagnosed as acute appendicitisand one case as nonspecific acute abdominal pain. All otherpatients were classified as clinically equivocal cases, includ-ing five patients who eventually required emergency sur-gery for complicated ACD. Overall, of the 28 patients whounderwent surgery for ACD, the indication for a laparotomywas clinically evident in 12 cases, including the five patientswho were misdiagnosed as acute appendicitis. US identifiedall cases that subsequently underwent operative therapy al-though, as already pointed out, six cases were misinter-preted as acute appendicitis. While US and CT were alwaysperformed at the day of admission, colonoscopies were per-formed after a median 3.5 days (mean, 7.7 ± 3.5; range,0–28), and water-soluble contrast enemas were done at amedian 6 days (mean, 6.7 ± 5.4; range, 2–28) after admis-sion.

Discussion

Ultrasound (US) is increasingly used by surgeons in theinitial evaluation of the patient with acute abdominal pain

Fig. 3. Transverse section in the left lower quadrant in a case of compli-cated sigmoid diverticulitis. Note the target pattern of the sigmoid colonwith asymmetric hypoechogenic thickening of the wall (T). A small ir-regular hypoechogenic target with a central air reflection, visualized at 5 hrepresents an inflamed diverticulum (D). It is surrounded by a hypoecho-genic halo (shaded area). A well-confined abscess of 2 × 1 cm can be seento the right of the diverticulum (A).

Fig. 4. Transverse section in the left lower quadrant in a case of perforatedsigmoid diverticulitis with advanced local peritonitis. Note the faintly vis-ible, poorly defined hypoechogenic target pattern of the sigmoid colon (T),which is surrounded by a noncompressible zone of increased echogenicity.The inflammatory pseudo-tumor has attained a diameter of 7.5 cm andshows evidence of the spread of inflammation to pericolic fat and mesen-tery. Close to the abdominal wall, the halo is divided by multiple hy-poechogenic strata, representing fluid collections between the differentlayers of edematous epiploic appendices, mesenteric, and pericolic fat (on-ion-skin appearance).

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[2, 6, 11]. This study establishes that surgeons trained inultrasound imaging can effectively use this method to diag-nose acute colonic diverticulitis (ACD).

Computed tomography constitutes the current gold stan-dard imaging modality in complicated diverticulitis [1, 9].Like CT, US imaging allows the physician to define theextent of extramucosal inflammation and identify sequelaeof ACD, such as perforation and abscess, without intralu-minal procedures or contrast extravasation. The colon wasrelatively easy to access by US because of its close prox-imity to the abdominal wall and its size. The inflamed seg-ments usually attained a considerable size; they averaged3.5 × 9.9 cm in this study.

The diagnostic sonomorphology of ACD establishedduring this study was similar to that reported by other au-thors [13, 14, 16]. Besides some rather unspecific criteria ofinflammatory bowel disease, such as thickening of the co-lonic wall to 4–18 mm, lack of compressibility, and hypo-or aperistalsis, we observed a number of more specificsigns, such as diverticula (50%), local abscesses (20%), andfluid collections or fistulas (5%). Inflamed diverticula ordi-narily were visualized as grape-like hypoechogenic struc-tures, surrounded by an often double contoured wall. Theyfrequently displayed bright acoustic reflexes caused bytrapped air and feces. With extensive disease, hyperecho-genic halos surrounding the involved colonic segment werenoted; in addition, there was a lack of synchronous move-ment with breathing. This finding, which was considered anultrasonographic sign of peridiverticulitis, was noted insome 40% of patients.

Although no single sonographic criterion was consid-ered diagnostic, it was evident from this study that visual-ization of an inflammatory target sign in the left lower quad-rant, together with hyperechogenic halo and diverticula, ishighly suggestive of ACD in a symptomatic patient. Con-sequently, the 84% accuracy of this study for the sono-graphic diagnosis is quite comparable to the results fromthree other prospective trials published by recognized ex-perts in the field of ultrasonography, who reported an over-all accuracy of 82–98%, sensitivity of 84–98%, and a speci-ficity of 80–96% [4, 12, 15].

One potential pitfall, however, is the clinical presenta-tion of right-sided colonic diverticulitis, which is eithercaused by a solitary cecal diverticulum or a displaced sig-moid colon. Both conditions may be impossible to distin-guish from acute appendicitis. This presentation accountedfor five false clinical diagnoses and six false US results.Previous studies did not comment on this particular diffi-culty; therefore, this problem may have been a reflection of

lack of experience [6, 9]. CT may be a better alternative inthese circumstances.

Not unexpectedly, the accuracy for the clinical diagno-sis of ACD was low, but this problem is well documented inthe literature [10, 16]. The clinical diagnosis is rarely moreaccurate than 75% [3, 5]. However, assessing the site andseverity of the disease is important, particularly in compli-cated diverticulitis, since the outcome largely depends on atimely diagnosis [7, 8]. The routine use of CT is hamperedby its own restrictions—mainly limited availability and highcost [1, 9]. Use of colonoscopy and radio-opaque enema isalso limited, due to the increased frequency of complica-tions in ACD. Therefore, they cannot always be employedimmediately; the resulting diagnostic time lag of severaldays was also found in the present study.

Based on the results of this study, it appears that USimaging is a fast, feasible, and effective diagnostic modalityfor patients in whom ACD is suspected. US imaging facili-tates early confirmation of ACD and permits rational man-agement decisions to be made. Whether or not US will alterthe surgical management of these patients remains to beseen.

References

1. Ambrosetti P, Robert J, Witzig JA, Mirescu D, deGautard R, Borst F,Rohner A (1992) Incidence, outcome and proposed management ofisolated abscesses complicating acute left sided colonic diverticulitis:a prospective study of 140 patients. Dis Col Rec 35: 1072–1076

2. Davies AH, Mastoraku I, Cobb R, Rogers C, Lindsell D, Mc.Mortensen NJ (1991) Ultrasonography in the acute abdomen. Br JSurg 78: 1178–1180

3. Dawson JL, Harrow I, Roxburgh RA (1965) Diverticulosis coli com-plicated by diffuse peritonitis. Br J Surg 52: 354–357

4. Federmann G (1989) Sonographie in der Diagnostik der akuten Kolon-divertikulitis. Chirurg 60: 415–416

5. Hiltunen KM, Kolehmainen H, Vuorinen T, Matikainen M (1991)Early water-soluble contrast enema in the diagnosis of acute colonicdiverticulitis. Int J Colorecal Dis 6: 190–192

6. Klotter HJ, Zielke A, Niess C, Sitter H, Rothmund M (1992) Sonog-raphie beim akuten abdominellen Notfall. Chirurg 63: 597–605

7. Kronborg O (1993) Treatment of perforated sigmoid diverticulitis: aprospective randomized trial. Br J Surg 80: 505–507

8. Krukowski ZH, Matheson NA (1984) Emergency surgery for diver-ticular disease complicated by generalized and fecal peritonitis: a re-view. Brit J Surg 71: 921–927

9. McKee RF, Deignan RW, Krukowski ZH (1993) Radiological inves-tigation in acute diverticulitis. Brit J Surg 80: 560–565

10. Parulekar SG (1985) Sonography of colonic diverticulitis. J Ultra-sound Med 4: 659–666

11. Paterson-Brown S, Vipond MN (1990) Modern aids to clinical deci-sion-making in the acute abdomen. Br J Surg 77: 13–18

12. Puylaert JBCM, Rutgers PH, Lalisang RI, deVries BC, van der WerftSDJ, Dorr JPJ, Block RAPR (1987) A prospective study of ultraso-nography in the diagnosis of appendicitis. N Engl J Med 317: 666–669

13. Schwerk WB, Schwarz S, Rothmund M (1992) Sonography in acutecolonic diverticulitis: a prospective study. Dis Col Rectum 35: 1077–1084

14. Townsend RR, Jeffrey RB, Laing FG (1989) Cecal diverticulitis dif-ferentiated from appendicitis using graded compression sonography.AJR 152: 1229–1230

15. Verbanck J, Lambrecht S, Rutgeers L, Ghillebert G, Buyse T, NaesensM, Tytgat H (1989) Can sonography diagnose acute colonic diverticu-litis in patients with acute intestinal inflammation? A prospectivestudy. J Clin Ultrasound 17: 661–666

16. Wilson SR, Toi A (1989) The value of sonography in the diagnosis ofacute diverticulitis of the colon. AJR 154: 1199–1202

Table 1. Sonomorphology of acute colonic diverticulitis

FindingAverage(mm)

Range(mm)

Wall thickness 7.7 ± 2.6 4–18Target width 35 ± 8 24–48Segment length 99 ± 32 60–200Hyperechogenic halo 23 ± 5.6 12–30

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Case reports

Laparoscopically assisted abdominoperineal resection and simultaneoustotal anorectal reconstruction with electrostimulatedstatic-dynamic graciloplasty

E. Cavina, M. Seccia, M. Chiarugi, P. Banti, G. Zocco

Emergency Surgery Unit, Department of Surgery, Ospedale Santa Chiara, Via Roma 67, 56100 Pisa, Italy

Received: 1 July 1996/Accepted: 19 November 1996

Abstract. Bilateral electrostimulated graciloplasty, per-formed in a ‘‘static-dynamic’’ configuration around a per-ineal colostomy (total anorectal reconstruction—TAR), hasbeen proven a reliable way to restore continence in patientswho undergo to abdomino perineal resection (A.Pe.R.) ofthe anorectum for lower rectal cancer. In selected cases,laparoscopically assisted TAR can significantly improvebody-image preservation and aesthetic results. A 33-year-old woman affected by lower rectal cancer was submitted tolaparoscopic-assisted A.Pe.R and TAR with simultaneousbilateral graciloplasty; a suprapubic median mini-accesswas adopted to fully mobilize the mesorectum in absence ofpneumoperitoneum. A subcutaneous pulse generator andspecial electrodes were also implanted to chronically elec-trostimulate the graciloplasty. In spite of postoperativebleeding which required a blood transfusion, postoperativeoutcome was satisfactory; electrostimulation was started onthe 10th postoperative (p.o.) day and the patient was dis-charged on the 17th p.o. day. Two months after TAR, levelII continence (N.S. Williams Scale) was achieved. In se-lected cases, laparoscopically assisted A.Pe.R. and TAR canbe safely adopted to preserve body image and quality of life,avoiding at the same time a large abdominal approach anda ‘‘permanent’’ abdominal colostomy.

Key words: Rectal cancer — Graciloplasty — Laparoscopy— Sphincter reconstruction — Electrostimulation — Neo-sphincter

Total Anorectal Reconstruction (TAR) was adopted in ayoung woman affected by lower rectal cancer with the aimof avoiding both a large abdominal approach and a perma-

nent abdominal colostomy; technique and a preliminary fol-low-up study are presented.

Recent literature reviews on laparoscopic vs open colonsurgery state that ‘‘the laparoscopy has become an accept-able alternative for the treatment of a variety of colorectaldisorders’’ and at the same time that ‘‘in conclusion, thesewere no statistically significant differences in costs or out-come between laparoscopic and open colorectal proce-dures’’ [24].

As far as oncological safety of laparoscopic surgery isconcerned, potential hazards of tumor recurrences at lapa-roscopic port sites are highlighted by many recent reports,even though the effectiveness and statistical significance ofthis phenomenon are controversial [1, 5, 8, 10, 13–15, 22,25, 34].

In spite of that, the total number of colorectal laparo-scopic or laparo-assisted procedures is growing and thou-sands of cases are collected in international registers [3, 4,9, 11, 12, 16, 17, 20, 21, 23, 26, 28, 30, 33, 35, 36]. As ofMarch 1996, the Italian national register Societa` Italiana diChirurgia Endoscopica (S.I.C.E.) reported 664 VLCs;28.7% (190 VLCs) were carried out for rectal cancer and8% (53 VLCs) consisted in A.Pe.R.

Presumably, in the near future, more detailed guidelinesallowing performance of better laparoscopic or laparo-assisted colorectal surgery will be available; standardizedprotocols for patient enrollment, oncological risk evalua-tion, and an effective comparison vs open surgery (costs,aesthetic results, quality of life, postoperative discomfort,complication rates, etc.) will also be better defined.

Keeping these prospects in mind, our initial enthusiasmin performing colorectal laparoscopic surgery has been re-duced, and this approach is now submitted to a prudent andstrict selection, with the exclusion of all cases presentinghigh risk of tumor recurrence, in particular at port sites.

Concerning the ‘‘aesthetic’’ aspects, it has recently beenaffirmed that ‘‘in the young patients the improved cosmeticresults after laparoscopic surgery may play a significantrole’’ [36].Correspondence to:E. Cavina

SurgicalEndoscopy

© Springer-Verlag New York Inc. 1997Surg Endosc (1997) 11: 1209–1212

Since 1991 to date, our laparoscopy experience hasmainly been based on biliary tract diseases (1,113 cases).Colorectal laparoscopy surgery was limited to 31 cases, themajority of which were treated for right colonic cancer; inall these cases, lymphoadenectomy was carried out in theabsence of pneumoperitoneum.

The management of the reported case was inspired bythe contemporary necessity of a correct oncologic approachand the restoration of sphincteric function, giving to a 33-year-old woman the possibility of a good quality of lifetogether with aesthetic benefits.

Continence restoration was based on the same techniqueof TAR performed during a 10-year experience in which 99electrostimulated graciloplasties were wrapped around aperineal colostomy in ‘‘static-dynamic’’ fashion.

During this experience, good continence rates rangedfrom 70 to 87% depending on stimulation protocols anddevices (short-term/chronic stimulation), and no significantdifferences were observed in early and 5-year mortalityrates between this technique and A.Pe.R. [7].

Materials and methods

In February 1996, a 33-year-old woman was admitted to our unit forsurgical treatment of a lower rectal adenocarcinoma. Previous outpatientstudies (endoscopy, endorectal sonography, pelvic CAT scan) demon-strated the presence of a 2 × 4 cmtumor involving the posterior wall of therectum, 1 cm above the anal verge. No extramural spreading or metastaseswere observed with either CAT or US evaluation. Combined chemo- andradiotherapy (fluorouracil [5FU]—45 Gy) was then carried out by theOncology Unit of our institution, obtaining a tumor size reduction of 50%.Preoperative staging was T2N0M0, confirmed by specimen examination(T0N0Mx—Grading 2/4, B1 Astler-Coller system stage).

Technique

After bowel preparation (iso-osmotic laxative solution) and antibiotic pro-phylaxis (cephalosporin), the patient was submitted to VL approachthrough four ports placed as shown in Fig. 1; intraoperative US evaluation(laparoscopic ultrasound probe 6.5–7.5 MHz—Esaote Biomedica, Genova,Italy) excluded liver, pre-aortic, and pelvic involvement, confirming theexistence of gallbladder microlithiasis.

After inferior mesenteric vein section, transverse colon, splenic flexure,descending colon, and sigma were fully mobilized and the inferior mes-enteric artery (IMA) resected at its origin.

Pre-aortic lymphoadenectomy was then extended from above this pointdown to the presacral space; laparoscopic cholecystectomy was also car-ried out [18, 19, 29, 32, 38].

Through a median suprapubic mini-access (9 cm in length), open sur-gery was then started, pursuing the following steps:

● A preliminary, accurate examination of the mobilized colon to evaluatethe adequacy of its vascular supply and length in order to lower it to theperineal floor

● Proximal colonic stump section and blunt mobilization of the rectum● Dissection of the mesorectum, rectum, and lateral pedicles from the

lower pelvic floor and the vagina

The subsequent perineal resection was then accomplished according to the‘‘classic’’ Miles procedure and suture landmarks were placed on the leva-tor’s-ani insertions to allow the neosphincter anchoring. The colon wasthen lowered to the perineal floor where it was left closed with a Foleycatheter inserted into the lumen; no diversionary procedures were applied.

According to our previously described ‘‘static-dynamic’’ draft, bilat-eral graciloplasty was carried out as follows [7]:

● Full mobilization of both muscles through three segmental incisions● Left gracilis wrapped behind the perineal colonic stump, reproducing the

puborectalis sling function (Fig. 2)

● Right gracilis wrap configured in a clockwise ‘‘a,’’ simulating the analsphincter

● Both muscle bellies sutured to landmarks previously placed on the le-vator’s-ani insertions

● Gracilis tendons fixed to subcutaneous fascia, to avoid excessive tensionaround the perineal colostomy

Electrostimulation

Electrostimulation device implant was carried out as the final step of theprocedure once all incisions were sutured, muscle relaxant administrationwas suspended, and gentamicin was locally flushed. Platinum-iridium elec-trodes (model 4300 Implantable Unipolar Leads; Medtronic Interstim,Kerkrade, The Netherlands) were placed on each muscle, following a com-bined technique of ‘‘over-the-nerve’’ and intramuscular implant.

After the main nerve identification, carefully avoiding any direct dam-age, the proximal part (1.5 cm) of each exposed electrode was fixed to theperineural, while the remaining part (2.5 cm) was inserted into the muscleperpendicular to its longitudinal axis.

Both electrodes were connected to a quadripolar Implantable PulseGenerator (Itrel II IPG, model, 7424; Medtronic Interstim, Kerkrade, TheNetherlands) placed in a subcutaneous abdominal pocket; basal stimulationparameters were then recorded and incisions were sutured. Intraoperativefull contraction was obtained at 0.8 V amplitude and 315V impedance,recorded 90 minutes after the last muscle-relaxant administration.

Results

Postoperative course was complicated by consistent bleed-ing which probably originated from colonic dissection sur-faces; after clinical and ultrasound monitoring the compli-cation was conservatively treated. Nevertheless, a transfu-sion of two blood units was needed [6, 27]. In spite of that,the succeeding postoperative (p.o.) course was uneventful.Colonic stump was resected on the 3rd p.o. day and a co-locutaneous suture was carried out under local anesthesia onthe 5th p.o. day. Hospital length of stay was 17 days.

Electrostimulation was started on the 10th p.o. day for 6h and progressively increased to 24 h; stimulation param-eters were then assessed to allow an acceptable continenceeven during the first training period of cyclic (on/off) stimu-lation.

According to previous studies [2, 31, 37], a chronicstimulation protocol was then carried out with the followingparameters: amplitude: 1.8 V, frequency: 25 pps, on/offratio: 0.1/1.2 s. Four weeks after starting electrostimulation,

Fig. 1. Postoperative view of the abdomen.

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no deviation from the protocol is noted and patient conti-nence is classified as II of the Williams modified Scale. Theelectromanometry (EMM) study performed in ‘‘IPG-ONmode’’ shows MRP and MVP values of 60 mmHg and 80mmHg, respectively; dynamic vector volumetry confirmshomogeneous pressure areas corresponding to the trans-posed muscles.

Discussion

We believe that in the described case, as in future VL-assisted procedures, a correct preoperative staging and alaparoscopic intraoperative US are mandatory to evaluaterisks of recurrence and the feasibility of a laparoscopic pro-cedure. Surgical maneuvers carried out in the upper perito-neal cavity preliminary to the pelvic dissection were accept-able from the oncological point of view and very useful forthe subsequent open mini-access.

The open mini-access allowed full pelvic control, re-duced operation length, and permitted at the same time anapproach to the mesorectum in the absence of pneumoperi-toneum which decreased oncologic risks of contamination.

The aesthetic aspect was particularly relevant in the re-ported case, due to the fact that open surgery would other-wise have led to a large median laparotomy and to a per-manent abdominal stoma, with consequent severe impair-ment in quality of life and ‘‘body-image’’; from this pointof view, the final result was excellent (Fig. 1). Short-term (4weeks) functional results anticipate a future continence inthe best range of our previous results: at the moment colonicvoiding is regular; a mini-enema is needed on alternatedays; continence is reasonably acceptable (occasional leak-age), and the patient uses a minipad per day for security.

On the basis of this experience we can conclude that alaparoscopically assisted A.Pe.R with a simultaneous TARis an appropriate and a safe continence-restoring procedurein selected cases.

References

1. Alexander EJT, Jaques BC, Mitchell KG (1993) Laparoscopically as-sisted colectomy and wound recurrence (letter). Lancet 341: 249–250

2. Baeten CGMI, Konsten J, Spaans F, Visser R, Bourgeois AMMC,Wagenmakers AJM, Soeters PB (1994) Dynamic graciloplasty fortreatment of faecal incontinence. Lancet 338: 9: 1163–1165

3. Beart R (1994) Laparoscopic colectomy: status of the art. Dis Colonrectum 37 (Suppl): S47–S49

4. Benitez LD, Plasencia G, Viamonte M, Jacobs M, Edelman DS (1996)Laparoscopic assisted colectomy: a retrospective review. Surg Endosc10: 223 (Abstract)

5. Bouvy ND, Marquet RL, Jeekel H, Bonjer J (1996) Gasless laparos-copy versus CO2 pneumoperitoneum in relation to the development ofabdominal wall metastases. Surg Endosc 10: 210 (S154)

6. Breton G, Pomp A, Gagner M (1996) Complications related to lapa-roscopic surgery for intestinal obstruction. Surg Endosc 10: 211(S155)

7. Cavina E (1996) Outcome of restorative perineal graciloplasty withsimultaneous excision of the anus and rectum for cancer. Dis ColonRectum 39 (2): 1–9

8. Cirocco WC, Schwartzman A, Golub RW (1994) Abdominal wallrecurrence after laparoscopic colectomy for colon cancer. Surg 116:842–846

9. Fielding G, Stitz R, Nathanson L, Lumley J, Rhodes M (1996) Lap-aroscopic assisted colorectal surgery. Surg Endosc 10: 211 (S158)

10. Fielding G, Stitz R, Nathanson L, Lumley J, Rhodes M, Bailey I(1996) Laparoscopic assisted colectomy for malignant disease. SurgEndosc 10: 231 (Abstract)

11. Fowler DL, White SA, Anderson CA (1995) Laparoscopic colon re-section: 60 cases. Surg Laparosc Endosc 5: 468–471

12. Franklin ME, Ramos R, Rosenthal D, Schuessler W (1993) Laparo-scopic colonic procedures. World J Surg 17: 51–56

13. Fusco MA, Paluzzi MW (1993) Abdominal wall recurrence after lap-aroscopic assisted colectomy for adenocarcinoma of the colon. DisColon Rectum 36: 858–861

14. Jacquet P, Sugarbaker P (1996) Wound recurrence after laparoscopiccolectomy for cancer: new rationale for intraoperative intraperitonealchemotherapy. Surg Endosc 10: 295–296

15. Jawad MZA (1996) Abdominal wall recurrence after laparoscopicallyassisted colon resection for malignant tumors. Surg Endosc 10: 237(Abstract)

16. Kim HC, Geis WP (1996) Laparoscopic assisted colon surgery by asingle surgeon: techniques and results. Surg Endosc 10: 240 (Abstract)

17. Lacy Am, Garcı`a-Valdecasas JC, Pique´ JM, Delgado S, Campo E,Bordas JM, Taura` P, Grande L, Fuster J, Pacheco JL, Visa J (1995)

Fig. 2. Static-dynamic graciloplasty model:both gracilis muscles are wrapped around theperineal colostomy(C). The deeper wrap mim-ics the puborectalis sling function, passing be-hind the colonic stump(B), while the secondwrap (A), circularly surrounds the colon.

1211

Short-term outcome analysis of a randomized study comparing lapa-roscopic vs open colectomy for colon cancer. Surg Endosc 9: 1101–1105

18. Larach SW, Salomon MC, Williamson PR, Goldstein E (1993) Lap-aroscopic assisted abdominoperineal resection. Surg Laparosc Endosc3: 115–118

19. Milsom JW, Marchesa P, Fazio VW (1996) Retroperitoneal mesentericdissection in laparoscopic oncologic colorectal surgery. Surg Endosc10: 210 (S153)

20. Monson JRT, Darzi A, Declan Carcy P, Guillou PJ (1992) Prospectiveevaluation of laparoscopic-assisted colectomy in an unselected groupof patients. Lancet 340: 831–833

21. Monsons JRT, Hill ADK, Darzi A (1995) Laparoscopic colonic sur-gery. Br J Surg 82: 150–157

22. Nduka CC, Monson JRT, Menzies-Gow N, Darzi A (1994) Abdominalwall metastases following laparoscopy. Br J Surg 81: 648–652

23. Ota DM (1995) Laparoscopic colon resection for cancer. Surg Endosc9: 1318–1322

24. Pfeifer J, Wexner SD, Reissman P, Bernstein M, Noguera JJ, Singh S,Weiss E (1995) Laparoscopic vs open colon surgery. Surg Endosc 9:1322–1326

25. Ramos JM, Gupta S, Anthone GJ, Ortega AE, Simons AJ, Beart RW(1994). Laparoscopy and colon cancer. Is the port site at risk? Apreliminary report. Arch Surg 129: 897–899

26. Ramos JM, Beart RW Jr, Goes R, Ortega AE, Schlinkert RT (1995)Role of laparoscopy in colorectal surgery. Dis Colon Rectum 38: 494–501

27. Reissman P, Wexner SD, Cohen SM, Nogueras JJ, Jagelman DG(1994) Complications of laparoscopic colorectal surgery. Surg Endosc8: 562 (Abstract)

28. Rouffet F, May JM, Vacher B, Fingerhut A, Elhadad A, Flamant Y,Mathon C, Gainant A (1994) Curative resection for left colonic car-

cinoma: hemicolectomy vs segmental colectomy. Dis Colon Rectum37: 651–659

29. Schoucair A, Brouch H, Herold A (1994) Laparoscopic abdomino-perineal rectum resection. Surg Endosc (Abstr 4th World Congr En-dosc Surg Kyoto 16–19 June 1994) 8: 508

30. Scoggin SD, Frazee RC, Snyder SK, Hendricks JC, Roberts JW, Sym-monds RE, Smith RW (1993) Laparoscopic-assisted bowel surgery.Dis Colon Rectum 36: 747–750

31. Seccia M, Menconi C, Balestri R, Cavina E (1994) Study protocolsand functional results in 86 electrostimulated graciloplasties. Dis Co-lon Rectum 37 (9): 897–904

32. Tanaka J, Ito M, Shindo Y, Kotanagi H, Koyama K (1996) Laparo-scopically assisted resection of the lower rectum. Surg Endosc 10:338–340

33. Van Ye TM, Cattey RP, Lyle GR (1994) Laparoscopically assistedcolon resection compares favorably with open technique. Surg Lapa-rosc Endosc 4: 25–31

34. Walsh D, Wattchow D, Wilson T (1993) Subcutaneous metastasesafter laparoscopic resection of malignancy. Aust N Z J Surg 63: 563–565

35. Wexner SD, Cohen SM, Johansen OB, Noguers JJ, Jagelman DG(1993) Laparoscopic colorectal surgery: a prospective assessment andcurrent perspective. Br J Surg 80: 1602–1605

36. Wexner SD, Reismna P, Pfeifer J, Bernstein M, Geron N (1996) Lap-aroscopic colorectal surgery: analysis of 140 cases. Surg Endosc 10:133–136

37. Williams NS, Patel J, George BD, Hallan RI, Watkins ES (1991)Development of an electrically stimulated neoanal sphincter. Lancet338 (9): 1166–1169

38. Wu JS, Fleshman JW (1996) Early experience with laparoscopic ab-dominal perineal resection. Surg Endosc 10: 267 (Abstract)

1212

Is outpatient cholecystectomy safe for the higher-risk elective patient?

A. J. Voitk

Department of Surgery, Suite 1840, The Salvation Army Scarborough Grace Hospital, 3030 Birchmount Avenue, Scarborough,Ontario, Canada M1W 3W3

Received: 26 December 1996/Accepted: 2 April 1997

AbstractBackground:This study was done to determine the safety ofoutpatient cholecystectomy for the higher-risk patient.Methods:All patients over age 70 or with American Societyof Anesthesiologists physical status classification of 3 orgreater, from all 515 consecutive patients booked for elec-tive cholecystectomy between April 1, 1994, and March 31,1996, were reviewed.Results:Of 85 higher-risk patients, 77 were booked as out-patients. Sixty-one were successfully completed as outpa-tients, with no complications or readmissions related to theiroutpatient status. Of 24 admitted patients, 15 had specificindications for hospitalization. Nine were admitted for rea-sons of ‘‘precaution.’’ One of these developed a complica-tion, possibly related to her inpatient status. The other eightcould have been managed as outpatients.Conclusions:Outpatient cholecystectomy is safe for thehigher-risk patient. Patients who recover uneventfully fromsurgery can be discharged without harmful effects. ‘‘Pre-cautionary’’ hospitalization may be harmful.

Key words: Laparoscopic cholecystectomy — High-riskpatient — Ambulatory surgery — Safety

Outpatient cholecystectomy has been the standard of prac-tice at the Salvation Army Scarborough Grace Hospitalsince 1994. Although it has been demonstrated repeatedlythat neither old age nor comorbidity precludes safe outpa-tient surgery [2, 3, 6–8, 11–13], some clinicians remainskeptical about the prudence of such practice for higher-riskpatients [9]. Both age [1, 3, 14] and physical status [4, 5, 10]have been shown to be reliable predictors of surgical risk.To determine the safety of elective outpatient cholecystec-tomy for higher-risk patients, this paper examines the fate ofall higher-risk patients at the Salvation Army ScarboroughGrace Hospital during 2 years of routine outpatient chole-cystectomy.

Methods and patients

The Salvation Army Scarborough Grace Hospital is a 256-bed acute-carenonteaching hospital served by four general surgeons and located on theoutskirts of a major urban center. All patients booked for elective chole-cystectomy by all four surgeons between April 1, 1994, and March 31,1996, inclusive, were identified. Patients above age 70 or with an AmericanSociety of Anesthesiologists physical status classification of 3 (ASA 3) orhigher were selected and the fate of those successfully treated as outpa-tients was reviewed in detail. All operations were done under generalinhalation anesthesia. The operative technique and perioperative manage-ment have been described [11]. All patients were telephoned by a DaySurgery nurse the day after surgery and all were seen by the operatingsurgeon within 15 days of operation. For the purposes of this study, out-patient was defined as discharge on the day of surgery; overnight stay wasconsidered admission to hospital, even if total stay was under 24 h. Prob-ability was determined by thex2 test and significance assumed at thep <0.05 level.

Results

In the years under study 515 elective cholecystectomieswere done, of which 85 were done on higher-risk patients.Age was a risk factor for 57 patients and comorbidity for 46;18 patients had both risk factors. Cardiovascular diseasewas the sole or most significant contributor to ASA classi-fication for 78% of the higher-risk patients. The incidenceof acute cholecystitis, conversion, admission, readmission,or complication was not significantly different betweenthese subsets. Average door-to-door time for outpatientswas 6 h.

The 28% admission rate of the higher-risk patients wassignificantly higher than the 12% admission rate of the

Table 1. Clinical characteristics of higher and lower-risk populations ex-pressed as percent

n Male Acute chole Converted Admitted

Higher risk 85 34 14 6 28Lower risk 430 21 7 3 12p n/a p > 0.05 p > 0.05 p > 0.05 p < 0.05

Surg Endosc (1997) 11: 1147–1149

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lower-risk patients. The higher- and lower-risk populationsare compared in Table 1.

Of the 85 higher-risk patients, 77 were booked for out-patient cholecystectomy, which was successfully accom-plished for 61. These 61 higher-risk outpatients encounteredno problems related to outpatient status; 26% had minorcomplications and two readmissions (one patient came withabdominal pain 3 weeks later, was admitted, and had anERCP; the other patient returned with a fractured hip 4months postoperatively). The 24 admitted patients had a17% minor complication rate and one readmission 3 weekspostoperatively for percutaneous drainage of a subphrenicabscess. Complication rates and readmission rates did notdiffer significantly between higher-risk outpatients andhigher-risk admitted patients. Table 2 compares thesegroups: Both are essentially similar, except for a greaternumber of conversions in the admitted group.

Sixteen patients, booked as outpatients, were admittedduring the perioperative period. A specific reason for hos-pitalization became apparent for 12 patients: five were con-verted to open surgery, three needed intravenous antibiotics,and one each because of hypoxia, profound vomiting andsocial reasons. Four patients were admitted for ‘‘precaution-ary’’ reasons; none of these required any active interventionin hospital, all were discharged the next morning, and nonehad any readmissions or complications.

A decision to admit had been made during the preop-erative evaluation in the office for eight higher-risk patients.For three a specific indication for hospitalization was docu-mented: unstable heart failure, anticipated further surgery,and social reason. Reason to admit was ‘‘precautionary’’ forthe other five. One of these five developed pulmonary con-gestion a few hours after surgery, needing intravenous di-uresis; she was discharged well the next morning. The otherfour did not need any active intervention in the hospital,were discharged the next morning, and had no readmissionsor complications. Average length of stay was 2.7 days forpatients admitted for specific indications and 1.1 days forthose admitted for ‘‘precautionary’’ reasons (p < 0.05).

Discussion

The complication rate for these 515 patients was refresh-ingly low, possibly because all operations were done bysurgeons with extensive laparoscopic experience. The aimof this study was not to compare the overall results of thesefour surgeons to those of any other group but rather toassess the safety of routine outpatient surgery for the higher-risk patient. Both the increased conversion rate and hospitaladmission rate show that higher-risk outpatients did indeedhave more complications than their lower-risk counterparts.However, the results clearly show that routinely booking

higher-risk patients as outpatients is safe. Although theyhave a higher complication rate, complications needing hos-pital admission become readily apparent during the 6-h pe-riod of observation accorded to outpatients. Patients whoremain stable can be discharged without fear of delayedinstability which might have been prevented by hospitaladmission, as there were no readmissions or complicationsrelated to outpatient status among higher-risk patients whohad been discharged.

Of nine higher-risk patients admitted as a ‘‘precaution,’’eight needed no intervention and could have been treated asoutpatients. The pulmonary congestion developed by onepatient postoperatively was evident within hours and wouldhave been detected readily had she been booked as an out-patient. Possibly her congestion could have been preventedhad she been an outpatient. Intravenous fluids of outpatientsare discontinued early to allow them to become mobile andleave. Since she was booked as a ‘‘precautionary’’ inpa-tient, intravenous fluids were continued and may havehelped precipitate the congestion.

Readmission rates were no different for higher or lowerrisk patients. Of all 515 cholecystectomies over the 2 years,the readmission rate was 2% and rate of return visits toEmergency 6%; review suggested that overnight admissionmay have prevented about one-quarter of the Emergencyvisits (<2% of all patients) and none of the readmissions.These data give no cause to doubt the wisdom of outpatientcholecystectomy and the findings presented do not supportthe concept that higher-risk patients fare better with routineadmission to hospital. The opposite may be true, as sug-gested by the patient who developed pulmonary congestion:Hospitalization is an interventional treatment with its owncomplications.

This study reports the fate of actual outpatients and isnot an interpolation of inpatient results with speculation ofwhat would happen had they been outpatients. Most of thepatients of Saunders and co-workers seem to have beeninpatients, proving that keeping patients in the hospital didnot forestall the complications noted by them. Most of theminor complications documented Saunders and co-workersbecame evident 2–3 days after surgery and the more seriousones after 5–7 days. Since the standard for most surgeonswho still keep their patients in hospital after laparoscopicsurgery is a 1–2-day stay, the majority of complicationscould still go undetected at discharge.

These patients have no suitable inpatient controls, asoutpatient laparoscopic cholecystectomy, without selectionbecause of medical status or risk, was routine for the au-thor’s institution during this study. However, since no com-plications or readmissions related to outpatient status weredetected, it seems unlikely that a randomized controlledstudy could produce better results in the outpatient arm.

Table 2. Clinical characteristics of higher-risk outpatients and higher-risk inpatients (expressed as percent)

n >70 ASA > 3 >70 & ASA >3 MaleAcutechole

Minorcomplications Conversions Readmissions

Outpatients 61 69 52 20 41 16 26 0 3Admitted 24 63 58 25 17 8 17 21 4p n/a >0.05 >0.05 >0.05 >0.05 >0.05 >0.05 <0.05 >0.05

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Comparing these results to those of Saunders and co-workers, it seems that the question for a randomized con-trolled study to settle is not whether outpatient treatment isequally safe, but rather whether keeping patients in hospitalpromotes onset of complications.

Acknowledgments.The author is indebted to Ms. Diana Schouten and Dr.Robert A. Mustard for help with the statistical analyses, Ms. Sumi Ignatiusfor help with the records, and Dr. Remo Zadra for critical review of themanuscript.

References

1. Dawson B, Reed WA (1980) Anaesthesia for surgical outpatients. CanAnaesth Soc J 27: 409–411

2. Federated Ambulatory Surgery Association Special Study 1 (1987)Alexandria, Virginia, Federated Ambulatory Surgery Association

3. Gold BS, Kitz DS, Leckey JH, Neuhaus JM (1989) Unanticipatedadmission to the hospital following ambulatory surgery. JAMA 262:3008–3010

4. Keenan RL, Boyan CP (1985) Cardiac arrest due to anesthesia: a studyof incidence and causes. JAMA 253: 2373–2377

5. Marx GF, Mateo CV, Orkin LR (1973) Computer analysis of postan-esthetic deaths. Anesthesiology 39: 54–58

6. Meridy HW (1982) Criteria for selection of ambulatory surgical pa-tients and guidelines for anesthetic management: a retrospective studyof 1553 cases. Anesth Analg 61: 921–926

7. Natof HE (1980) Complications associated with ambulatory surgery.JAMA 244: 1116–1118

8. Natof HE (1984) Ambulatory surgery: patients with pre-existing medi-cal problems. Ill Med J 166: 101–104

9. Saunders CJ, Leary BF, Wolfe BM (1995) Is outpatient laparoscopiccholecystectomy wise? Surg Endosc 9: 1263–1268

10. Vacanti CJ, VanHouten RJ, Hill RC (1970) A statistical analysis of therelationship of physical status to postoperative mortality in 68,388cases. Anesth Analg 49: 564–568

11. Voitk AJ (1994) Outpatient cholecystectomy: implications for hospitalutilization. Leadership Health Serv 3: 21–23

12. Voitk AJ (1995) Routine outpatient cholecystectomy. Can J Surg 38:262–265

13. Voitk AJ (1996) Outpatient cholecystectomy. J Laparoendosc Surg 6:79–81

14. Wetchler BV (1988) Outpatient anesthesia. The geriatric outpatient.Probl Anesth 2: 128–131

1149

Original articles

Selection criteria for laparoscopic cholecystectomy in an ambulatorycare setting

C. R. Voyles,1,2 B. R. Berch1,2

1 Surgical Clinic Associates, University of Mississippi, Jackson, MS, USA2 Department of Surgery, University of Mississippi, Jackson, MS, USA

Received: 1 April 1997/Accepted: 27 May 1997

AbstractBackground:The ambulatory care center offers patient con-venience and reduced costs after uneventful laparoscopiccholecystectomy.Methods:A prospectively accumulated database of 1,750cholecystectomies performed by one surgeon in a hospitalsetting was analyzed to test criteria for ambulatory chole-cystectomy. Proposed criteria included age less than 65,absence of upper abdominal operations, and elective opera-tions in healthy patients at low risk for common bile ductstones.Results:Of 1,750 cholecystectomies, only 605 patients metall criteria for outpatient care. Discharge (from the in-hospital setting) was accomplished within 24 h of operationin 92% (first 3 years) and 98% (last 4 years) of selectedcases. Only one patient (0.2%, 1/605) was converted to anopen procedure; another was readmitted 30 h postopera-tively with hemorrhage from the liver bed.Conclusions:Laparoscopic cholecystectomy can be per-formed safely in an ambulatory care setting, given carefulselection and education of patients and documented expe-rience of the surgical team.

Key words: Laparoscopic cholecystectomy — Outpatient— Ambulatory

Laparoscopic cholecystectomy is the procedure of choicefor symptomatic cholelithiasis; most patients are dischargedfrom the hospital within 24–48 h. Many procedures arecurrently being performed in ambulatory care centers [2, 4,5]. However, the transition to the outpatient setting is ac-ceptable only if the complication rate is quite low and thepatients are reliably and safely discharged within 24 h.

In this study, we reviewed the prospectively accumu-lated data on 1,750 patients from a hospital setting in orderto verify a strategy for identifying those patients appropriatefor laparoscopic cholecystectomy in an ambulatory care fa-cility with overnight stay capabilities.

Materials and methods

From February 1990 through February 1997, 1,750 cholecystectomieswere performed by a single surgeon. Data were compiled prospectivelyregarding age, sex, final diagnosis, enzyme levels, common bile duct(CBD) diameter by preoperative ultrasound, operation performed, postopstay, and complications.

Criteria for the ideal patient were set by empirical methods:electiveoperations only; age less than 65; no significant underlying medical prob-lems; no previous upper abdominal operations; ‘‘no/low’’ risk for commonbile duct stones. The criterion of ‘‘no/low’’ risk was based on two preop-erative studies: (1) maximum CBD diameter by preoperative ultrasound#5 mm and (2) normal biochemical studies (alkaline phosphatase, serumglutamic oxaloacetic transaminase, bilirubin, and amylase) [7].

The course of selected ‘‘ideal’’ patients was then evaluated for com-pleted laparoscopic cholecystectomy, hospital stay# 24 h, and avoidanceof significant complications.

Results

Of the 1,750 cholecystectomies performed, 10% were ex-cluded from outpatient consideration because their chole-cystectomy was performed incidental to other abdominaloperations (Table 1). Another 25% were excluded becauseof emergencies (acute cholecystitis, suspected CBD stones,jaundice, pancreatitis, etc.), 19% because of age over 65,and 1% because of underlying medical problems or upperabdominal problems. Of the remaining 757 patients, one-fifth were excluded because of elevated liver enzymes and/or CBD dilatation. Therefore, the remaining sample of‘‘ideal’’ patients included 605 of the 1,750 patients or 35%of the total number.

Conversion from laparoscopic to open cholecystectomywas necessary in only one of 605 patients in order to betterdefine the anatomy. One patient was discharged after 18 h,only to return with bleeding from the liver bed; transfusionand reoperation were required.

Correspondence to:C. R. Voyles, 1421 North State Street[304 Jackson,MS 39202, USA

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© Springer-Verlag New York Inc. 1997Surg Endosc (1997) 11: 1145–1146

The analysis of postoperative stay was separated intotwo periods (1990–1992 and 1993–1996). The percentageof ideal candidates discharged in 24 h or less was higher inthe most recent period with 98% of patients being dis-charged (Table 2). Reasons for hospitalization longer than24 h included conversion to an open operation (one) andnausea (six).

During the last year of the study, only 25% of the‘‘ideal’’ patients were discharged the same day from thehospital setting. Overnight stay was often necessary becauseof late afternoon operations. Supported by this study, wehave begun to perform laparoscopic cholecystectomy in anambulatory care facility which has overnight capability. Thefacility charges for laparoscopic cholecystectomy are 30%less in the ambulatory care center (approximately $2,700 vs$4,000).

Discussion

Within the last decade, cholecystectomy has advanced froma 4- to 5-day hospitalization with the open procedure to acomplete outpatient procedure for selected patients. The pa-tient benefits of laparoscopic cholecystectomy in the ambu-latory care setting include convenience and reduced costs[1, 2, 4, 5]. The benefits to the surgeon also include con-venience, plus a more orderly operative schedule becausedisruptions are avoided that result from emergencies in thehospital setting [4, 5]. The benefits of convenience and re-duced costs are real and laudable as long as patient safety isnot compromised.

Since conversion from a laparoscopic to an open proce-dure generally requires hospitalization, it is important to iden-tify any preoperative risk factors that would increase therisk for an open procedure. Interestingly, the risk factors for‘‘conversions’’ are the same factors that were originallyjudged to be relative contraindications to laparoscopic cho-lecystectomy [8]. These risk factors include advanced age,obesity, previous operations, pregnancy, and signs or symp-toms of either acute cholecystitis or common bile duct stones.

The accuracy of stratifying risk for common bile ductstones has been questioned by many investigators [3]. In ourprevious study, a ‘‘no/low’’ risk category of patients was

defined by normal liver enzymes and common bile ductdiameter (#5 mm). In the ‘‘no/low’’ risk patients, operativecholangiograms were not obtained as long as there were nosigns of acute cholecystitis or cystic duct abnormality [7].With a 7-year follow-up, there has been no clinical evidenceof choledocholithiasis in over 800 patients judged to be at‘‘no/low’’ risk and in whom operative cholangiograms werenot obtained. Proponents of routine cholangiograms arguethat 4–5% of patients have unsuspected stones in spite ofpreoperative studies. The discrepant findings must be ex-plained by either false-positive studies or else clinically in-significant findings by the ‘‘routine’’ cholangiographers;less likely, our follow-up may have missed recurrent dis-ease. While the controversy about routine cholangiographyis likely to continue, all agree that the availability of chol-angiography equipment is mandatory in both hospital set-tings and ambulatory care centers.

The safety of laparoscopic cholecystectomy in selectedpatients in an ambulatory center has been supported by sev-eral studies. However, early surveillance with open com-munication is essential to reduce the risks associated withunrecognized complications. The progressively shortenedfacility stay must be offset by excellent patient teachingabout the expected postoperative course and early officefollow-up. In retrospect, the one patient who had a post-operative hemorrhage would have benefitted from a 48-hrather than a 24-h hospitalization. Increasing pain, nausea,or fever after the first postoperative day should be carefullyevaluated since complications such as biliary leaks, intesti-nal injury, and hemorrhage may not be fully apparent withinthe first 24 h.

As a caveat specific to most laparoscopic studies, thegood results reported by many experienced surgeons in es-tablished laparoscopic centers may not be readily duplicatedin less experienced centers [6].

Conclusion

Given careful selection of patients, laparoscopic cholecys-tectomy can be safely performed in an ambulatory caresetting. Our proposed criteria for patient selection is sup-ported by an acceptably low complication rate and earlydischarge.

References

1. Arregui ME, Davis CJ, Arkush A, Nagan RF (1991) In selected patientsoutpatient laparoscopic cholecystectomy is safe and significantly re-duces hospitalization charges. Surg Laparosc Endosc 1: 240–245

2. Farha GJ, Green BP, Beamer RL (1994) Laparoscopic cholecystectomyin a freestanding outpatient surgery center. J Laparoendosc Surg 4:291–294

3. Koo KP, Traverso LW (1996) Do preoperative indicators predict thepresence of common bile duct stones during laparoscopic cholecystec-tomy? Am J Surg 171: 495–499

4. Llorente J (1992) Laparoscopic cholecystectomy in the ambulatory sur-gery setting. J Laparoendosc Surg 2: 23–26

5. Reddick EJ (1992) Laparoscopic cholecystectomy in freestanding out-patient centers. J Laparoendosc Surg 2: 65–67

6. Southern Surgeons Club (1991) A prospective analysis of 1518 laparo-scopic cholecystectomies. NEJM 324: 1073–1078

7. Voyles CR, Sanders DL, Hogan R (1994) Common bile duct evaluationin the era of laparoscopic cholecystectomy. Ann Surg 219: 744–752

8. Zucker KA, Bailey RW, Gadacz TR, Imbembo AL (1991) Laparoscopicguided cholecystectomy. Am J Surg 161: 36–44

Table 1. Reasons for exclusion (1,750 patients)

Reason No. Balance

Incidental procedure 170 1,580 (90%)Emergency 446 1,134 (65%)Age >65 356 778 (44%)Complex medical problems 21 757 (43%)Increased risk for CBD stones 152 605 (35%)

Table 2. Hospital stay#24 hours

Years 1990–1992 1993–1996

All electives 501/590 (85%) 488/544 (90%)All electives <65 370/406 (92%) 340/351 (97%)All electives <65,

no/low risk for stones285/309 (92%) 289/296 (98%)

1146

Laparoscopic Nissen fundoplication in children under 2 years of age

O. Zamir, R. Udassin, D. Seror, A. Vromen, H. R. Freund

Department of Surgery and Pediatric Surgery, Hadassah University Hospital Mount Scopus, and the Hebrew University-Hadassah Medical School,Jerusalem, 91240 Israel

Received: 16 April 1997/Accepted: 30 June 1997

AbstractBackground: Antireflux operations have been recom-mended for infants and children suffering from complica-tions related to gastroesophageal reflux (GER). In recentyears, the laparoscopic approach has been used increasinglyfor antireflux surgery in adult patients. This is our initialexperience with Nissen fundoplication in infants and chil-dren under 2 years of age.Patients:We operated on 11 patients weighing between 3.0and 10.0 kg. The main indications for surgery were GER-induced aspiration pneumonia and failure to thrive, in spiteof intensive conservative treatment. All patients except onehad an associated neurological abnormality, including sixpatients with familial dysautonomia.Results:All attempted operations were completed success-fully laparoscopically, with only a few postoperative com-plications and acceptable short-term results. The clinicalconsiderations and technical aspects unique to this specificgroup of patients are discussed.Conclusion:Laparoscopic Nissen fundoplication is feasible,safe, and effective, even in very small babies.

Key words: Laparoscopy — Fundoplication — Infants andchildren — Gastroesophageal reflux

Gastroesophageal reflux (GER) may result in severe com-plications in infants and young children, including failure tothrive, recurrent aspiration pneumonia, apnea, asthma, andpeptic stricture of the esophagus. The problem is especiallycommon in neurologically impaired children. It has beenwidely accepted in recent years that even small childrenwith severe symptomatic GER, including those with neuro-logical impairment, may benefit from an antireflux opera-tion such as Nissen fundoplication [3, 6, 10]. The very sameconclusion was drawn for children with familial dysautono-mia [12].

With advances in laparoscopic technique, this approach

was applied to various antireflux procedures in adults, in-cluding Nissen fundoplication. Recent reports suggestedthat Nissen fundoplication can be safely accomplished lapa-roscopically in most adult patients who need an antirefluxoperation, with acceptable morbidity and short-term results[2, 4, 5]. There have been a number of recent reports oflaparoscopic fundoplication in children and adolescents [7–9, 11, 13]. In this report, we describe our experience withNissen fundoplication in 11 infants and children who were<2 years of age at the time of operation. Some specifictechnical aspects and difficulties encountered in these smallbabies are discussed.

Patients

Between October 1994 and November 1996 11 children(seven male and four female) <2 years of age (range, 3–24months; mean, 12.2 months) underwent modified Nissenfundoplication at Hadassah University Hospital Mount Sco-pus. Their body weight at the time of operation rangedbetween 3.0 and 10.0 kg (mean, 7.2 kg). All children exceptone had associated abnormalities, mainly familial dysauto-nomia (six patients) or other neurological deficit (four pa-tients). In all cases, conservative treatment was initially at-tempted; surgery was undertaken only after failure of allnonsurgical measures. The main complications leading tooperation were recurrent lung infections and failure to thrive(Table 1). Three patients were transferred for surgery di-rectly from the Department of Pediatrics following pro-longed hospitalization for persistent vomiting and severerecurrent aspiration pneumonia. The indications for surgery,the preoperative work-up, and other relevant clinical detailsare shown in Table 1.

During the study period, two babies with apparent delayin gastric emptying on barium meal or nuclear scan wereexcluded from the laparoscopic approach because this find-ing was considered an indication for pyloroplasty. In onepatient with evidence of gastric emptying delay, laparoscop-ic procedure was employed, but pyloromyotomy was addedat the end of the operation through a short supraumbilicalincision. Two other babies underwent an open procedurebecause of their parents’ preference. The parents of all pa-Correspondence to:O. Zamir

Surg Endosc (1997) 11: 1202–1205

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© Springer-Verlag New York Inc. 1997

tients were given a detailed explanation of the laparoscopicprocedure, and written consent was obtained in each case.

Surgical technique

The procedure was performed under general endotrachealanesthesia with the child lying prone near the lower end ofthe operating table and the surgeon standing between thepatient’s legs. A urethral catheter and a nasogastric tubewere routinely inserted. A CO2 pneumoperitoneum was es-tablished using a Veress needle inserted through an infra-umbilical incision. Pressures of 7–8 mm Hg only were usedin the smaller babies andù12 mm Hg in larger children. Anangled 30° 10-mm scope was used in the larger children,while a 5-mm scope was used in three children weighing <5kg. Four additional 5-mm ports were placed under directvision and secured in place with a suture. A right lateralsubcostal port was used for retraction of the liver anteriorlywith a blunt grasper, and two ports, located one at each sideof the camera port, were used for bimanual surgery. Thefifth port was located on the left side for caudal traction of

the stomach and for traction of the esophagus, which wasencircled with a tape following its mobilization. After place-ment of ports, the operating table was placed in a reverseTrendelenburg position. Pediatric 3.5-mm short instruments(Jarit Surgical Instruments, Inc, Hawthorne, NY, USA) andadult 5-mm instruments were used.

The upper part of the gastrohepatic omentum and thephrenoesophageal ligament were first divided using curvedbipolar coagulating scissors (Everest Medical, Minneapolis,MN, USA). The esophagus was mobilized using a bluntdissector. The plane of dissection could be identified clearlyand mobilization was easily accomplished in these smallchildren because of the minimal fat tissue present betweenthe esophagus and the crura and in the hiatus. A short rubbersling was usually placed around the freed esophagus to fa-cilitate its manipulation while expanding the retroesopha-geal space and during construction of the fundic wrap. Inmost cases, division of the short gastric vessels was notnecessary. In two patients, partial division of the short gas-tric vessels was necessary to accomplish a tension-freewrap. One or two silk sutures were used to approximate thecrura behind the esophagus.

Table 1. Clinical data

Age(mo)sex

Weight(kg)

Associateddisease

Indication forsurgery

Preoperativework-up Procedure

Operationtime(min)

Hospitalstay(days)

Follow-upperiod(mo)

24 Male 8.2 Familial dysauto-nomia

Recurrent pneu-monia & ap-neic spells

Milk scan NF, G, App 200 10 29

7 Female 4.7 Familialdysautonomia

Aspirations,recurrentpneumonia &failure to thrive

Milk scan NF, G, App 195 17 24

9 Male 8.7 Familialdysautonomia

Recurrentpneumonia

pH study, bariummeal, milkscan,esophagoscopy

NF, G, App 200 9 22

15 Male 8.8 Familialdysautonomia

Recurrentpneumonia &failure to thrive

Milk scan NF, G, App 265 8 20

11 Male 7.4 Cerebral palsy Recurrentpneumonia &aspirations

Barium meal NF, G, App 225 9 16

9 Female 7.7 Recurrentpneumonia,aspirations, &asthma

pH study, bariummeal

NF, G, App 225 9 16

6 Female 4.9 Cerebral palsy &intractableseizures

Aspirations &persistentvomiting

Barium meal NF, G, App 140 7 15

12 Male 8.3 Familialdysautonomia

Persistentvomiting,dehydration, &choking attacks

Milk scan NF, G App,pyloroplasty

185 16 14

19 Male 10.0 Familialdysautonomia

Recurrentpneumonia

Milk scan NF, G, App 190 7 11

19 Female 8.0 Microcephaly Failure to thrive& recurrentpneumonia

pH study, bariummeal,esophagoscopy

NF, G 210 7 9

3 Male 3.0 Methylmalonicacidemia &severeneurologicaldeficit

Failure to thrive& persistentvomiting

Milk scan NF, G 270 7 5

NF, Nissen fundoplication; G, gastrostomy; App, appendectomy.

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After passing the fundus behind the esophagus, the na-sogastric tube was replaced by a bougie (18–26 Fr) to assurea floppy fundoplication. A 2–3-cm long wrap was con-structed using interrupted nonabsorbable sutures that werepassed through both the stomach and the esophageal walland tied with either extracorporeal or intracorporeal knot-ting technique. Special care was taken to avoid entrapmentof the vagus nerves. Pledgets were used in seven cases. Inall but two patients, appendectomy was also performed toavoid future confusion with the frequently occurring attacksof abdominal pain in these children.

At the end of the procedure, a point on the anteriorstomach wall suitable for gastrostomy was selected andpulled through the trocar site located in the left hypochon-drium, which was slightly enlarged. A tube gastrostomy wasfashioned, securing the stomach wall to the fascia with afew stitches. Since entrapment of omentum occurred post-operatively in two of our early cases, it is now our practiceto close the fascia of all 10-mm ports as well as the 5-mmports. All wounds were closed with subcuticular absorbablestitches.

Results

All 11 attempted laparoscopic fundoplications were suc-cessfully completed as such. The mean operating time was210 min (range, 140–270 min). Because of their poor pre-operative respiratory status, most patients needed aggres-sive pulmonary physiotherapy in an intensive care unit post-operatively, but only two patients required continuous me-chanical ventilation for 24–48 h after surgery. Enteralfeeding was gradually started 2–4 days postoperatively.Nine children had a relatively smooth recovery and weredischarged home in 7–10 days after surgery. In two chil-dren, entrapment of omentum in 5- and 10-mm portswounds required surgical repair in the early postoperativeperiod, prolonging their hospital stay to 16 and 17 days,respectively. The mean postoperative hospital stay was 9.6days.

In a follow-up period of 5–29 months (mean, 16.5months), all patients reportedly stopped vomiting. Episodicnausea or retching persisted in two children with familialdysautonomia, apparently as part of their primary disease.Leakage around the gastrostomy tube occurred in two pa-tients and was successfully treated on an ambulatory basis.Nine patients showed complete resolution of symptoms re-lated to GER. Two patients required readmission to thehospital because of pulmonary infection. Barium study inboth of them showed an intact fundoplication in an intra-abdominal position, with no evidence of GER. We found noevidence of delayed gastric emptying in the postoperativefollow-up period in any of our patients.

Discussion

In recent years, laparoscopic Nissen fundoplication hasbeen performed with increasing frequency in adult patientswith symptomatic GER because it causes minimal trauma tothe abdominal wall and supposedly eases patient recovery

[5]. Our initial experience demonstrates that Nissen fundo-plication can be accomplished successfully and safely usingthe laparoscopic approach in very small babies sufferingfrom severe GER.

Infants and children who are candidates for antirefluxprocedure differ in many aspects from the adult population.In adults, GER is typically associated with hiatal hernia andis usually unrelated to any other abnormality. In children, onthe other hand, there is usually no hiatal hernia, but clini-cally significant GER is often associated with neurologicalimpairment, metabolic abnormality, or some other severeunderlying disease. Therefore, even after successful surgicalresolution of GER, these babies often remain very sick dueto their primary disease.

Many children undergoing antireflux operation are atincreased risk because of chronic parenchymal lung damagedue to recurrent episodes of pneumonia and because theyare often severely malnourished. Operative risk is especiallyhigh in children with familial dysautonomia [1, 12]. Con-comitant impairment of gastrointestinal motility is alsounique to the pediatric population. In particular, impairmentof the swallowing mechanism and delayed gastric emptyingshould be taken into account by the surgeon. Hence, whenthe swallowing mechanism is impaired, gastrostomy shouldbe constructed for postoperative feeding or fluid adminis-tration to prevent persistent aspirations. Likewise, the sur-geon should consider pyloroplasty when there is preopera-tive evidence of delayed gastric emptying [3]. In this case,we usually prefer an open procedure, although a pyloro-plasty can be accomplished through a small laparotomy in-cision at the end of the laparoscopic procedure. This optionwas elected in one case in this series.

There are several technical concerns in laparoscopicNissen fundoplication that are unique to infants and smallchildren. Because the operating space is very small, it isnecessary to use specially designed short instruments and tohandle them with great care. To prevent dislocation, thetrocars need to be secured to the skin by stitches. The pneu-moperitoneum should be maintained at pressures as low as7–8 mm Hg. Elevation of pressure may cause difficulty inventilation, with resultant hypercarbia. It is sometimes nec-essary to increase the pneumoperitoneum pressure tempo-rarily, for example during suturing, and to immediately de-flate the abdomen if expiratory CO2 increases or any diffi-culty in ventilation is encountered. Insufflation of a largevolume of cold CO2 may cause hypothermia in small ba-bies. Therefore, loss of the pneumoperitoneum must be keptto a minimum during surgery.

At the same time, the minimal fat around the esophagusin these small babies and the absence of hiatus hernia makethe definition of the dissection planes clearer. Thus, thedissection itself, including mobilization of the esophagus,identification of the vagus nerves, and construction of thefundic wrap are easier in small children than in adults. Fur-thermore, it is usually unnecessary to divide the short gastricvessels to achieve a tension-free wrap.

Small children who need an antireflux operation oftensuffer from chronic lung disease, which makes them espe-cially susceptible to postoperative lung complications. Thelaparoscopic approach seems to minimize these complica-tions. The minimal trauma to the upper abdominal wall inthis approach results in less impairment of respiration and

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minimizes the need for narcotics and sedatives postopera-tively. Recent reports suggested that recovery was smootherfollowing laparoscopic antireflux operations than after openprocedures, with comparable short-term results [11, 13].

We conclude that laparoscopic Nissen fundoplication isfeasible and safe in very small children and infants and thatit appears to offer some advantages over the standard opentechnique.

References

1. Beilin B, Maayan C, Vatashski E, Shulman D, Vinograd I, AronsonHB (1985) Fentanyl anesthesia in familial dysautonomia. AnesthAnalg 64: 72–76

2. Dallemagne B, Weerts JM, Jehacs C, Markiewicz S (1991) Laparo-scopic Nissen fundoplication; preliminary report. Surg Laparosc En-dosc 1: 138–143

3. Fonkalsrud EW, Foglia RP, Ament ME, Berquist W, Vergas J (1989)Operative treatment of the gastroesophageal reflux syndrome in chil-dren. J Pediatr Surg 24: 525–529

4. Geagea J (1991) Laparoscopic Nissen’s fundoplication; preliminaryreport on ten cases. Surg Endosc 5: 170–173

5. Jamieson GG, Watson DI, Jones RB, Mitchel PC, Anvari MA (1994)Laparoscopic Nissen fundoplication. Ann Surg 220: 137–145

6. Kazerooni NL, VanCamp J, Hirschi RB, Drongowski RA, Coran AG(1994) Fundoplication in 160 children under 2 years of age. J PediatrSurg 29: 677–681

7. Lloid DM, Robertson GSM, Jonstone JMS (1995) Laparoscopic Nis-sen fundoplication in children. Surg Endosc 9: 781–785

8. Lobe TE, Schropp KP, Lunsford K (1993) Laparoscopic Nissen fun-doplication in childhood. J Pediatr Surg 28: 358–361

9. Meehan JJ, Georgeson KE (1996) Laparoscopic fundoplication in in-fants and children. Surg Endosc 10: 1154–1157

10. Randolph J (1983) Experience with the Nissen fundoplication for cor-rection of gastroesophageal reflux in infants. Ann Surg 198: 579–584

11. Szold A, Udassin R, Maayan C, Vromen A, Seror D, Zamir O (1996)Laparoscopic modified Nissen fundoplication in children with familialdysautonomia. J Pediatr Surg 31: 1560–1562

12. Udassin R, Seror D, Vinograd I, Zamir O, Nissan S (1992) Nissenfundoplication in the treatment of children with familial dysautonomia.Am J Surg 164: 332–336

13. Zee van der DC, Bax NMA (1996) Laparoscopic Thal fundoplicationin mentally retarded children. Surg Endosc 10: 659–661

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Minimally invasive treatment of acute biliary pancreatitis

F. Ricci, G. Castaldini, G. de Manzoni, G. Borzellino, L. Rodella, R. Kind

First Department of General Surgery, University of Verona, 37126 Verona, Italy

Received: 23 September 1996/Accepted: 2 April 1997

AbstractBackground:Stones of the common bile duct are the mostimportant factor in acute pancreatitis (AP). Endolaparo-scopic surgery plays a well-recognized role in the treatmentof this pathology.Methods:From January 1992 to December 1995 we ob-served 62 cases of acute biliary pancreatitis (ABP). In 57cases (4 93.4%) we proposed a minimally invasive treat-ment, based on performance of endoscopic retrograde chol-angiopancreatography (ERCP) combined with endoscopicsphincterotomy (ES) and then of laparoscopic cholecystec-tomy (LC).Results:ERCP was attempted in emergency in 40/57 casesand successfully done in 34 cases. An ES was performed inall but two cases. In 51 patients we performed LC. Theoverall morbidity was 8.9% with no mortality.Conclusions: In the case of ABP early treatment canachieve the restoration of patency of the papilla, reducingthe risk of associated cholangitis and the development ofpancreatic necrosis. The cholecystectomy prevents the riskof relapse of ABP.

Key words: Acute biliary pancreatitis — Endoscopic ret-rograde pancreatography — Laparoscopic cholecystectomy

Acute pancreatitis (AP) is a disease of by no means negli-gible social importance with an annual incidence of ap-proximately 10 cases/100,000 population [23, 25] and car-ries a mortality rate of around 10% [2, 15].

Stones of the common bile duct are undoubtedly themost important etiological factor in AP. On the basis of thedata reported in the literature, biliary etiology is responsiblefor 50–60% of cases of AP [2, 12, 25] with incidencesranging from 16 to 70% [20]. While, on the one hand, thesevariations reflect the different ethnic and cultural character-

istics of the patients or the dyshomogeneity of the diagnos-tic criteria adopted, on the other, it is undeniable that asubstantial percentage of cases of AP defined as ‘‘idio-pathic’’ are in actual fact due to the presence of microli-thiasis or bile crystals [17, 22]. Thus, the relative incidenceof biliary etiology would appear to be underestimated, somuch so indeed that in our own experience such an etiologyhas been confirmed in 75% of the AP cases observed [3].

A number of investigators, moreover, believe that acutebiliary pancreatitis (ABP) will relapse in 50% of caseswithin 6 months if the patient does not undergo a cholecys-tectomy [10, 18–21, 28].

The development and increasingly widespread use ofendolaparoscopic surgery has enabled us to propose a mini-mally invasive approach for this type of disease, accordingto a therapeutic protocol involving, first, the performance ofemergency endoscopic retrograde cholangiopancreatogra-phy (ERPC) combined with endoscopic sphincterotomy(ES), and, once the acute attack has been resolved, laparo-scopic cholecystectomy (LC).

Particular concomitant pathological situations such asacute cholecystitis or an intraperitoneal fluid collection canalso benefit from minimally invasive treatment by means ofUS-guided skin puncture. With a view to assessing the ef-ficacy and validity of minimally invasive treatment we re-viewed the data on patients admitted to our department forAP over the period from January 1992 to December 1995.

Materials and methods

Over the period from January 1992 to December 1995 some 82 patientswith a diagnosis of AP were admitted to the Verona University 1st De-partment of General Surgery. As regards the etiology of the AP, we ob-served alcohol abuse in 14 cases (17%), inflammatory or neoplastic diseaseof the duodenal papilla in four cases (4.9%), postoperative onset of AP inthree cases (3.6%), and biliary etiology in 61 cases (74.4%).

The diagnosis of ABP was based on medical history (established evi-dence of gallstones, previous episodes of biliary colic, absence of alcoholabuse), suggestive abnormalities in blood-chemistry tests (ALP > 250 IU/l,ALT > 100 IU/l, bilirubin > 25 mmol/l), and, at ultrasonography of the bileducts, (lithiasis, microlithiasis, or bile sludge in the gallbladder, dilatationof the bile ducts, or choledocholithiasis).

In the ABP cases, the patients were submitted to a minimally invasiveCorrespondence to:F. Ricci, I Divisione Clinicizzata di Chirurgia, Osped-ale Civile Maggiore, Piazzale Stefani, 1, 37126 Verona, Italy

Surg Endosc (1997) 11: 1179–1182

SurgicalEndoscopy

© Springer-Verlag New York Inc. 1997

treatment according to a protocol involving the execution of an emergencyERCP combined with ES for the purposes of achieving early removal ofthe obstacle to pancreatic outflow. Once the acute attack had been resolved,the patient was kept in the department and a laparoscopic cholecystectomywas performed in order to prevent any relapse of AP. This treatment waspossible in 57/61 cases of ABP (4 93.4%).

The mean age of these patients was 52.1 years (range: 24–86); in 19/57cases (33.3%) the patients were aged > 70 years. The male/female ratio was1.1:1. We used Ranson scores for a prognostic assessment: We thus ob-served ‘‘mild’’ AP (Ranson scores < 3) in 46/57 cases (80.7%) and ‘‘se-vere’’ AP (Ranson scores$ 3) in the other 11 cases (19.3%). Within thelatter group we observed scores of 3–4 in eight cases (with a mean mor-tality rate of 16% according to Ranson), scores of 5–6 in two cases (re-ported mortality 40%), and a score of 7 in one case (reported mortality100%). In the more clinically demanding cases, or when ultrasonographyrevealed the presence of intraabdominal fluid collections, an emergencyabdominal CT scan was performed.

Results

In our study we observed a biliary etiology of AP in 61/82cases (74.4%). In 4/61 cases (6.5%) a pancreatic necrosec-tomy was performed with the positioning of multiple ab-dominal drains (one death). These patients were referred toour department from another hospital as a result of deterio-ration of their general condition. A mean period of 7 days(range: 4–11) had elapsed since onset of symptoms. Wetherefore excluded these four cases from our analysis.

In 57/61 cases of ABP (93.4%) we examined the patientwithin only a few hours of onset of symptoms. It was thuspossible to offer these patients the minimally invasive treat-ment described above.

The ERCP was attempted in all 57 patients. In 40 cases(70.2%) the procedure was an emergency ERCP (within 48h of onset of symptoms) and proved successful in 34 cases.The feasibility of the examination in emergency conditionswas therefore 85%. In the remaining 17 cases the procedurewas attempted after 48 h and proved successful in 15 cases(88.2% feasibility). In eight cases (three of which with a‘‘severe’’ prognosis) the procedure failed at the first at-tempt. The causes of failure were the presence of substantialduodenal edema preventing visualization of the papilla (sixcases), a bulky duodenal diverticulum (one case), and theonset of an allergic reaction to the iodinized contrast me-dium (one case). In five cases of duodenal edema, a secondERCP was successfully attempted after a mean interval of 8days (range: 6–12). The remaining three patients, whose APattack was mild, refused to repeat the examination and de-clined any further surgical treatment; they were treated with

medical therapy alone and discharged once the acute attackhad been resolved. These patients are, of course, excludedfrom the analysis of the data on the cholangiographic studyof the main bile duct and ES. In all, the ERCP was success-ful in 54/57 cases (94.7%).

We observed the presence of common bile duct stones(CBDS) in 26/34 patients (76.5%) within 48 h and in 10/20patients (50%) after 48 h. If we consider only the 11 patientswith a severe prognosis, the respective percentages were87.5% (7/8 patients) and 66.6% (2/3 patients). Dilatation ofthe common bile duct (CBDD) was observed in 23/34 pa-tients (67.6%) within 48 h and in 9/20 patients (45%) after48 h. In the cases with a severe prognosis, the respectivevalues were 87.5% (7/8 patients) and 33.3% (1/3 patients).In particular, we observed CBDD without evidence ofCBDS or edema of the papilla in six cases. In these patients,after execution of ES, we observed an out-gushing of densebile (Table 1).

The presence of papillary edema was observed in 13/54cases (24%), five of whom had a severe prognosis. In sixcases this finding was not associated with CBDD or CBDS.

We performed ES in 52/54 cases (96.3%). The proce-dure was not performed in the other two cases, since, in onecase, the papilla was broad enough, while, in the other case,we managed to perform only a pre-cut of the papilla, which,however, was sufficient to guarantee bile outflow.

Extraction of choledochal stones by means of a Dormiabasket was necessary in 38 cases and mechanical lithotripsyin five cases. In 15 cases a nasobiliary probe was positionedat the end of the procedure, so as to be able to perform acholangiographic follow-up examination a few days later.

In this phase we registered 7% morbidity (four cases ofbleeding of the papilla). The mortality rate was nil.

The results of laparoscopic cholecystectomy are shownin Table 2.

The AP was accompanied by acute cholecystitis in fourcases. These patients were submitted at entry to US-guidedpercutaneous cholecystostomy, with a rapid improvement inpain symptoms, leukocytosis, and hyperpyrexia.

In three of the eight patients in whom ERCP failed at thefirst attempt owing to duodenal oedema, ultrasonographyrevealed an overdistended gallbladder with walls of normalthickness. In these cases we performed a US-guided percu-taneous cholecystostomy and later a transcholecystic chol-angiography documenting the presence of a papillary ob-stacle to bile outflow.

Table 1. ERCP findingsa

Timing ofERCP

Predictedseverity CBDS CBDD

Before 48 hb Mild 19/26 cases (73.1%) 16/26 cases (61.5%)Severe 7/8 cases (87.5%) 7/8 cases (87.5%)All cases 26/34 cases (76.5%) 23/34 cases (67.6%)

After 48 hb Mild 8/17 cases (47%) 8/17 cases (47%)Severe 2/3 cases (66.6%) 1/3 cases (33.3%)All cases 10/20 cases (50%) 9/20 cases (45%)

a Common bile duct stones (CBDS) and common bile duct dilatation (CBDD) related to severity of ABPand timing of ERCPb From the onset of symptoms

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In one case of acute necrotizing-hemorrhagic pancreati-tis the CT scan performed at entry revealed a fluid collec-tion occupying the right parietocolic sulcus. An 8-Fr drain-age catheter was therefore positioned via a US-guided per-cutaneous route, enabling the collection to be drained off.Repeated US follow-up scans showed progressive reductionof the collection.

In one last case, we observed a pancreatic collectionlocated in the body-tail of the pancreas developing into apseudocyst. This mass was responsible for pain in the lefthypochondriac region associated with a sensation of nauseaand vomiting due to gastric compression. After performanceof an ERCP, combined with ES, had ruled out the existenceof any communication between the pseudocyst and the pan-creatic ductal system, the patient was submitted 51 daysafter the AP attack to US-guided percutaneous drainage ofthe pseudocyst with placement of a 7-Fr catheter. Afterdischarge, the patient was followed up on an outpatientbasis with repeated US scans. After 62 days, the drainagecatheter was removed and the patient underwent laparo-scopic cholecystectomy.

The mean hospital stay for the entire treatment was 14.9days (range: 7–37). This value was 12.7 days (range: 7–28)in cases of mild AP and 21.5 (range: 12–3) in cases ofsevere AP.

All the patients were followed-up. No patient had re-lapse of ABP after a median follow-up of 6 months (range6–54).

Discussion

We should make it clear right from the outset that in thisstudy attention is focused on the group of 57 patients suf-fering from ABP and treated with wholly minimal invasivetherapy: ERCP + ES ± percutaneous cholecystostomy orpercutaneous drainage of peritoneal collections + laparo-scopic cholecystectomy.

An attack of ABP will occur in the course of time inroughly 4–8% of patients suffering from gallstone disease[1, 19, 20]. In actual fact, ABP is a nosological entity whichis continually and progressively on the increase. In our ownexperience, we have observed a biliary etiology of AP inabout 75% of cases (61/82 patients).

Analysis of the literature shows that, whereas, on theone hand, the mild forms of ABP evolve favorably, in mostcases with medical therapy alone [4, 7, 8], on the other, thesevere forms are characterized by local and/or systemiccomplications. Mortality rates of 8–10% are still being re-ported today in AP populations [2, 12, 15].

ERCP combined with ES is today one of the mainstaysin the treatment of ABP. However, there is no agreementamong the various investigators as to the indications andactual efficacy of these procedures when performed in theemergency setting (within 48 h). A number of authors [1, 7,16, 24] believe that this combination is indicated in the earlyphase only in the severe forms of ABP or in cases present-ing associated cholangitis or CBDS, since ERCP + ES is byno means complication-free and the mild forms would notappear to benefit noticeably from the procedure. Other in-vestigators [6, 13, 21, 27] stress the importance, both diag-nostic and therapeutic, of ERCP + ES in cases of AP, re-gardless of the prognostic assessment. Some other authors[5, 14, 26] support the use of preoperative ERCP only se-lectively, based on persistent elevated pancreatic and/orliver enzymes or evidence of CBDS by ultrasonography. Ifthese criteria are not met, it is possible to perform an LCwith routine intraoperative cholangiography and, if neces-sary, laparoscopic CBD exploration, with stone retrievalthrough the cystic duct or saline flushing of the CBD.

Our own feeling is that emergency ERCP (within 48 h)should be performed in all cases of AP of confirmed orstrongly suspected biliary etiology. In our experience, theprocedure proved successful in the emergency setting inapproximately 85% of cases, revealing the presence ofCBDS and dilation of the common bile duct in 76.5% and67.6% of cases, respectively. An ES was performed in prac-tically all cases. The approach in the early phase yielded acorrect etiological diagnosis as well as ensuring that thepatient received immediate therapy through cleansing of themain bile duct. These maneuvers, moreover, appear to besafe even in elderly patients, who, in our patient sample,account for 33.3% of the total. The overall morbidity ratewe observed was 7% and the mortality rate nil.

The execution of laparoscopic cholecystectomy, prefer-ably performed in the course of the same hospital stay afterresolution of the acute attack, permits definitive treatment ofthe disease, preventing recurrences of ABP. As we havealready reported, the risk of relapse in patients with ABP is50% of cases within 6 months of the first attack. The op-eration, which other authors do not regard as necessary afterexecution of an ES and which is now standardized in termsof surgical technique, does not take much longer to performthan in routine cases (90 min on average). Perioperativecholangiography, which we perform in 92.1% of cases, is auseful means of confirming both the anatomical picture andthe clearing of the bile duct with good outflow at papillarylevel.

The best results in terms of patient and socioeconomic

Table 2. Results of laparoscopic cholecystectomy, performed in 51 cases

Performed successfully 51/51 cases 100%Converted to open cholecystectomy 0/51 cases 0%Intraoperative cholangiography 47/51 cases 92.1%Performed during same hospital stay; 34/51 cases 66.6%

mean interval from ERCP 7.3 days (range 5–21) –Performed during 2nd scheduled admission 17/51 cases 33.3%

mean interval from ERCP 42 days (range 18–65) –Morbility 1/51 cases 1.9%Mortality 0/51 cases 0%

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benefit were achieved when the cholecystectomy was per-formed in the course of the same hospital stay, once theacute attack had been resolved (reversion of serum amylaseand leukocytosis values to normal).

US-guided transhepatic percutaneous cholecystostomyis indicated in cases of cholecystitis associated with ABP.This procedure affords a rapid improvement in the patient’sclinical course, thereby laying the foundations for perform-ing the minimally invasive treatment [11]. Furthermore, af-ter failure of ERCP, percutaneous cholecystostomy allowsdecompression of the bile ducts in cases where the gallblad-der is overdistended. In these cases, too, the overdistentionof the gallbladder is an indicator of the increased pressure ofthe bile ducts with a patent cystic duct, the latter being asinequa nonfor effective transcholecystic drainage.

Conclusions

We think that in the presence of suspected or ultrasono-graphically confirmed ABP, treatment must be given asearly as possible and must be aimed at achieving two pri-mary objectives:

1. The restoration of patency of the papilla both in order toreduce the risk of associated cholangitis and in order toprevent and/or reduce the development of pancreatic ne-crosis

2. Treatment of the associated bile duct and gallbladderpathology to prevent the risk of relapse of ABP

In light of this, in our opinion, the execution of a com-bined ERCP plus ES as early as possible, followed duringthe same hospital stay by a laparoscopic cholecystectomy,once the acute attack has been resolved, could modify theoutcome of patients suffering from ABP. This approachshould be further evaluated in prospective trials comparingother alternative treatments.

References

1. Bedford RA, Howerton DH, Geenen JE (1994) The current role ofERCP in the management of benign pancreatic disease. Endoscopy 26:113–119

2. Blamey SL, Osborne H, Gilmour WH, O’Neill J, Carter DC (1983)The early identification of patients with gallstone associated pancre-atitis using clinical and biochemical factors only. Ann Surg 158: 574–578

3. Borzellino G, Ricci F, Veraldi D, Cordiano C (1995) Role of endo-laparoscopic surgery in acute biliary pancreatitis. In: Lezoche E, Pa-ganini AM, Bergi G (eds) Thoraco-laparoscopic and minimally inva-sive surgery. Milano, Italy, pp 145–148

4. Bradley EL III (1993) A clinically based classification system foracute pancreatitis. Arch Surg 128: 586–590

5. Canal DF, Broadie TA (1994) Results of laparocholecystectomy forthe treatment of gallstone pancreatitis. Am Surg 60: 495–499

6. Carr-Locke DL (1990) Acute gallstone pancreatitis and endoscopictherapy. Endoscopy 22: 180–183

7. Carr-Locke DL (1992) Role of endoscopy in gallstone pancreatitis.Am J Surg 165: 519–521

8. Cooperman AM, Siegel J, Neff R, Reddy S, Hammerman H (1991)Gallstone pancreatitis: combined endoscopic and laparoscopic ap-proaches. J Laparoendosc Surg 1: 115–117

9. Corfield AP, Cooper MJ, Williamson RCN, Mayer AD, McMahonMJ, Dickson AP, Shearer MG, Imrie CW (1985) Prediction of severityin acute pancreatitis: prospective comparison of three prognostic in-dices. Lancet 24: 403–407

10. De Iorio AV, Vitale GC, Reynolds M, Larson GM (1995) Acute bil-iary pancreatitis. Surg Endosc 9: 392–396

11. de Manzoni G, Furlan F, Guglielmi A, Brunelli G, Laterza E, Ricci F,Genna M, Borzellino G, Cordiano C (1992) Acute cholecystitis: ul-trasonographic staging and percutaneous cholecystostomy. Eur J Ra-diol 15: 175–179

12. Demmy TL, Burch JM, Feliciano DV, Mattox KL, Jordan GL (1988)Comparison of multiple-parameter prognostic systems in acute pan-creatitis. Am J Surg 156: 492–496

13. Fan ST, Lai ECS, Mok FPT, Lo CM, Zheng SS, Wong J (1993) Earlytreatment of acute biliary pancreatitis by endoscopic papillotomy. NEngl J Med 328: 228–232

14. Graham LD, Burrus RG, Burns RP, Chandler KE, Barker DE (1994)Laparoscopic cholecystetomy in biliary pancreatitis. Am Surg 60: 40–43

15. Mann DV, Hershman MJ, Hittinger R, Glazer G (1994) Multicentreaudit of death from acute pancreatitis. Br J Surg 81: 890–893

16. Neoptolemos JP, Carr-Locke DL, London NJ, Bailey IA, James D,Fossard DP (1988) Controlled trial of urgent endoscopic retrogradecholangiopancreatography and endoscopic sphincterotomy versus con-servative treatment for acute pancreatitis due to gallstones. Lancet 29:979–983

17. Neoptolemos JP, Davidson BR, Winder AF, Vallance D (1988) Roleof duodenal bile crystal analysis in the investigation of ‘‘idiopathic’’pancreatitis. Br J Surg 75: 450–453

18. Neoptolemos JP, Stonelake P, Radley S (1993) Endoscopic sphincter-otomy for acute pancreatitis. Hepatogastroenterology 40: 550–555

19. Pellegrini CA (1993) Surgery for gallstone pancreatitis. Am J Surg165: 515–518

20. Ranson JHC (1982) Etiological and prognostic factors in human acutepancreatitis: a review. Am J Gastroenterol 77: 633–638

21. Rhodes M, Armstrong CP, longstaff A, Cawthorn S (1993) Laparo-scopic cholecystectomy with endoscopic retrograde cholangiopancrea-tography for acute gallstone pancreatitis. Br J Surg 80: 247

22. Ros E, Navarro S, Bru C, Garcia-Puge´s A, Valderrama R (1991)Occult microlithiasis in idiopathic acute pancreatitis: prevention ofrelapses by cholecystectomy or ursodeoxycholic acid therapy. Gastro-enterology 101: 1701–1709

23. Scuro LA, Cavallini G (1990) La patologia infiammatoria del pan-creas. Luigi Pozzi (ed) Roma, Italy

24. Soper NJ, Brunt LM, Callery MP, Edmundowicz SA, Aliperti G(1994) Role of laparoscopic cholecystectomy in the management ofacute gallstone pancreatitis. Am J Surg 167: 42–51

25. Steinberg W, Tenner S (1994) Acute pancreatitis. N Engl J Med 330:1198–1210

26. Targarona EM, Balague´ C, Viella P, Martinez J, Trias M (1994) Lap-aroscopic cholecystectomy for biliary pancreatitis. Br J Surg 81: 1694–1695

27. Uomo G, Galloro V, Rabitti PG, Marcopido B, Laccetti M, Visconti M(1991) Early endoscopic cholangiopancreatography and sphincteroto-my in acute biliary pancreatitis: report of 50 cases. Ital J Gastroenterol23: 564–566

28. Winslet MC, Imray C, Neoptolemos JP (1991) Biliary acute pancre-atitis. Hepatogastroenterology 38: 120–123

1182

Technique

Laparoscopic infrared imaging

W. W. Roberts,1 T. A. Dinkel,1 P. G. Schulam,1 L. Bonnell,2 L. R. Kavoussi1

1 Department of Urology, Brady Urological Institute, Johns Hopkins Medical Institutions, 4940 Eastern Avenue, Baltimore, MD 21224, USA2 Vipera Systems, Inc., 1464 Holcomb Road, Huntingdon Valley, PA 19006, USA

Received: 23 August 1996/Accepted: 14 October 1996

Abstract. A system was developed to determine the po-tential role of infrared imaging as a tool for localizing ana-tomic structures and assessing tissue viability during lapa-roscopic surgical procedures. A camera system sensitive toemitted energy in the midinfrared range (3–5mm) was in-corporated into a two-channel visible laparoscope. Laparo-scopic cholecystectomy, dissection of the ureter, and assess-ment of bowel perfusion were performed in a porcine modelwith the aid of this infrared imaging system. Inexperiencedlaparoscopists were asked to localize and differentiate struc-tures before dissection using the visible system and thenusing the infrared system. Assessment of bowel perfusionwas also conducted using each system. Infrared imagingproved to be useful in differentiating between blood vesselsand other anatomic structures. Differentiation of the cysticduct and arteries and transperitoneal localization of the ure-ter were successful in all instances using the infrared systemwhen use of the visible system had failed. This system alsopermitted assessment of bowel perfusion during laparoscop-ic occlusion of mesenteric vessels. These initial studiesdemonstrate that infrared imaging may improve the differ-entiation and localization of anatomic structures and allowassessment of physiologic parameters such as perfusion notpreviously attainable with visible laparoscopic techniques.It may thus potentially be a powerful adjunct to laparoscop-ic surgery.

Key words: Thermography — Laparoscopy — Infrared

Laparoscopy has resulted in significantly less postoperativemorbidity when compared with traditional open approachesfor many surgeries. This has led to an increasing demand forlaparoscopic applications; however, lack of tactile feedback,

two-dimensional imaging of the operative field, and hand–eye dissociation have limited its widespread adaptation forcomplex surgical procedures.

Infrared imaging (also referred to as infrared thermog-raphy) is a technology that can potentially provide addi-tional anatomic and physiologic information during lapara-scopic surgery. This study attempted to assess the utility ofinfrared thermography in a porcine model during laparo-scopic surgery.

Materials and methods

System design

The infrared system consisted of a laparoscope measuring 15 mm in di-ameter and 30 cm in length. Within the laparoscope parallel visible andinfrared channels transmitted images to visible and infrared electronic cam-eras, respectively. The cameras processed this information and relayed thedata to a video mixer and then to a display monitor (Fig. 1). The infraredcomponent of the system detected emitted energy in the midinfrared range,between 3 and 5mm, and was sensitive to gradations in temperature assmall as one-tenth of one degree Centigrade. Warm areas appeared whiteand cooler areas appeared black when the image was displayed. Thissystem was capable of displaying visible, infrared, blended, and compositeimages.

Animal studies

A porcine model was used for laparoscopic experimentation of the infraredimaging system. Three pigs were used for this study. After an adequatedepth of anesthesia was achieved, a pneumoperitoneum was obtained instandard fashion and five working trocars were placed. A 15-mm trocarwas placed supraumbilically and two 10-mm trocars were placed in themidclavicular line, one just subcostal and the other at the level of theanterior superior iliac spine. One trocar was placed in the posterior axillaryline at the level of the umbilicus. After placement of all trocars, laparo-scopic cholecystectomy, dissection of the ureter, and isolation of a segmentof bowel were performed. Three inexperienced laparoscopists (junior resi-dents) attempted to identify anatomic structures (cystic duct, cystic artery,and ureter) prior to dissection by visible inspection and then using theinfrared camera. Additionally, bowel ischemia was assessed by three ex-perienced laparoscopists. Mesenteric vessels were clipped and the bowelwas imaged with both the visible and infrared systems. Room temperaturesaline, applied to the operative field via an irrigator/aspirator, was used asa contrast-enhancing agent.Correspondence to:L. R. Kavoussi

SurgicalEndoscopy

© Springer-Verlag New York Inc. 1997Surg Endosc (1997) 11: 1221–1223

Results

In all three pigs, inexperienced laparoscopists could inde-pendently identify the ureter, cystic duct (Fig. 2), and cysticartery (Fig. 3) using the infrared imaging system, prior todissection, when these structures were not visibly apparent.Moreover, infrared imaging allowed assessment of tissueviability based upon degree of perfusion (Figs. 4, 5). Thisphysiologic data was not apparent with a visible imagingsystem during surgery but could readily be discerned by allsurgeons on the infrared images.

Discussion

Thermography is a process of two-dimensionally mappingtemperature differences by detecting the electromagnetic ra-diation emitted from a tissue or fluid that is warmer orcooler than its surroundings. Boltzmann’s law states that theradiation (E) emitted by a body is proportional to the fourthpower of its absolute temperature (T). The two variables arerelated bys, the Stefan-Boltzmann constant.

E 4 sT4

As a result of this physical law, even slight temperaturedifferences between adjacent areas will result in large dif-ferences in emitted radiation. This type of radiation is al-most exclusively within the infrared portion of the electro-magnetic spectrum, having wavelengths between 2 and 15mm. Visible light has shorter wavelengths, between 0.40and 0.75mm.

Special cameras have been designed to record infraredradiation emitted from the body. These cameras detect tem-perature gradients noninvasively and have been applied inwide-ranging areas of medicine as diagnostic devices, sur-gical instruments, and tools for measuring systemic tem-peratures [7].

The most well-publicized application of infrared ther-mography was breast cancer screening in the 1970s [2, 9].Based on the premise that a cancerous focus would have acharacteristic thermographic appearance, thermographs of apatient’s breasts were compared for symmetry. However,this technique failed because thermographic patterns of nor-mal breasts are highly complex and attempts to compare

them resulted in cancer detection rates below 50% in somestudies. However, in patients with known breast cancer,infrared thermography has proven useful in predicting tu-mor growth rates [3].

Other potential applications of this technology includediagnosing rheumatologic conditions [12], diagnosing car-pal tunnel syndrome [11], assessing and monitoring coro-nary artery disease [5], evaluating uterine activity duringlabor [13], assessing herpes labialis infection during flare-ups [1], assessing brain activity [10], and documenting andcharacterizing skin-temperature changes due to manycauses. Specific surgical applications include recovery-enhanced thermography for localization of cutaneous per-forators in skin flaps [4], intraoperative assessment of in-ternal mammary artery patency during coronary bypass pro-cedures [6], and evaluation of cerebrovascular heatclearance during arteriovenous malformation repair [8].

This is the first reported use of infrared thermography inconjunction with laparoscopy. The principles upon whichthe system is based make use of temperature gradients be-tween adjacent structures. Temperature differences withinthe body are slight so techniques are needed to accentuatethese gradients. Recovery-enhanced thermography has beenused in plastic surgery to identify cutaneous perforators. Aregion of skin is cooled by applying ice water and theninfrared images of the area are taken as it rewarms. Thevessels rewarm quickly and are distinguishable against acooler background. We have applied this same technique tolaparoscopic surgery. When room-temperature saline isused as an irrigant on the operative field, the whole field iscooled temporarily. As the field differentially rewarms,those structures, such as blood vessels, which rewarmquickly appear as white lines against a dark background. Inthis way vessels can be identified and differentiated fromother tubular structures and ducts. A second application ofthis same concept involves filling the upper urinary systemwith room-temperature saline. The pelvis and ureter appearblack against a warmer background which appears white.

There are many other potential surgical applications forthis system including localizing a ureteral stone during aureterolithotomy by instilling room-temperature saline intothe ureter to identify the level of obstruction. Assessment ofperfusion is possible with infrared imaging at the time of theprocedure, hours before visible alterations of the tissue areapparent. This may also be used to check the viability of asegment of bowel in patients who have suffered mesentericischemia or to provide a way to assess testicular blood flowduring laparoscopic orchidiopexy. Cancerous or precancer-ous lesions could potentially be identified based upon theirthermographic characteristics resulting from differentialblood flow.

The initial studies with this system are very promising;however, clinical applicability needs to be demonstrated. Indoing so, several design modifications will be implemented.First, the diameter of the laparoscope needs to be decreasedfrom 15 mm to 10 mm. Second, the combined infrared/visible camera dimensions should be downsized to approachthe dimensions of current visible cameras. Finally, a simplesurgeon-controlled switch, which will allow rapid alterna-tion between visible and infrared imaging, needs to be con-structed.

Fig. 1. The 300 × 15 mm laparoscope contains two channels that transmitdata to the visible and infrared cameras. The images are relayed to a videomixer and onto a monitor. This allows display of visible, infrared, com-posite, or blended images.

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The laparoscopic environment creates challenges for thesurgeon because of lack of tactile feedback, two-dimen-sional imaging of the three-dimensional operative field, andhand–eye dissociation. Infrared imaging may help to over-come these challenges by providing additional informationthat previously was not available using visible imaging.This technology may decrease the risks associated with lap-aroscopic procedures as well as decrease costs by shorten-ing operating time and thus has the potential to become avery powerful adjunct to laparoscopy.

Acknowledgment.This work was funded in part by a grant from the Ameri-can Foundation for Urological Disease. We thank Leonard Bonnell, DennisLeiner, and Thomas Brukilacchio of Vipera Systems, Inc., for providingtheir prototype Mid-Infrared Laparoscopic Imaging System.

References

1. Biagioni PA, Lamey P (1995) Electronic infrared thermography as amethod of assessing herpes labialis infection. Acta Derm Venereol(Stockh) 75: 264–268

2. Blume SS (1993) Social process and the assessment of a new imagingtechnique. Int J Technol Assess Health Care 9: 335–345

3. Head JF, Wang F, Elliott RL (1993) Breast thermography is a nonin-vasive prognostic procedure that predicts tumor growth rate in breastcancer patients. Ann N Y Acad Sci 698: 153–158

4. Itoh Y, Arai K (1995) Use of recovery-enhanced thermography tolocalize cutaneous perforators. Ann Plast Surg 34: 507–511

5. Lawson W, BenEliyahu D, Meinken L, Chernilas J, Novotny H, CohnP, Dervan J (1993) Infrared thermography in the detection and man-agement of coronary artery disease. Am J Cardiol 72: 894–896

6. Mohr FW, Falk V, Philippi A, Autschbach R, Krieger H, Diegeler A,Dalichau H (1994) Intraoperative assessment of internal mammaryartery bypass graft patency by thermal coronary angiography. Cardio-vasc Surg 2: 703–710

7. Nobell JJ (1992) Infrared ear thermometry. Pediatr Emerg Care 8:54–58

8. Okudera H, Kobayashi S, Toriyama T (1994) Intraoperative regionaland functional thermography during resection of cerebral arteriove-nous malformation. Neurosurgery 34: 1065–1067

9. Orel SG, Troupin RH (1993) Nonmammographic imaging of thebreast: current issues and future prospects. Semin Roentgenol 28: 231–241

10. Shevelev IA, Tsicalov EN, Gorbach AM, Budko KP, Sharaev GA(1993) Thermoimaging of the brain. J Neurosci Methods 46: 49–57

11. Tchou S, Costich JF, Burgess RC, Wexler CE (1992) Thermographicobservations in unilateral carpal tunnel syndrome: report of 61 cases.J Hand Surg 17A: 631–637

12. Thomas D, Siahamis G, Marion M, Boyle C (1992) Computerisedinfrared thermography and isotopic bone scanning in tennis elbow.Ann Rheum Dis 51: 103–107

13. Yang W, Zhang N, Yang PPT, Lin ZZ (1993) Determination of uterineactivity during labor by means of infrared thermography. J BiomechEng 115: 254–256

Figs. 2, 3. (far left and left,respectively) The gallbladder is inthe upper lefthand corner of thepictures. The cystic duct and cysticvessels are contained within thepedicle (c). Infrared imaging clearlydelineates the cystic duct, whichappearsdark, from the deep andsuperficial cystic arteries (a), whichappear aswhite lineson either sideof the cystic duct.

Figs. 4, 5. (far left and left,respectively) Using infrared imagingand room-temperature saline as acontrast-enhancing agent, asegmental mesenteric artery (a)appears as athin white line.Thebowel (b) perfused by that arteryappearswhite.The segmental arterywas clipped and a few minutes laterthe second infrared picture wastaken. The segmental artery nowappearsdark, as does the bowel,suggesting a compromised bloodflow. A clear line of demarcation isnoted between the compromised andwell-perfused regions of bowel.

1223

Video-laparoscopic staging of gastric cancer

A prospective multicenter comparison with noninvasive techniques

F. Asencio,1 J. Aguilo,2 J. L. Salvador,3 A. Villar, 1 E. De la Morena,4 M. Ahamad,1 J. Escrig,3 J. Puche,4

V. Viciano,2 G. Sanmiguel,1 J. Ruiz1

1 Hospital Arnau de Vilanova, Valencia, Spain2 Hospital de Xa´tiva, Valencia, Spain3 Hospital General, Castello´n, Spain4 Hospital Marina Alta, Denia, Spain

Received: 5 May 1996/Accepted: 10 March 1997

AbstractBackground:The high proportion of gastric carcinomas pre-sent in an unresectable stage, together with the emergenceof multimodal treatments, increases the usefulness of objec-tive staging methods that avoid unnecessary laparotomies.Methods:A prospective evaluation of the accuracy of lap-aroscopy in the staging of 71 patients with gastric adeno-carcinoma is presented. Serosal infiltration, retroperitonealfixation, metastasis to lymph nodes, peritoneal and livermetastasis, and ascites were determined in the stagingworkup. Sensitivity, specificity, and predictive values werecalculated and compared with those obtained with ultraso-nography (US) and computed tomography (CT).Results:The diagnostic accuracy of laparoscopy in the de-termination of resectability was 98.6%. Consequently, over40% of patients were spared unnecessary laparotomies.Laparoscopy yielded diagnostic indices superior to US andCT for all the tumoral attributes studied. Our techniquepermits accurate assessment and pathologic verification ofliver and the peritoneal and retroperitoneal extent of tumorinvasion in the majority of patients.Conclusions:Laparoscopy in gastric adenocarcinoma is areliable technique that provides accurate assessment of re-sectability and stage, thus avoiding unnecessary laparoto-mies in patients in whom surgical palliation is not indicated.A stepwise diagnostic workup combining imaging andminimally invasive techniques is proposed.

Key words: Stomach — Cancer — Staging — Laparoscopy— Resectability

Surgical therapy still represents the treatment of choice forpatients with primary gastric adenocarcinoma, but surgerymay have reached its limits concerning the rate of resect-ability, mortality, and survival.

Most gastric carcinomas are currently diagnosed in ad-vanced tumor stages, 15–50% of patients being unresectable[11–13]. The high morbidity (13–23%) and mortality rates(10–36%) after laparotomy in unresected patients, togetherwith the new palliation techniques for malignant dysphagiain cancer of the proximal stomach, have given a priority toavoiding inappropriate surgery [8, 10, 11].

On the other hand, higher response rates to new antitu-moral combinations referred to in the literature [1, 12, 22]implicitly question the usefulness of objective staging meth-ods that facilitate the preoperative assignment of patients tomultimodal treatments.

Despite the introduction of ultrasonography (US), com-puted tomography (CT), and magnetic resonance, imagingmethods lack sufficient accuracy when dealing with gastriccancer, and the surgeon often faces a wide discrepancy be-tween preoperative and intraoperative staging. Thus, explor-atory laparotomy continues to be the only reliable stagingmethod for gastric cancer currently available.

With the introduction of surgical videocelioscopy, thistechnique is increasingly being appreciated as a valuablestaging technique in a variety of gastrointestinal cancers,and high accuracy in the detection of intraabdominal me-tastases has been reported [7, 9, 10, 20].

Our primary objective is to evaluate the efficiency andsafety of surgical laparoscopy in the staging and determi-nation of resectability of gastric cancer patients deemedresectable by conventional imaging techniques. Addition-

An original article by the Grupo Inter-Hospitalario Valenciano (G.I.H.V).Presented in part at the 19th ESMO Congress, Lisbon, Portugal, 1994Correspondence to:F. Asencio, Plaza Mestre Ripoll 9 dcha. 28a, 46022—Valencia, Spain

Surg Endosc (1997) 11: 1153–1158

SurgicalEndoscopy

© Springer-Verlag New York Inc. 1997

ally, the staging ability of laparoscopy is compared withthese diagnostic methods.

Patients and methods

Patients

Between July 1992 and March 1995, all patients with biopsy-proven gastricadenocarcinoma admitted to four public hospitals in the Valencian Com-munity were eligible for the study. Obviously unresectable lesions andpatients who presented bleeding or gastric outlet obstruction requiringbypass procedures were excluded. All patients gave their informed consentbefore final inclusion in the study.

Seventy-six patients with presumably resectable lesions after the per-formance of conventional imaging were prospectively included. Ultraso-nography was performed in all patients and dynamic contrast-enhanced CTwas additionally performed in 37. The restricted use of CT dependedexclusively upon availability in different centers.

Laparoscopy was performed in these 76 patients. Five patients wereexcluded from further study since they were finally not operated on at ourinstitutions and/or entered neoajuvant chemotherapy programs that couldinfluence postoperative tumor staging. Thus, 71 patients (43 men and 27women) remained evaluable throughout the study.

Laparoscopic technique

Laparoscopy was performed with general anesthesia, either as an indepen-dent procedure or before laparotomy. A maximum of three ports was used(umbilical, right and left of the midline). The visible surfaces of the stom-ach, liver, diaphragm, omentum, and peritoneal surfaces were systemati-cally explored in search of malignant deposits and ascites. A second portpermitted the introduction of a palpation probe. The combined inspectionand probing provided an estimate of the tumoral extension within thestomach. Enlarged lymph nodes were also explored. By elevating the liver,the undersurface and the hepatoduodenal ligament were inspected. Thesemaneuvers were aided by elevating the head of the operating table. Accessto the lesser sac was obtained after dissecting a small opening at the greateromentum near the greater curvature, as described elsewhere [3]. The pos-terior wall of the stomach and the relationship of the tumor to retroperi-toneal structures (i.e., pancreas) were assessed, thus determining its resect-ability. Finally, the pelvic cavity was examined by elevating the foot endof the table.

The following attributes were determined in the staging workup: ana-tomical localization of the tumor, serosal infiltration, tumor fixation, me-tastasis to lymph nodes, peritoneal and liver metastasis, and ascites.

To reduce operative risks and time, laparoscopic obtention of serosaland nodal biopsies and inspection of retrogastric area were consideredessential only if relevant for the fulfillment of the primary objective (globalstage and resectability). Otherwise it was left to the surgeon’s consider-ation.

Upon laparoscopic evaluation, patients were considered eligible forsurgery when conditions for tumor resection were present.

Analysis

TNM staging was accomplished after the UICC classification (1987). Tosimplify laparoscopic evaluation, stage I and II have been unified in asingle I/II stage since its preoperative discrimination has currently no in-fluence in decision-making.

For an objective interpretation, the tumoral attributes evaluated wereconsidered as true positives only after being confirmed by histopathologicexamination (laparoscopic/laparotomic biopsy or surgical specimen).Negative findings were only considered as true negatives if the absence oftumoral invasion was confirmed at laparotomy or in the resected specimen.With the intention of doing evaluation, equivocal, failed, or otherwise-unfulfilled requirements were considered as negatives for statistical analy-sis.

Diagnostic indices (i.e., sensitivity, specificity, and predictive values ofpositive and negative tests) and their 95% confidence intervals were cal-

culated for the three diagnostic procedures evaluated (US, CT, and lapa-roscopy) in two-way contingency tables of frequencies of positive andnegative results constructed as either true or false upon surgical and his-tologic evaluation.

To determine the diagnostic capability of laparoscopy in the investi-gation of tumors located in the proximal stomach and particularly in itsposterior surface, true and false diagnosis of serosal and retroperitonealinvasion have been compared between upper third and ‘‘not upper third’’lesions by means of the chi square test with Yates’ continuity correction.

Results

Patients ranged in age from 47 to 81 years (mean: 65.8).Tumors were located in the lower third of the stomach in 19patients (27%), in the middle third in 21 (30%), in the upperthird in 12 (17%), in two-thirds in 16 (22%), and in thewhole stomach in three (4%).

The distribution of tumors by final stage (UICC-1987)was as follows: stage Ia: three (4.2%); stage Ib: two (2.8%);stage II: nine (12.7%); stage IIIa: 12 (16.9%); stage IIIb: 10(14.1%); stage IV: 35 (49.3%).

The complications of laparoscopy were minimal andmost patients were discharged after 1 or 2 days if the pro-cedure was performed independently.

After laparoscopic staging, laparotomy was discarded in29 (40.8%) cases due to advanced disease not previouslyproven by the other preoperative tests. The main reasonswere peritoneal metastasis in 16 patients, malignant ascitesin 15, liver metastases in 12, Krukenberg tumor in two, andretroperitoneal fixation in eight. Most unresectable patientswere affected by the coexistence of more than one of thesefindings. The other 42 patients were deemed resectable. Inone of these patients resection was finally not feasible dueto retroperitoneal fixation of the tumor. Thus, the resect-ability rate, that is, the proportion of patients effectivelyundergoing either radical or palliative gastrectomy, was57.7% (41 out of 71); 83% of these patients underwentcurative surgery (UICC Ro) while 17% had palliative op-erations. The diagnostic accuracy of laparoscopy in deter-mination of resectability was 98.6% (70 out of 71 cases).

Table 1 presents the correspondence of laparoscopicstage with final stage. The overall proportion of correctlydiagnosed stages was 80% (57 accurate, 14 down-staging,and 0 up-staging). Laparoscopic diagnosis of a stage I/IItumor presented a positive predictive value (PPV) of 53.8%.When laparoscopy determined a stage III tumor, PPV in-creased to 85.7%. The laparoscopic diagnosis of a stage IVtumor was 100% accurate (PPV4 100).

Table 2 presents the diagnostic indices of laparoscopy,with their confidence intervals, in relation to the major at-tributes used in the staging workup of gastric cancer. Lap-aroscopy yielded a statistically significant relationship withtrue diagnosis for all these attributes studied independently(p < 0.05).

Laparoscopic biopsy correctly identified 40 of 52 se-rosa-positive cases, with 12 false negatives (FN) and nofalse positives (FP), offering a sensitivity of 76.9% and aspecificity of 100%, a positive predictive value (PPV) of100%, and a negative predictive value (NPV) of 47.8%.

Laparoscopic nodal biopsy correctly identified 30 of 48node-positive cases, with 18 FN and no FP, offering a sen-sitivity of 62.5% and a specificity of 100%, a PPV of 100%,and an NPV of 33.3%.

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Liver metastases were accurately detected in all 14 pa-tients with confirmed hepatic metastases, with no FNs andno FPs, offering a sensitivity and a specificity of 100% anda PPV and an NPV of 100%.

Peritoneal implants were correctly identified and biop-sied by the laparoscope in 16 of the 18 patients with dem-onstrated peritoneal metastases, with two FNs and no FPs,offering a sensitivity of 88.9% and a specificity of 100%, aPPV of 100%, and an NPV of 95.5%.

The presence of ascitic fluid was correctly identified inall 15 patients with confirmed ascites, with no FN and noFP, offering results of 100% in all diagnostic indices. Cy-tological analysis detected malignant cells in 13 cases andwas negative in two.

Laparoscopic evaluation of the lesser sac correctly iden-tified eight of 14 cases with proven retroperitoneal exten-sion of the tumor, with six FNs and no FP, offering a sen-sitivity of 57.1% and a specificity of 100%, a PPV of 100%,and an NPV of 87% in determining retroperitoneal invasion.

Table 3 presents the diagnostic indices of computed to-mography. CT only demonstrated a statistically significantrelationship with true diagnosis in the assessment of asciticfluid (p < 0.05), while the accuracy for hepatic metastasisdid not reach this significance.

The results of ultrasonographic staging only demon-strated a statistically significant association (p < 0.05) withtrue diagnosis in the detection of liver metastases, present-ing a sensitivity of 38.5% and a specificity of 100%, a PPVof 100%, and an NPV of 84.3%.

With the association of both scanning techniques (US +CT), the diagnostic yield for all the attributes studied wasnot statistically improved.

Tables 4–6 compare the diagnostic indices obtainedwith the three different tests for the detection of lymphnode, liver, and peritoneal metastases.

No statistical differences could be found in the laparo-scopic detection of serosal and retroperitoneal invasion inrelation to tumor location (upper third vs ‘‘not upperthird’’).

Discussion

Laparoscopy has been evaluated in the management of pa-tients with gastric cancer with somewhat conflicting results.This procedure has been limited, for the most part, to evalu-ation of visible hepatic or peritoneal metastasis [10, 13]. Ithas thus been suggested that laparoscopy cannot permit anaccurate evaluation of anatomical tumor extension. A pau-city of reports (except for Russian authors) describing theutilization of laparoscopy for preoperative evaluation ofgastric carcinoma supports this belief [4, 7, 10, 13, 17].Currently, technological developments in laparoscopy fa-cilitate surgical manipulations in the abdomen that couldincrease its diagnostic capabilities in gastric malignancies.Some recent reports seem to confirm this point [2, 15, 18].

As determined solely on the basis of laparoscopic evalu-ation, resectability success rate was 98.6%, an appreciableimprovement when compared with the rate of 57.7% usingstandard staging methods (US, CT), and thus, 40.85% ofpatients with presumably operable gastric cancer werespared unnecessary laparotomies. Similar results are ob-tained by other authors [10, 13, 17].

In our experience, using the technique described in this

Table 1. Correspondence of laparoscopic stage with final stage: positive predictive values (PPV) with 95% confidence intervals

Laparoscopic stage

TotalI + II III IV

Correct 14 (53.8%) 12 (85.7%) 31 (100%) 57 (80%)Down-staging 12 (46.2%) 2 (14.3%) 0 14 (20%)PPV 53.8 85.7 10095% C.I. 33.4–73.4 57.2–98.2 99.8–100

Total 26 (100%) 14 (100%) 31 (100%) 71 (100%)

Table 2. Diagnostic indices and 95% confidence intervals for attributes of gastric cancer as assessed by laparoscopy and confirmed by histology orlaparotomy

Attribute Patients Positives Sensitivity Specificity

Predictive value

Positive Negative

Serosa 63 52 76.9 100 100 47.8Infiltration* 63.1–87.5 71.5–100 91.1–100 26.8–69.4Lymph node 57 48 62.5 100 100 33.3Metastasis* 47.3–76.1 66.4–100 88.4–100 16.5–54.0Liver 56 14 100 100 100 100Metastasis* 76.8–100 91.6–100 76.9–100 91.6–100Peritoneal 60 18 88.9 100 100 95.5Metastasis* 65.3–98.6 91.6–100 79.4–100 84.5–99.4Retroperitoneal 54 14 57.1 100 100 87.0Infiltration* 28.9–82.3 91.2–100 63.1–100 73.7–95.1Ascites* 66 15 100 100 100 100

78.2–100 93.0–100 78.2–100 93.0–100

* p < 0.05

1155

report, an accurate assessment of TNM stage can be ob-tained by laparoscopy. Nevertheless, laparoscopic diagnosisof a stage I/II tumor has little more than a 50–50 chance ofbeing correct (like flipping a coin, for instance). This diag-nostic capability increases when a stage III tumor is de-tected (57–98%) and yields absolute accuracy when lapa-roscopy identifies a stage IV tumor. The imperative of his-tologic confirmation for stage determination eliminates theincidence of errors due to up-staging.

The technique performs best for the determination ofliver and peritoneal metastases as well as for the detectionof small amounts of ascitic fluid that can be collected forcytological examination. This accuracy decreases in the as-sessment of serosal affection and nodal infiltration. Never-theless, the visually guided biopsy of these targets rendersabsolute specificity, thus permitting accurate decision mak-

ing in biopsy-positive cases. Similar experiences have beenreported recently [19, 21]. The limitations of the techniqueare currently due to the presence of adhesions in the supra-mesocolic area (i.e., carcinoma of the gastric stump). Threepatients could not be properly evaluated by laparoscopy dueto internal adhesions of previous abdominal operations, in-cluding the single error in laparoscopic determination ofresectability.

When imaging techniques are revised in the literature [5,11, 13, 17, 21], the high accuracy for liver metastases fallsin the presence of small superficial lesions. This was thecase in our study, since all patients presented presumablyresectable lesions after conventional preoperative staging.Ozarda [16] has shown that 11% of patients with hepaticmetastases fail to present them on the surface of the organ.These lesions will probably pass unseen by laparoscopy, as

Table 3.Diagnostic indices and 95% confidence intervals for attributes of gastric cancer as assessed by computed tomography and confirmed by histologyor laparotomy

Attribute Patients Positives Sensitivity Specificity

Predictive value

Positive Negative

Serosa 34 29 69.0 60.0 90.9 25.0Infiltration 49.1–84.7 14.7–97.7 70.8–98.9 5.5–57.2Lymph node 33 27 66.7 66.7 90.0 30.8Metastasis 46.0–83.5 22.3–95.7 68.3–98.8 9.1–61.4Liver 30 7 28.6 100 100 82.1Metastasis 3.7–71.0 85.2–100 15.8–100 63.1–93.9Peritoneal 32 10 0.0 – – –MetastasisRetroperitoneal 32 10 30.0 90.9 60.0 74.1Infiltration 6.7–65.2 70.8–98.9 14.7–94.7 53.7–88.8Ascites* 33 10 30.0 100 100 76.7

6.7–65.2 85.2–100 29.2–100 57.7–90.1

* p < 0.05

Table 4. Diagnostic indices and 95% confidence intervals of the three tests for the detection of lymph nodes

Test Patients Positives Sensitivity Specificity

Predictive value

Positive Negative

Laparoscopy 57 48 62.5 100 100 33.3(*) 47.3–76.1 66.4–100 88.4–100 16.5–54.0US 57 48 15.2 88.9 87.2 17.0

6.3–28.9 51.7–99.7 47.4–99.7 7.6–30.8CT 33 27 66.7 66.7 90.0 30.8

46.0–83.5 22.3–95.7 68.3–98.8 9.1–61.4

* p < 0.05

Table 5. Diagnostic indices and 95% confidence intervals of the three tests for the detection of liver metastasis

Test Patients Positives Sensitivity Specificity

Predictive value

Positive Negative

Laparoscopy 56 14 100 100 100 100(*) 76.8–100 91.6–100 76.9–100 91.6–100US* 56 14 38.5 100 100 84.3

13.9–68.4 91.8–100 47.8–100 71.4–93.0CT 30 7 28.6 100 100 82.1

3.7–71.0 85.2–100 15.8–100 63.1–93.9

* p < 0.05

1156

well as by exploratory laparotomy, without the aid of intra-operative (or laparoscopic) ultrasonography [2]. Peritonealmetastases are almost undetectable by imaging techniques;and their presence usually precludes gastric resection. In ourexperience, both types of lesions were almost systematicallydetected by laparoscopy.

The degree of posterior fixity of the tumors is describedas difficult to assess by laparoscopic examination, mostfalse-negative results being due to the posterior extension ofthe tumor [10, 13]. With the use of surgical laparoscopy, thetechnique described permits accurate assessment of the ret-roperitoneal extent of tumor invasion.

Laparoscopy could also be an appropriate method bywhich to determine tumoral response to chemotherapy; con-ventional staging methods are currently inaccurate. Effec-tiveness of different therapeutic regimens could be moreaccurately compared, and current discrepancies could bethus obviated.

The theoretical risk for tumor spreading after diagnosticlaparoscopy reported in the literature [6] was accepted be-cause all patients with positive biopsies underwent postop-erative or neoadjuvant (excluded from analysis) chemo-therapy treatments.

Considering the invasive condition of laparoscopy, al-though clearly underutilized for gastric cancer staging, thisprocedure might not be practical for this purpose in allcases. Endoscopic ultrasound (EUS) is now regarded asmost accurate in the preoperative determination of the de-gree of gastric wall infiltration [15, 18] and could play an im-portant role in patient preselection for staging laparoscopy.

A stepwise diagnostic workup combining imaging andminimally invasive techniques could be a reasonable ap-proach for gastric cancer in the future, as recommended bySendler [18]. After diagnosis by endoscopy and biopsy, im-aging techniques (US/CT) and guided needle biopsieswould represent the first line in staging. For patients withoutobviously advanced disease, further selection could be fa-cilitated by EUS. Tumors regarded as T1–T2 by EUS wouldundergo straight forward laparotomy. Considering that T3tumors have 88% positive lymph nodes [14] and that theperitoneal cavity is an important failure site for patients whohave either T3 or T4 lesions, this subgroup would be se-lected for staging laparoscopy.

Conclusions

Laparoscopic staging of gastric adenocarcinoma is a reliabletechnique that provides accurate assessment of resectability,

thus obviating unnecessary laparotomies in patients inwhom surgical palliation is not indicated. If evidence ofinoperability is equivocal, accurate diagnosis of metastaticinvolvement requires histologic confirmation before a pa-tient is denied potentially curative surgical treatment. In ourexperience, laparoscopic guided biopsies permit this confir-mation in most patients.

In addition, TNM staging could facilitate the assignmentof patients to preoperative (neoadjuvant) treatment sched-ules in controlled studies or the assessment of tumoral re-sponse to multimodal antitumoral therapies.

When compared with computerized tomography and ul-trasound, laparoscopic diagnosis was superior in assessingall tumoral attributes tested in the study.

The most convenient timing for staging laparoscopy(preoperative vs independent procedures) as well as the po-tential hazards of the method, such as free tumor cell im-plantation into the abdominal wall, should be determinedwith further experience.

Acknowledgments.Thanks are due to S. Pero, M.D., from the ValencianInstitute for Studies in Public Health (IVESP), for his revision of themanuscript and for his scientific counseling.

References

1. Ajani J, Mansfeld P, Ota D (1995) Potentially resectable gastric car-cinoma: current approaches to staging and preoperative therapy. WorldJ Surg 19: 216–220

2. Anderson D, Campbell S, Park K (1996) Accuracy of laparoscopicultrasonography in the staging of upper gastrointestinal malignancy.Br J Surg 83: 1424–1428

3. Asencio Arana F (1994) Laparoscopic access to the lesser sac in gas-tric cancer staging. Surg Laparosc Endosc 4: 438–440

4. Boliukh B, Alekseev V (1992) Exploratory laparoscopy in stomachcancer. Klin Khir 9–10: 54–55

5. Colin-Jones D, Rosch T, Dittler H (1993) Staging of gastric cancer byendoscopy. Endoscopy 25: 34–38

6. Cook T, Dehn T (1996) Port-site metastases in patients undergoinglaparoscopy for gastrointestinal malignancy. Br J Surg 83: 1419–1420

7. Cuesta MA, Meijer S, Borgstein P (1992) Laparoscopy and assessmentof digestive tract cancer. Br J Surg 79: 486–487

8. Geoghegan JG, Keane TE, Rosenberg IL, Dellipiani AW, Peel AL(1993) Gastric cancer: the case for a more selective policy in surgicalmanagement. J R Coll Surg Edinb 38: 208–212

9. Greene F (1992) Laparoscopy in malignant disease. Surg Clin NorthAm 72: 1125–1137

10. Gross E, Bancewicz J, Ingram G (1984) Assessment of gastric cancerby laparoscopy. Br Med J 288: 1577

11. Hallisey M, Allum W, Roginski C, Fielding J (1988) Palliative surgeryfor gastric cancer. Cancer 62: 440–444

12. Kiyabu M, Leichman L, Chandrasoma P (1992) Effects of preopera-tive chemotherapy on gastric carcinoma. Cancer 70: 2239–2245

Table 6. Diagnostic indices and 95% confidence intervals of the three tests for the detection of peritoneal metastasis

Test No. patients No. positives Sensitivity Specificity

Predictive value

Positive Negative

Laparoscopy 60 18 88.9 100 100 95.5(*) 65.3–98.6 91.6–100 79.4–100 84.5–99.4US 60 18 6.3 100 100 73.7

0.2–30.2 91.6–100 – 60.3–84.5CT 32 10 0.0 – – –

* p < 0.05

1157

13. Kriplani AK, Kaput BM (1991) Laparoscopy for pre-operative stagingand assessment of operability in gastric carcinoma. Gastrointest En-dosc 37: 441–443

14. Maruyama K, Gunven P, Okabayashi K, Sasako M, Kinoshito T(1989) Lymph node metastases in gastric cancer. Ann Surg 210: 596

15. O’Brien M, Fitzgerald E, Lee G, Crowley M, Shanahan F, O’SullivanG (1995) A prospective comparison of laparoscopy and imaging in thestaging of esophagogastric cancer before surgery. Am J Gastroenterol90: 2191–2194

16. Ozarda A, Pickren J (1962) The topographic distribution of liver me-tastases: its relation to surgical and isotope diagnosis. J Nucl Med 3:149–152

17. Possik R, Franco E, Pires D, Wohnrath D, Ferreira E (1986) Sensi-tivity, specificity, and predictive value of laparoscopy for the stagingof gastric cancer and for the detection of liver metastases. Cancer 58:1–6

18. Sendler A, Dittler H, Feussner H, Nekarda H, Bollschweiler E, Fink U,

et al. (1995) Preoperative staging of gastric cancer as precondition formultimodal treatment. World J Surg 19: 501–508

19. Tognarelli B, Blanc P, Peray P, Galindo G, David XR, Rouillon JM(1993) The value of laparoscopy in the staging of digestive systemcancers. Ann Gastroenterol Hepatol (Paris) 29: 229–232

20. Warshaw A, Gu Z, Wittenberg J, Waltmann A (1990) Preoperativestaging and assessment of resectability of pancreatic cancer. Arch Surg125: 230–233

21. Watt I, Stewart I, Anderson D, Bell G, Anderson J (1989) Laparos-copy, ultrasound and computed tomography in cancer of the oesopha-gus and gastric cardia: a prospective comparison for detecting intra-abdominal metastases. Br J Surg 76: 1036–1039

22. Wilke H, Preusser P, Fink U (1990) New developments in the treat-ment of gastric carcinoma. Semin Oncol 17 (Suppl 2): 61–70

23. Zakharov S, Kutepov V, Kalachev V (1988) Possibilities of laparos-copy in the diagnosis of disseminated cancer of the stomach. Klin Khir5: 37–38

1158

Tailored augmentation of the lower esophageal sphincter inexperimental antireflux operations

S. M. Freys, K. H. Fuchs, J. Heimbucher, A. Thiede

Department of Surgery, University of Wu¨rzburg, Josef-Schneider-Str. 2, D-97080 Wu¨rzburg, Germany

Received: 29 January 1997/Accepted: 2 April 1997

AbstractBackground:Modern upper GI function studies allow forthe detection of several pathophysiological factors that con-tribute to gastroesophageal reflux disease. The informationobtained can lead to therapeutic consequences in patientswith an indication for a surgical intervention, i.e., an indi-vidualized choice of antireflux procedure according to theexisting pathophysiologic defect.Methods: In an experimental study on mini-pigs the me-chanical effect of four standardized antireflux operations(anterior and posterior 180° hemifundoplication, Nissen-DeMeester and Nissen-Rossetti 360° fundoplication) on thelower esophageal sphincter (LES) was investigated. It wasthe aim of the study to objectively determine the extent ofchanges in pressure and length parameters at the LES ac-cording to the performed antireflux procedure.Results:It could be demonstrated that different degrees offundic wrap formation lead to a proportional mechanicaleffect at the LES according to the size of this wrap.Conclusion:Choosing a distinct type of fundoplication willallow for a tailored augmentation of the LES according tothe individual functional defect.

Key words: Gastroesophageal reflux disease — Surgicaltherapy — Antireflux operations — Lower esophagealsphincter — Experimental study

Gastroesophageal reflux disease (GERD) is a multifactorialprocess [5, 15]. The most important functional defect thatseems to be involved concerns the high-pressure zone in thedistal esophagus. This high-pressure zone functions as areflux barrier which is in many publications nominated thelower esophageal sphincter (LES) [7, 31, 39]. The recentimprovement and understanding in the pathophysiology of

the disease [15, 29] as well as the establishment of laparo-scopic techniques in GERD has made surgical therapy moreattractive for patients [4, 5]. Surgical therapy focuses on themechanical augmentation of the high-pressure zone in thedistal esophagus. Even though a great variety of antirefluxprocedures have been developed over the past 20–30 yearsit seems obvious that wrapping the fundus of the stomach ina total or a partial circumference around the high-pressurezone of the distal esophagus leads to an improvement of thereflux barrier function at the esophagogastric junction. Thisimprovement can be observed with a full fundic wrap suchas a Nissen fundoplication, with a partial fundic wrap suchas the Belsey Mark IV procedure, with the positioning of anAngelchick antireflux procedure, and with a posterior gas-tropexy such as the Hill repair. The assessment of the func-tional changes comparing the postoperative manometric re-sults is difficult since these operations are usually per-formed in different institutions on different patientpopulations by many surgeons. Some comparative studies,even randomized trials, have shown that there seems to beno difference in the mechanical effect on the antireflux bar-rier between full and partial wraps [23]; others have showna stronger mechanical augmentation with a full fundoplica-tion [8]. At present there is an ongoing controversial dis-cussion over whether to tailor shape the mechanical aug-mentation of a defective LES by using, in some patients, a360° fundoplication and in other patients a partial wrap [14,20, 22]. The extent of the augmentation is not only impor-tant for the antireflux effect, since it may also cause sideeffects for the patients, especially postoperative bloatingand persistent dysphagia [1]. The purpose of this study wasto assess the mechanical action of different antireflux pro-cedures in order to evaluate whether different principles ofoperative augmentation at the esophagogastric junction canlead to a modulation of the exerted mechanical effect in astandardized fashion. The answer to this question could bethe basis for a discussion of whether it is useful to create atailor-shaped augmentation of the LES according to the in-dividual functional defect.Correspondence to:S. M. Freys

Surg Endosc (1997) 11: 1183–1188

SurgicalEndoscopy

© Springer-Verlag New York Inc. 1997

Materials and methods

Study protocol

Four antireflux procedures were performed on 28 mini-pigs (four groups ofseven animals each). Immediately pre- and postoperatively and 2 monthspostoperatively an esophagogastroduodenoscopy and an esophageal ma-nometry were performed. Surgery and investigations were performed in theExperimental Laboratory at the Department of Surgery of Wu¨rzburg Uni-versity. The study protocol was approved and a written consent was givenby the Committee on Animal Research of the Government of Unterfranken,Wurzburg, according to the German Law on the Protection of Animals.

Selection and preparation of animals

Healthy mini-pigs with a body weight of 23–62 kg were used. All animalsunderwent a veterinary examination prior to the study. The diet consistedof dry food and water. Three days prior to the investigations and operationsthe animals were fed with Fresubin (Fresenius, Inc.) and water, and finallyon the last day only water was allowed. This standardized regimen allowedfor an empty upper GI tract during the endoscopic investigations prior tomanometry and operation. Immediately before the investigations the ani-mals were sedated using a 600-mg i.m. injection of azaperon. All investi-gations and operations were performed under general anesthesia with in-tubation and ventilation (thiopental-natrium: 5 mg per kg bodyweight,N2O: 2.5 l per minute, O2: 0.65 l per minute). The animals were positionedand fixed in a supine position on an operation table.

Endoscopy

An endoscopic inspection of the upper GI tract was performed prior to anyinvestigation and operation. A PQ 20 gastroscope (Olympus Inc.) wasused. On the one hand, this investigation was performed to rule out anyexisting pathology, to check whether the upper GI tract was emptied, andpostoperatively, to visually control the operative result. On the other hand,the endoscopy was used to position a guide wire in the stomach which thenserved as a path finder for the manometry probe used for esophagealmanometry.

Esophageal manometry

All pre- and postoperative esophageal manometries were performed with aperfusion system according to a standardized protocol using the DeMeestercriteria for characterization of the LES [13, 39]. Motility studies wereperformed using a water-perfused, low-compliance manometry systemwith a 170-cm five-channel catheter and an eight-channel catheter. Thedistance between channel openings was 5 cm in the five-channel catheter;in the eight-channel catheter the openings were on the same level. Theperfusion was performed with distilled water at a rate of 0.5 ml per minuteand channel. All investigations were recorded on a computerized system(Polygraf HR, Synectics, Inc., Frankfurt, Germany) and the analysis wasperformed with a commercially available software system (Polygram, Gas-trosoft, Inc., Irvine, Texas, USA). During each motility study a station-to-station pull-through was performed with the five-channel catheter at a paceof 1 cm per 30 s. With this investigation the total length, the intraabdominallength, and the resting pressure of the LES were measured. The second partof each motility study consisted of a rapid motorized pull-through using theeight-channel catheter at a pace of 0.5 cm per second. This investigationallowed for the computerized calculation of the sphincter pressure vectorvolume using the above-mentioned software [30].

Antireflux procedures

All antireflux operations were performed laparoscopically. Four types ofoperations were performed on seven animals each: (1) anterior 180° hemi-fundoplication [14], (2) posterior 180° hemifundoplication according toToupet [35], (3) 360° fundoplication according to Nissen-DeMeester [6],and (4) 360° fundoplication according to Nissen-Rossetti [27].

The laparoscopic access was equal in all operations using five trocarsin the midabdomen: After establishment of the pneumoperitoneum using aVeress needle, a 10-mm optic was inserted via a left paraumbilical trocar.Four further 10-mm trocars were subsequently inserted into the abdomenunder direct vision. The liver retractor was inserted through the right lateraltrocar. The gastric fundus was then pulled laterocaudally using a graspingforceps through the left lateral trocar. The two other paramedian trocarswere used for active operating instruments. Following a visual inspectionthe peritoneum and phrenicoesophageal membrane were incised and theLES was dissected from left to right, leading to a complete exposure of theanterior aspect of the sphincter. Subsequently the LES was dissected dor-sally, allowing for a complete mobilization of the distal esophagus withcareful identification of both vagal nerves. Before the performance of theactual fundoplication a posterior hiatoplasty was carried out in all casesusing one nonabsorbable stitch. Thus, the dissection of the LES region wasidentical in all four procedures.

During the anterior 180° hemifundoplication the fundic wrap waspulled to the right side in front of the distal esophagus. It was subsequentlysutured to the left lateral aspect of the LES with a single stitch. Two furtherstitches were used for a fixation of the fundus at the LES, and finally, twostitches were performed to fixate the anterior aspect of the fundic wrap onthe right crus of the diaphragm.

During the posterior 180° hemifundoplication according to Toupet thedorsal part of the fundic wrap was pulled through behind the esophagusfrom left to right. This dorsal part of the fundic wrap was then sutured withtwo single stitches to the right crus of the diaphragm starting just above thehiatoplasty. The posterior wrap was additionally fixed with two singlestitches each between the fundic wrap and the right as well as the leftborder of the LES.

During the 360° fundoplication according to Nissen-DeMeester thedorsal part of the fundic wrap was pulled through behind the esophagusfrom left to right, creating a symmetric wrap of a dorsal and anterior fundicflap around the LES; then the short and floppy 360° wrap was positionedat the LES using the posterior and the anterior fundic flap by running asingle U suture through both flaps and the right lateral aspect of the esoph-ageal wall. In order to enforce this suture, 1-cm absorbable pledgets (Ethi-sorb) were used on each side of the fundic flaps underneath the stitches.During the 360° fundoplication according to Nissen-Rossetti a similar pro-cedure was performed as during the Nissen-DeMeester version; however,in this case the wrap was longer, with four single stitches between theupper and the lower aspect of the fundus and two further single stitchesbetween the anterior part of the fundic wrap and the anterior wall of thestomach.

Nonabsorbable sutures (Seralene, Serag-Wiessner Inc., Naila, Ger-many) were used during all procedures. During the performance of theactual fundoplication a 9-mm tube was passed into the esophagus to allowfor a calibration of the cardia. At the end of each procedure the abdomenwas desufflated and the 5 trocar incisions were closed with 2 absorbablestitches each.

Postoperative investigations

Following each operation esophageal manometry was immediately per-formed in each animal. Oral feeding was started on postoperative day 1 andi.v. fluids were discontinued. All animals were kept under observation inour animal house for the period of 1 week with daily visits. Subsequentlythe animals returned to a farm until 2 months following each operation,when a follow-up endoscopy and manometry were performed in the Ex-perimental Laboratory under general anesthesia according to the above-mentioned protocol and the animals were subsequently sacrificed.

For each investigated group the median, minimum, and maximum val-ues of the four measured manometric parameters were calculated. A sta-tistical comparison between the values of the individual pigs and betweengroups was performed according to their nature using the Wilcoxon RankSum Test for paired and unpaired values.

Results

According to the study protocol, 28 mini-pigs were inves-tigated successfully: following endoscopy and esophagealmanometry the antireflux procedure was performed, imme-

1184

diately followed by a control manometry and 2 months post-operatively by a control endoscopy and esophageal mano-metry.

Preoperative investigations

There were no pathologic findings in any of the animals onendoscopic inspection. The preoperative diet successfullyled to an emptied upper GI tract, allowing for comparableconditions in all animals. The median values of the fourparameters gathered from each preoperative esophageal ma-nometry serving as normal values for the investigated ani-mals are listed in Table 1.

Operative data

The operative time for all procedures ranged between 35and 90 min. In six of the 28 animals we encountered intra-operative problems: In two animals of the anterior hemi-fundoplication group, one animal of the Nissen-DeMeestergroup, and two animals of the Nissen-Rossetti group, bleed-ing from the spleen occurred, which in each case could betreated by electrocoagulation. In one animal of the posteriorhemifundoplication group a left-sided pneumothorax wasdetected intraoperatively. It was treated by insertion of achest drain which could be extracted on extubation. Thepostoperative course in all animals was uneventful with nocomplications.

Postoperative investigations

The follow-up endoscopies 2 months after each operationdid not show pathologic findings in any of the 28 investi-gated animals. There were no signs of a loosening of thewrap in any case. The manometric characteristics of LEScompetence were gathered for each animal immediatelypostoperatively and 2 months after the operation. Figure 1delineates the course of the median values of these param-eters. The graphs show that following all four antirefluxprocedures we found higher median values for the sphinctercharacteristics immediately postoperatively as compared tothe 2-month values, probably due to postoperative tissueedema. When comparing the preoperative values of the LEScharacteristics with the values obtained 2 months postop-eratively in each individual animal, we found the differ-ences listed in Table 2.

A better impression can be obtained regarding the rela-tive change of the four manometric LES characteristics, i.e.,the percentage increase of the postoperative values indi-vidually related to the preoperative values. The median val-

ues of this kind of representation of the obtained measure-ments are depicted in Fig. 2.

Significant differences between the four operativegroups with regard to the relative change of LES character-istics could only be found for LES intraabdominal lengthbetween both 360° fundoplications and the anterior 180°hemifundoplication (p < 0.03) and for LES pressure vectorvolume between both 360° and both 180° procedures (p <0.01).

These results can be summarized as follows: There is animmediate rise in all LES function characteristics; 2 monthsafter the operation this ‘‘edema effect’’ has waned and thetrue mechanical effect of the fundoplication is measured.LES total length increases after all four procedures; how-ever, it is statistically significant only after the Nissen-Rossetti fundoplication. LES intraabdominal length is unal-tered by the two hemifundoplications and doubled by both360° procedures. LES resting pressure is significantly in-creased by all four operations. LES pressure vector volumeis also significantly increased after all four fundoplicationswith increasing degrees proportional to the size of the wrap.

Discussion

This experimental study focused on an optimal standardizedcomparison of different antireflux procedures to learn aboutthe precise mechanical consequences that a surgeon cancause when applying these procedures. The rationale for ourinvestigation is the frequently reported, troublesome sideeffects of antireflux operations such as dysphagia and gasbloat, as well as the (current discussion on the) usefulness ofa tailored approach. Several factors contributed to thechoice of the mini-pig as animal model. The ideal of anerect moving animal model is currently not available forethical and economic reasons. The mini-pig offers a highdegree of anatomical and physiologic congruence with thehuman conditions [26]. For these reasons it has already beenused as an established model for physiologic investigationsof the LES [19]. Further reasons for choosing this animalmodel, especially with regard to standardization, were avail-ability, technical feasibility, and relativity of the plannedprocedures with regard to the subjective impairment of theindividual animal. Due to the aforementioned anatomic andphysiologic congruence to the human condition it was pos-sible to perform the planned procedures (endoscopy, perfu-sion manometry, laparoscopic antireflux procedures) ac-cording to the same protocols and using the same instru-ments as are standard in the treatment of patients.

A possible reservation regarding the use of an animalmodel was that operative procedures designed to treatpathologic conditions would be applied on healthy subjectspresenting physiologic conditions. However, a sufficientcomparison of different operative techniques is only pos-sible with the prerequisite of constant starting conditions,which, in the case of this animal model are guaranteed bythe physiologic structures of the esophagogastric junction.

Four different antireflux procedures were chosen fromthe large spectrum of available operations. Their choice isexplained by the fact that these four represent the clinicallymost established operations; hence, they can be performedwith an appropriate amount of standardization. On the other

Table 1.Manometric characteristics of the LES in the mini-pig (serving asnormal preoperative values)

Manometric characteristics Median Range

LES total length, cm 3 2–5LES intraabdominal length, cm 1 0–3LES resting pressure, mmHg 5 1–16LES pressure vector volume, mmHg2cm 506 129–2,212

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hand, these operations should have a different mechanicalaction at the esophagogastric junction: two procedures in-volving the formation of a 360° wrap each having a differ-ent wrap length and two procedures with a 180° wrap, eachpresenting a different positioning and anchoring of the wrapat the esophagogastric junction. The 360° fundoplicationaccording to Nissen-Rossetti was chosen since it representsthe standard procedure worldwide. The second 360° proce-dure is the DeMeester modification of the Nissen procedure.

This modification had been established in order to reducethe ratio of postoperative problems such as dysphagia, gasbloat, and dumping syndrome. This modified version is cur-rently routinely applied in several centers very successfully[4, 5, 12, 14]. The anterior 180° fundoplication and theposterior 180° fundoplication according to Toupet werechosen as hemifundoplications. Both procedures lead to apartial augmentation of the LES region requiring only alittle mobilization of the fundus. The Toupet technique rep-

Fig. 1. Course of manometric LEScharacteristics.

Table 2. Comparison of pre- and postoperative values of the manometric LES characteristicsa

FundoplicationLES totallength

LES intraabdominallength

LES restingpressure

LES pressurevector volume

Anterior 180° n.s. n.s. p < 0.02 p < 0.02Posterior 180° n.s. n.s. p < 0.001 p < 0.001Nissen-DeMeester n.s. p < 0.04 p < 0.02 p < 0.02Nissen-Rossetti p < 0.04 n.s. p < 0.02 p < 0.02

a n.s.4 no statistical significant difference,p <4 significance value

Fig. 2. A Relative change of manometric LES characteristics (pre-op. vs 2 months postop.).B Relative change of manometric LES characteristics (pre-op.vs 2 months postop.).

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resents a rather comprehensive procedure with positioningand fixation of the fundic wrap behind the esophagus on theright crus and on the right and left border of the esophagus.

The manometric results of the experimental antirefluxprocedures show a rather uniform trend if comparing theimmediate postoperative motility studies with the studiesafter 2 months: The median values of the four LES param-eters were uniformly higher right after the operation thanafter 2 months. This finding can be explained by the tissueedema secondary to the operative trauma at the esophago-gastric junction which had resolved after 2 months.

Both partial fundoplications lead to rather similar me-chanical changes at the LES: The LES total length increasesslightly more with the posterior hemifundoplication accord-ing to the extent of dissection if compared with the anteriorhemifundoplication. Neither procedure leads to a change inthe intraabdominal LES length. The LES resting pressureincreases slightly more following the posterior if comparedto the anterior version, most probably because of a slightkinking phenomenon secondary to the posterior localizationof the wrap and a concomitant ventralization of the esopha-gus.

Following both 360° fundoplications a different situa-tion is encountered, as expected: While the Nissen-Rossettitechnique leads to a distinct prolongation of the LES totallength (60%), the modified DeMeester technique with ashort floppy wrap leads to a rather small increase of LEStotal length (25%) comparable to that following the anterior180° hemifundoplication. However, both 360° wraps lead toa secure intraabdominal position of the LES region with adoubling of the intraabdominal LES length in both groups.Looking at the LES resting pressure increases we again finddifferences in both techniques: The Nissen-Rossetti tech-nique leads to a doubling of the resting pressure, while themodified technique with the loose and floppy wrap leads toa pressure increase (75%) corresponding to that of the pos-terior hemifundoplication.

The change of the manometrically determined LEScharacteristics can be thought of as the mechanical effectbeing exerted by an antireflux procedure. This mechanicaleffect can be measured best by means of the LES pressurevector volume. It is equivalent to the quantitative measurefor the resistance put up by a sphincter against a passingparticle. The comparison of the median values of the LESpressure vector volume demonstrates the different potenciesof the antireflux procedures: The higher the degree of wrapformation, i.e., the more complex the anchoring mechanismat the esophagogastric junction, the more distinct is its me-chanical effect. The weakest augmentation is achieved bythe anterior hemifundoplication. A stronger reconstructioncan be performed with the posterior hemifundoplication dueto the complex fixation of the fundic wrap behind theesophagus, which also leads to an increase in LES totallength. The Nissen-DeMeester procedure with the 360°wrap leads to a further increased mechanical reconstructionwhich finally reaches maximum values with the Nissen-Rossetti technique because of the rather complex long andtight wrap formation.

The historic development of antireflux surgery is char-acterized by a multitude of different techniques, which in-dividually have been propagated by surgical schools. Con-sequently the experience in antireflux surgery was restricted

at different centers usually to one ‘‘school operation.’’ Withdeveloping knowledge on the pathophysiologic backgroundof GERD, surgeons are gradually becoming aware of thefact that the choice of operation should no longer followonly the ‘‘school opinion’’ but rather be based on well-assessed and widely accepted data as well as on the indi-vidual functional defect causing GERD [9, 14]. In the cur-rent literature 21 studies report on manometric investiga-tions before and after antireflux operations: From eightretrospective studies we find five reporting on the Nissenfundoplication [10, 18, 24, 25, 36], one on the Collis op-eration [28], one on the Belsey operation [21], and finallyone on a comparison of the Nissen and Belsey techniques[32]. Five prospective studies investigate the Nissen, Hill,and Watson procedures [1–3, 11, 38]. Finally there are eightprospective randomized studies that compare the Nissenprocedure with a second (2× Angelchik [17, 33], 3× Toupet[22, 23, 34], 1× Lind [37]) or with two further operativetechniques (1× Belsey and Hill [8], 1 × Toupet and Lortat-Jacob [16]). The results of these comparative studies do notallow for a general recommendation on the individual pro-cedures. Three studies report on advantages in applying theNissen fundoplication [16, 17, 33], two studies rather favorthe Toupet technique [22, 34], and three studies see nodifferences in the compared techniques [8, 23, 37].

A general recommendation on ‘‘the best’’ antirefluxprocedure seems therefore not possible, since the spectrumof possible causal factors and their combinations cannot becorrected by one standard operative procedure. There alsoremains a controversial discussion in the future on whetherto use a partial or full wrap. In order to evaluate the appli-cability of the tailored operative concept it is necessary toobtain precise data on the preoperative status and on themechanical effect being exerted by a distinct antireflux pro-cedure. From the surgical technical point of view and fromrecent reports [14, 20, 23, 38] it appears that the mechanicaleffect at the esophagogastric junction can be well tailoredaccording to the chosen operative procedure. However, afinal judgment on whether a specific antireflux procedure issuperior to another can only be answered by long-term pa-tient follow-up.

We conclude from our results that standardized antire-flux operations with different degrees of fundic wrap for-mation can lead to a proportional mechanical effect at theLES according to the size of this wrap. Choosing a distincttype of fundoplication with a determined mechanical effectwill allow for a tailored augmentation of the LES. Thus, itwill be possible to offer GERD patients with an indicationfor an operative therapy the option of an antireflux proce-dure tailored according to the individual functional defect.

References

1. Ackermann C, Margreth L, Muller C, Harder F (1988) Das Lang-zeitresultat nach Fundoplication. Schweiz Med Wochenschr 118: 774

2. Bell RCW, Hanna P, Powers B, Sabel J, Hruza D (1996) Clinical andmanometric results of laparoscopic partial (Toupet) and complete(Rossetti-Nissen) fundoplication. Surg Endosc 10: 724

3. Csendes A, Braghetto I, Korn O, Corte´s C (1989) Late subjective andobjective evaluations of antireflux surgery in patients with refluxesophagitis: analysis of 215 patients. Surgery 105: 374

4. Cuschieri A (1993) Laparoscopic antireflux surgery and hiatal herniarepair. World J Surg 17: 40

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6. DeMeester TR, Bonavina L, Albertucci M (1986) Nissen fundoplica-tion for gastroesophageal reflux disease. Evaluation of primary repairin 100 consecutive patients. Ann Surg 204: 19

7. DeMeester TR (1987) Definition, detection and pathophysiology ofgastroesophageal reflux disease. In: DeMeester TR, Matthews HR(eds) International trends in general thoracic surgery. Benign Esoph-ageal Disease. CV Mosby, St Louis, p 99

8. DeMeester TR, Fuchs KH (1988) Comparison of operations for un-complicated reflux disease. In: Jamieson GG (ed) Surgery of the oe-sophagus. Churchill Livingstone, Edinburgh, p 299

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10. Ellis FH Jr (1985) Nissen fundoplication: a clinical and manometricassessment of results. In: DeMeester TR, Skinner DB (eds) Esophagealdisorders: pathophysiology and therapy. Raven Press, New York, p197

11. European Study Group of Antireflux Surgery (ESGARS) Current sta-tus and trends in laparoscopic antireflux surgery. Endoscopy (in press)

12. Feussner H, Siewert JR (1992) Hat die Antirefluxchirurgie noch eineIndikation?—aus chirurgischer Sicht. Chir Gastroenterol 8: 184

13. Freys SM, Heuer-Jo¨hnk U (1991) In: Fuchs KH, Hamelmann H (eds)Gastrointestinale Funktionsdiagnostik in der Chirurgie. PraktischerKurs: Stationa¨re Osophagusmanometrie. Blackwell, Berlin, p 255

14. Fuchs KH, Heimbucher J, Freys SM, Thiede A (1994) Management ofgastro-esophageal reflux disease 1995. Tailored concept of anti-refluxoperations. Dis Esoph 7: 250

15. Fuchs KH, Freys SM, Heimbucher J, Fein M, Thiede A (1995) Patho-physiologic spectrum in patients with gastroesophageal reflux diseasein a surgical GI-function laboratory. Dis Esoph 8: 211

16. Hay JM, Zeitoun G, Segol Ph, Pottier D (1990) Surgical treatment forgastroesophageal reflux: which procedure is the best? In: Little AG,Ferguson MK, Skinner DB (eds) Diseases of the esophagus, vol II:benign diseases. Futura, Mount Kisco, NY, p 189

17. Hill ADK, Walsh TN, Borger CM, Byrne PJ, Hennessy TPJ (1994)Randomized controlled trial comparing Nissen fundoplication and theAngelchick prosthesis. Br J Surg 81: 72

18. Johansson J, Johnsson F, Joelsson B, Flore´n CH, Walther B (1993)Outcome 5 years after 360° fundoplication for gastro-oesophageal re-flux disease. Br J Surg 80: 46

19. Johnsson F, Joelsson B (1985) Mechanical and physiologic propertiesof the distal esophageal sphincter: a study in the piglet. In: DeMeesterTR, DB Skinner (eds) Esophageal disorders: pathophysiology andtherapy. Raven Press, New York, p 35

20. Kauer WK, Peters JH, DeMeester TR, Heimbucher J, Ireland AP,Bremner CG (1995) A tailored approach to antireflux surgery. J Tho-rac Cardiovasc Surg 110: 141–146

21. Lerut T, Coosemans W, Christiaens R, Gruwez JA (1990) The BelseyMark IV antireflux procedure: indications and long-term results. In:Little AG, Ferguson MK, Skinner DB (eds) Diseases of the esophagus,vol II: benign diseases. Futura, Mount Kisco, NY, p 181

22. Lundell L, Abrahamsson H, Magnus R, Sandberg N, Olbe LC (1991)Lower esophageal sphincter characteristics and esophageal acid expo-sure following partial or 360° fundoplication: results of a prospective,randomized, clinical study. World J Surg 15: 115

23. Lundell L, Abrahamsson H, Ruth M, Rydberg L, Lo¨nroth H, Olbe L(1996) Long term results of a prospective randomized comparison oftotal fundic wrap (Nissen-Rossetti) or semifundoplication (Toupet) forgastro-oesophageal reflux. Br J Surg 83: 830

24. Luostarinen M, Isolauri J, Laitinen J, Koskinen M, Keyrilainen O,Markkula H, Lahtinen E, Uusitalo A (1993) Fate of Nissen fundopli-cation after 20 years. A clinical, endoscopical, and functional analysis.Gut 34: 1015

25. Martinez de Haro L, Parilla Paricio P, Ortiz Escandell MA, MoralesCuenca G, Videla Troncoso D, Cifuentes Tebar J, Garax Pelegrin V(1992) Antireflux mechanism of Nissen fundoplication. Scand J Gas-troenterol 27: 417

26. Nickel R, Schummer A, Seiterle E (1987) Lehrbuch der Anatomie derHaustiere. Paul Parey Verlag, Band III, p 147 ff

27. Nissen R (1956) Eine einfache Operation zur Beeinflussung der Re-fluxoesophagitis. Schweiz Med Wochenschr 86: 590

28. Orringer MB (1985) The combined Collis-gastroplasty-Nissen fundo-plication for gastroesophageal reflux. In: DeMeester TR, Skinner DB(eds) Esophageal disorders: pathophysiology and therapy. RavenPress, New York, p 203

29. Richter JE (1994) Pathophysiological basis of therapy for gastro-esophageal reflux disease. Dis Esoph 7: 223

30. Stein HJ, DeMeester TR, Naspetti R (1991) Three-dimensional imag-ing of the lower esophageal sphincter in gastroesophageal reflux dis-ease. Ann Surg 214: 374

31. Stein HJ, Barlow AP, DeMeester TR, Hinder RA (1992) Complica-tions of gastroesophageal reflux disease: role of the lower esophagealsphincter, esophageal acid/alkaline exposure, and duodenogastric re-flux. Ann Surg 216: 35

32. Stipa S, Fegiz G, Iascone C, Paolini A, Moraldi A, deMarchi C,Addario Cieco P (1989) Belsey and Nissen operations for gastro-esophageal reflux. Ann Surg 210: 583

33. Stuart RC, Dawson K, Keeling P, Byrne PJ, Hennessy TPJ (1989) Aprospective randomized trial of Angelchik prosthesis versus Nissenfundoplication. Br J Surg 76: 86

34. Thor KBA, Silander T (1989) A long-term randomized prospectivetrial of the Nissen procedure versus a modified Toupet technique. AnnSurg 210: 719

35. Toupet A (1963) Technique d’oesophago-gastroplastie avec phreno-gastropexie appliquee dans la cure radicale des hernies hiatales etcomme complement de l’operation d’Heller dans les cardiospasmes.Mem Acad Chir 89: 394

36. Vassilakis JS, Xynos E, Kasapidis P, Chrysos E, Mantides A, Nicolo-poulos, N (1993) The effect of floppy Nissen fundoplication on esoph-ageal and gastric motility in gastroesophageal reflux. Surg GynecolObstet 177: 608

37. Walker SJ, Holt S, Sanderson CJ, Stoddard CJ (1992) Comparison ofNissen total and Lind partial transabdominal fundoplication in thetreatment of gastro-oesophageal reflux. Br J Surg 79: 410

38. Watson A, Jenkinson LR, Ball CS, Barlow AP, Norris TL (1991) Amore physiological alternative to total fundoplication for the surgicalcorrection of resistent gastro-oesophageal reflux. Br J Surg 78: 1088

39. Zaninotto G, DeMeester TR, Schwizer W, Johansson KE, Cheng SC(1988) The lower esophageal sphincter in health and disease. Am JSurg 155: 104

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The dramatic reality of biliary tract injury duringlaparoscopic cholecystectomy

An anonymous multicenter Belgian survey of 65 patients

J.-F. Gigot, J. Etienne, R. Aerts, E. Wibin, B. Dallemagne, F. Deweer, D. Fortunati, M. Legrand, L. Vereecken,J.-M. Doumont, P. Van Reepinghen, C. Beguin

The Belgian Group for Endoscopic Surgery (B.G.E.S.), rue Saint Georges, Feluy, Belgium

Received: 21 February 1997/Accepted: 10 March 1997

AbstractBackground:Most reports concerning the outcome of pa-tients with biliary tract injury during laparoscopic cholecys-tectomy come from tertiary referral centers, and resultscould be very different in the everyday practice of commu-nity surgeons.Objective: The objective is to define the presentation,mechanisms, results of treatment, and long-term outcome ofbiliary tract injuries during laparoscopic cholecystectomy inthe setting of a community surgeon’s practice.Methods:An anonymous retrospective multicenter surveyof 9,959 patients who underwent laparoscopic cholecystec-tomy was conducted by the Belgian Group for EndoscopicSurgery, composed mainly of community general surgeons.Results:Sixty-five patients with bile duct injury were re-ported on; the incidence was 0.5%, varying from 0.35 to1.3% according to the experience of the surgeon. Thirty-four percent of ductal injuries occurred with experiencedsurgeons, often in association with local predisposing riskfactors. Injury occurred in 87% of cases during dissection ofthe Calot triangle, with severe injury occurring in 46% ofpatients. Intraoperative cholangiography was performed in34% of patients and was associated with a significantlyimproved operative detection rate of injury (68% vs 32%,p4 0.007). Operative detection of injury occurred in 45% ofpatients; diffuse bile ascitis was encountered postopera-tively in 29%. The overall mortality was 9%, the postop-erative biliary complication rate 31%, and the reinterventionrate 14%. During a median follow-up of 49 months (range,3–78 months), 20 of the 61 surviving patients (33%) hadrecurrent biliary strictures. Multivariate analysis demon-strated that the age of the patient (odds ratio: 0.893) and the

presence of biliary peritonitis (odds ratio: 0.061) were in-dependent predictive factors for mortality and that the ageof the patient (odds ratio: 1.049) and the occurrence ofpostoperative biliary complications (odds ratio: 0.161) afterthe initial biliary repair were independent predictive factorsfor late biliary stricture.Conclusions:Biliary tract injury is associated with signifi-cant mortality and complications in the practice of Belgiancommunity surgeons. Intraoperative detection of ductal in-jury by the routine use and a correct interpretation of intra-operative cholangiography improved outcome. The impactof the primary biliary repair on long-term outcome is anargument to refer these patients to specialized multidisci-plinary experts. The results highlight the importance of sur-gical experience, proper selection of patients for laparoscop-ic cholecystectomy, and conversion to laparotomy in diffi-cult cases.

Key words: Biliary tract injury — Laparoscopic cholecys-tectomy

Despite worldwide acceptance of laparoscopic cholecystec-tomy (LC) as the ‘‘gold standard’’ in the treatment of cho-lelithiasis [2, 22, 23] biliary tract injury (BTI) remains themost serious complication encountered with this procedure.Compared with open cholecystectomy, an increased rate ofBTI during LC has been reported [6, 12, 15, 21, 28, 30].Moreover, the incidence of BTI in various multicenter Eu-ropean surveys reaches 0.2–1% [7, 9, 11, 14, 15, 31, 32, 34,37–39]. Most reports concerning the outcome of patientswith BTI have come from tertiary referral centers [1, 5, 10,20, 27, 29, 40] and these results could be very different fromthose obtained in more general surgical practice [19, 26,32]. The expertise in these highly specialized centers and

Correspondence to:J.-F. Gigot, Department of Digestive Surgery, Saint-Luc University Hospital, Hippocrate Avenue, 10, 1200 Brussels, Belgium

Surg Endosc (1997) 11: 1171–1178

SurgicalEndoscopy

© Springer-Verlag New York Inc. 1997

the selection of patients there could represent a bias in re-porting the results of treatment. Thus, the most severely illpatients might have died before referral, and successfullytreated patients might not have been referred to these cen-ters. To determine the short-term and long-term outcomes ofpatients with BTI in routine surgical practice, we undertookan anonymous multicenter survey within a Belgian multi-center surgical association. The Belgian Group for Endo-scopic Surgery (BGES), which includes mainly communitysurgeons.

Materials and methods

Ninety-eight Belgian surgeons—members of the BGES—received the pro-posal that they review retrospectively and anonymously their experiencewith LC, focusing on patients presenting with BTI. Seventy-five surgeons(77%) agreed to participate in the study (67 community surgeons and eightacademic surgeons). Thirty-two of the surgeons included some patientswith BTI in the survey. BTI was defined as an injury of any part of themajor extrahepatic biliary tract, excluding biliary leakage from the cysticduct or the gallbladder fossa with an intact extrahepatic biliary system.Anonymity of patients for each participating surgeon was guaranteed bythe first author, as the scientific coordinator of the group. An extensivequestionnaire was sent to the surgeons concerning their overall biliarylaparoscopic experience; the number of patients with BTI; their biliarylaparoscopic experience at the time of the BTI; the clinical data for thepatients; the intraoperative findings, including mechanism, site, and type ofBTI; the postoperative course of the patients; the need for reintervention;the number and type of biliary repairs; and the long-term follow-up (fo-cusing on biliary-related mortality and late biliary stricture). Patients’ files,cholangiographies, and any videotapes of the intervention were reviewed.A ‘‘primary’’ BTI was defined as an injury caused and repaired by thesurgeon performing the initial LC. The incidence of primary BTI duringLC was estimated for the entire group of surgeons, and for each individualsurgeon. Inclusion of patients referred for secondary biliary repair allowedfor some surgeons to correct their real incidence of bile duct injury.

The ‘‘French technique’’ of LC described by Dubois [13] and Perissat[25] was used in all patients. Electrocautery was the method of choice fordissection of the triangle of Calot and cholecystectomy.

Statistical analysis included use of the Fisher exact test for categoricalvariables and the Wilcoxon test for continuous variables. Multivariateanalysis was performed by logistic regression, using the SAS software. Fordeath and late biliary strictures, the model gives a value of 1 in case ofpresence and of 0 otherwise. Ap value of <0.05 was considered significant.Data are expressed as mean and median values, with ranges.

Results

From February 1990 to October 1993, 9,959 LCs were in-cluded in this study. Sixty-five patients with BTI were re-ported, with primary BTI repair in 50 cases. A secondary(referred) repair of the BTI was performed in 15 patients,mainly in university hospitals (11 patients). There were 46female and 19 male patients. The mean age was 55 years(median, 57; range, 19–80 years), but 14 patients were lessthan 40 years old (22%) and six less than 30 (9%). Theextent of surgical experience with LC for the 50 patientswith primary repair of BTI is given in Table 1.

Incidence

The overall incidence of primary BTI in this group of sur-geons was 0.5% (50 primary BTI in a total experience of9,959 LC), with a range varying for each surgeon from 0 to4%. The incidence of BTI was 1.3% (21 BTI in 1,600

patients) (range, 0–4%) when the surgeon had less than 50cases of experience and 0.35% (29 BTI in 8,242 patients)(range, 0–2.5%) when the surgeon had more than 50 casesof experience (p < 0.0001). The distribution of primary BTIrepairs according to the laparoscopic experience of the sur-geon at the time of BTI is illustrated in Fig. 1. Thirty-twosurgeons were responsible for 50 primary BTIs: 20 surgeons(62%) were responsible for one injury and 12 (38%) formultiple injuries (two BTIs for seven surgeons, three forfour surgeons, and four for one surgeon).

Preoperative clinical presentation

Forty-two patients (65%) presented before LC with clini-cally uncomplicated gallstones (with biliary colic in 38 pa-tients and nonspecific symptoms in 4). Acute cholecystitiswas observed in 14 patients, of whom eight underwentemergency operation and six were operated on after 6–8weeks of medical treatment. Chronic cholecystitis waspresent in five patients, and four patients presented clinicalor biochemical signs of choledocholithiasis.

Preoperative biliary workup included ultrasonographyin all patients, intravenous cholangiography in 32 (49%),and endoscopic retrograde cholangiopancreatography in 13(20%). Preoperative endoscopic sphincterotomy was per-formed in six patients (9%) for common bile duct stoneextraction. The presence of an aberrant right posterior he-patic duct was identified in one patient by preoperative en-doscopic retrograde cholangiopancreatography.

Intraoperative features

Laparoscopic exploration revealed that the gallbladder wasnormal in 34 patients (52%). Acute cholecystitis was

Fig. 1. Distribution of bile tract injury (BTI) according to the laparoscopicexperience of the surgeon (number of laparoscopic cholecystectomies)(LC) at the time of BTI.

Table 1.Surgeon’s experience in laparoscopic cholecystectomy for the 50patients with a primary biliary tract injury

Experience(no. of cases) No. of patients (%)

<10 8 (16) ] (44)10–50 14 (28)50–100 11 (22)>100 17 (34)

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present in 14 patients (including two cases of gangrenouscholecystitis) and scleroatrophic gallbladder in 17. A totalof 51 local predisposing risk factors for BTI were observedduring the surgical dissection in 40 patients (62%) (Table2). The average experience of the surgeon when local pre-disposing risk factors were absent was 65 LCs, comparedwith 150 LCs, when risk factors were present (p < 0.01). Inthe group of patients with primary BTI repair, excludingductal injury during laparoscopic common bile duct explo-ration, BTI occurred in the absence of local predisposingrisk factors in 55% (12 of 22 patients) when the surgeon hadless than 50 cases of experience, whereas BTI occurred withthe presence of these risk factors in 76% (19 of 25 patients)when the surgeon had more than 50 cases of experience(p 4 0.03).

The mechanism of the BTI at LC was identified in 63patients (97%) (Table 3). The injury occurred during dis-section of Calot’s triangle in 55 patients (87%), during thephase of cholecystectomy in five (8%), and during instru-mental transcystic maneuvers for common bile duct explo-ration in three (5%). Details on the mechanism of bile ductinjury are listed in Table 3. Failure to distinguish betweenthe cystic duct and the common bile duct was the mostcommon cause of injury; this was followed by instrumentalinjury and abuse of electrocautery, these two mechanismsusually being associated and related to the hook dissector.

The type and site of the bile duct injury were determinedin all patients. Partial injury occurred in 31 patients, com-plete transsection in 20, wide resection of the extrahepaticbile duct in six, local bile duct coagulation in four, andextensive thermal bile duct necrosis in four. Thus, severeinjury—complete transection, extensive resection, or ther-mal necrosis—was present in 30 patients (46%).

The biliary injury was located at the level of the cho-ledochus in 34 patients, at the common hepatic duct in 24,at the right hepatic duct in three, at an aberrant right pos-terior hepatic duct in three, and at the bifurcation of thehepatic duct in one patient. According to the Bismuth clas-sification [4], type I bile duct injury occurred in 33 patients,type II in 18, type III in six, type IV in two, and type V insix.

Intraoperative cholangiography (IOC) was performed inonly 22 patients (34%); it resulted in the prompt detection ofBTI in 15 patients (68%). In the remaining seven patients,IOC failed to detect the BTI because of misinterpretation bythe surgeon. In five of these patients, the lack of opacifica-

tion of the proximal bile duct system was erroneously con-sidered as normal or related to preferential transpapillarypassage of contrast material due to preoperative endoscopicsphincterotomy. In two of these patients, IOC was normal atthe time of initial LC, but these patients presented withpostoperative biliary peritonitis related to thermal injury.When IOC was not performed (43 patients), BTI was de-tected intraoperatively in 14 patients (33%)—by the occur-rence of bile in the operative field in seven patients, byfurther surgical dissection in six patients, and during con-version to laparotomy because of hemorrhage in one patient.The detection rate of BTI was 68% when IOC was per-formed compared with 32% when IOC was not used (p 40.007). If, when IOC was performed, it had been correctlyinterpreted, this tool would have detected ductal injury in 20of 22 patients (91%). The mean surgical experience whenBTI was detected during surgery was 183 LCs, comparedwith 63 LCs when BTI was not detected (p < 0.002). Therewas no relation between the type and severity of BTI andthe performance of IOC.

Mode of postoperative clinical presentation

Twenty-nine patients (45%) had their bile duct injury de-tected during surgery (group I), mainly by IOC (15 patients,52%). Eight patients (12%) presented with postoperativeexternal biliary fistula (group II). Three patients (5%) had alocalized peritoneal bile collection and 19 patients (29%) adiffuse bile ascitis (group III). Six patients (9%) presentedwith a postoperative biliary stricture (group IV)—in theearly postoperative period in three patients (after a mean of3 days; range, 1–5 days) and later in three other patients(after a mean of 4 months; range, 3–5 months).

Treatment and postoperative results

Six patients died, for an overall mortality of 9%. Four pa-tients died during the initial hospital stay, and two patientshad late biliary-related deaths due to severe cholangitis andrecurrent biliary stenosis. Immediate and late postoperativeoutcome are reported in Table 4.

In group I,all 29 patients were converted to laparotomyand treated by primary biliary suture without biliary drain-age in three patients, primary biliary suture with a T-tube in22, and hepaticojejunostomy in four. When a T-tube wasinserted, the mean duration of biliary drainage was 47 days(range, 10–120 days). Two of these patients underwent suc-cessful primary biliary suture laparoscopically. One patient(3.5%) died from biliary peritonitis and multiple organ fail-ure after primary biliary suture without T-tube drainage; thepostoperative course was complicated by bile ascitis fromsuture breakdown and necrosis. Postoperative biliary com-plications occurred in seven patients (24%), including bio-chemical pancreatitis (one patient), repeated cholangitis(one), external biliary fistula (four) (associated with residualcommon bile duct stone and hemobilia in one patient each),and postoperative bile ascitis (one). Reintervention was nec-

Table 2. Details of 51 local risk factors for biliary tract injury presentduring laparoscopic cholecystectomy in 40 patients (62%)

Risk factors No. of patients

Acute inflammation in the triangle of Calot 19Scleroatrophic cholecystitis with a short

cystic duct 14Huge impacted gallstone in the gallbladder

neck 8Biliary anomaly (aberrant right posterior

hepatic duct) 5Instrumental endobiliary maneuver during

transcystic laparoscopic common bileduct exploration 3

Mirizzi syndrome: gangrenous cholecystitis 1Gallbladder cancer 1

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essary in four patients (14%), including repositioning of theT-tube (one patient), endoscopic sphincterotomy for com-mon bile duct stone extraction with endoscopic stenting(one), external biliary diversion (one), and repeat hepatico-jejunostomy with arterial ligation for a hepatic artery aneu-rysm (one).

In group II, conservative medical treatment was initiallyinstituted in all eight patients, leading to resolution of theexternal biliary fistula in two patients, at 21 and 30 days.Biliary fistula persisted in the remaining six patients. Aftera mean interval of 3 months (range, 0.2–7 months), all eightpatients underwent biliary repair, with hepaticojejunostomyin five patients and biliary suture with T-tube in one. Thetwo remaining patients underwent ‘‘negative’’ reex-ploration, with choledochotomy and T-tube insertion, with-out detection of a type V BTI retrospectively. Biliary leakpersisted postoperatively in these two patients but resolvedspontaneously with subsequent dilatation of the posteriorbile duct system at 50 and 70 months postoperatively, butwithout evidence of clinical biliary complaints. A third pa-tient presented with a partial residual biliary stricture aftertwo previous attempts at surgical repair. There was no hos-pital mortality in this group.

In group III, with 22 patients, two patients with a local-ized collection of bile were treated by combining percuta-neous peritoneal drainage and endoscopic sphincterotomyin one patient and endoscopic stenting in the other. The

postoperative course in these two patients was uncompli-cated, and they remained free of symptoms 50 and 56months later. Twenty patients with diffuse bile ascitis un-derwent biliary repair by laparotomy after a mean of 11days (median, 8; range, 1–41 days). Treatment approachesincluded biliary suture without drainage in one patient, bil-iary suture with T-tube in six, surgical biliary stenting inone, hepaticojejunostomy in six, and total external biliarydiversion in six. Three patients (14%) died from septic bil-iary complications. Eleven patients (50%) had biliary post-operative complications, including external biliary fistula innine, cholangitis in one, and bile peritonitis in two. Fivepatients (23%) underwent reintervention, either with totalexternal biliary diversion, in four patients (with two post-operative deaths), or with reexplorative laparotomy forhemorrhage, in one. Hospital deaths occurred in two of fivepatients (40%) who required reintervention and one of 17patients (6%) who did not require reintervention. The dif-ference is not statistically significant.

In group IV with six patients, five patients underwentsurgery at 1, 2, 5, 120, and 150 days postoperatively. Biliaryrepair consisted of primary suture with T-tube in one patientand hepaticojejunostomy in four. The remaining patient wastreated at 3 months postoperatively by endoscopic stenting,with a successful result 77 months later. No hospital mor-tality, postoperative biliary complication, or reinterventionwas encountered in this group of patients.

Table 3. Mechanism of biliary tract injury during laparoscopic cholecystectomy in 63 patients in whomthe mechanism was identified (97%)

Mechanism of injuryNo. ofpatients

During dissection of the triangle of CalotAnatomic confusion between common bile duct

and cystic duct: During cholangiography 4During surgical dissection 22

and the cystic artery: 1Instrumental injury 13Coagulation 8Cystic duct avulsion 2Common bile duct tenting 2During urgent hemostasis 1Lateral clipping 1Adhesiolysis in front of common bile duct 1

During the phase of cholecystectomyGallbladder neck adherent to common bile duct 3Biliary anomaly 1Coagulation 1

During laparoscopic common bile duct explorationTranscystic balloon dilatation 2Instrumental Dormia basket injury 1

Table 4. Postoperative and long-term outcome in patients with biliary tract injury

Mode of presentation,no. of patients

Postoperative outcome, no. of patients (%)Long-term outcome

Follow-up,median (months)

Late mortality,no. of patients (%)

Late stricture,no. of patients (%)Mortality Biliary complications Reintervention

Operative detection, 29 1 (3.5) 7 (24) 4 (14) 46 1 (3.5) 8 (29)Biliary fistula, 8 0 2 0 46 0 3 (37)Biliary peritonitis, 22 3 (14) 11 (50) 5 (23) 53 1 (4.5) 9 (47)Biliary stricture, 6 0 0 0 58 0 0Entire series, 65 4 (6) 20 (31) 9 (14) 49 2 (3) 20 (33)

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Long-term results

The mean follow-up for the 61 surviving patients was 48months (median, 49; range, 3–78 months). Four patientswere dead at the time of follow-up, from a nonbiliary cause.Twenty patients (33%) presented with a late biliary strictureduring the follow-up period. Sixteen patients had jaundiceor cholangitis related to biliary stricture after a mean inter-val of 11 months (median, 5; range, 2–48 months) and werereoperated on with construction of a hepaticojejunostomy.Two of these patients died from septic biliary complications(one patient in group I and one in group III). Two otherpatients presented with partial biliary stricture 3 and 51months postoperatively without any clinical symptoms. Fi-nally, the two patients with an undetected Bismuth type Vinjury had bile duct dilatation and atrophy of the posteriorliver segments at 50 months and 70 months postoperativelywithout any biliary complaints. The incidence of late biliarystricture was 29% (eight of the 28 surviving patients, in-cluding two with partial stenosis) in group I, 37% (three ofthe eight surviving patients, including the two patients withuntreated Bismuth type V injury) in group II, 47% (nine ofthe 19 surviving patients) in group III, and 0% in group IV(Table 4).

Univariate statistical analysis demonstrated that the ageof the patient and biliary peritonitis were significant predic-tive factors for mortality and that the age of the patient,Bismuth type III injury, and occurrence of postoperativebiliary complications after initial biliary repair were predic-tive factors for late biliary stricture in patients sufferingfrom bile duct injury (Table 5). Multivariate statisticalanalysis (Table 6) determined that the age of the patient(odds ratio: 0.893) and the occurrence of biliary peritonitis(odds ratio: 0.061) were independent predictive factors formortality (c value4 0.857) and that the age of the patient(odds ratio: 1.049) and the occurrence of postoperative bil-iary complications (odds ratio: 0.161) were independentpredictive factors for late biliary stricture in these patients (cvalue4 0.778).

Discussion

The incidence of BTI in this multicenter series (0.5%) issimilar to that reported in other European national surveys(Table 7) [7, 9, 11, 14, 15, 31, 32, 34, 37–39] and that foundin a previous multicenter survey in Belgium [37]. Theanonymous inclusion of patients, the small size of the coun-try, and the participation of academic hospitals to whichbiliary repairs are usually referred are all factors that tend toensure that the reported incidence is an objective one. How-ever, the incidence could still be underestimated, because atthe time of the survey the BGES represented only about80% of all laparoscopic surgeons in Belgium and the sur-geons’ participation rate was only 77%. This incidencenonetheless does reflect the daily practice of Belgian com-munity surgeons rather than that of experts in this field.

The causes of BTI during LC are multifactorial: inherentrisk factors of the laparoscopic approach, lack of adequatesurgeons’ experience with LC, presence of local anatomicrisk factors, use of inappropriate surgical technique duringdissection of the triangle of Calot, lack of liberal conversionto laparotomy in difficult cases, and absence of completedand correctly interpreted intraoperative cholangiography.

Compared with open cholecystectomy, several factorsinherent in the laparoscopic approach could be implicated inthe occurrence of BTI: limitation to two-dimensional vision,loss of manual palpation of the porta hepatis, use of tan-gential and inferior approach to the common bile duct (incomparison with the vertical approach obtained with a rightsubcostal incision) giving suboptimal visualization of thecommon hepatic duct, poor visualization of the operativefield and thus difficulty in the control of bleeding when itoccurs, surgeon’s dependence on the material and on thecamera-holding assistant, blind manipulation of instru-ments, use (or abuse) of electrocautery, and surgeon’s in-experience with this new technology [26, 33].

As previously reported [10, 12, 24, 35, 36], the role ofthe surgeon’s learning curve was again highlighted here,since the incidence of BTI reaches 1.3% for surgeons with

Table 6. Multivariate analysis of predictive risk factors for mortality and late biliary stricture

Variable p valueCoefficient(standard error)

Oddsratio

95%confidence interval

MortalityAge 0.035 0.0535 0.893 0.8042–0.9919Biliary peritonitis 0.021 1.2089 0.061 0.0057–0.6514

Late biliary strictureAge 0.021 0.0207 1.049 1.0074–1.0925Postop. biliary

complications 0.004 0.6314 0.161 0.0468–0.5559

Table 5. Univariate analysis of predictive risk factors for mortality and late biliary stricture

Variable Outcome p value

Mortality Death SurvivingMean patient’s age (range) 68 (54–80) 53 (19–77) 0.02Biliary peritonitis (%) 5/21 (24%) 1/44 (2%) 0.01

Late biliary stricture Stricture No strictureMean patient’s age (range) 48 (19–74) 58 (29–80) 0.02Bismuth type III injury 5/5 (100%) 16/60 (27%) 0.02Postoperative biliary complications 12/20 (60%) 9/45 (20%) 0.003

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less than 50 cases of experience. In 55% of these cases, theprocedure was even described as an ‘‘easy cholecystecto-my,’’ without any predisposing local risk factors for BTI.However, adequate surgical training alone does not protectthe patient against the occurrence of BTI. It is indeed sur-prising to note that one-third of the patients in this surveywere operated on by surgeons with more than 100 cases ofexperience and that in most of the cases in which experi-enced surgeons were responsible for BTI, there were localpredisposing risk factors for ductal injury, such as acuteinflammation or chronic scarring in Calot’s triangle. Thus,this series demonstrated that even for experienced surgeonsproper selection of biliary diseases for the laparoscopic ap-proach remains a key factor in avoiding BTI. Ready con-version to laparotomy in such difficult cases involving in-flammatory changes, aberrant anatomy, or excessive bleed-ing is not to be considered a failure but rather good surgicaljudgment, to ensure the patient’s safety.

All types of ductal injury mechanisms previously re-ported were encountered in this survey, but misidentifica-tion between the common bile duct and the cystic duct,defined as the ‘‘classic injury’’ [5, 10, 29, 33], was the mostcommon. Combined instrumental and thermal injury withthe hook dissector was the second-most-common mecha-nism. Thermal injury due to electrocautery is specific to theLC technique, and therefore great caution should be usedduring dissection of the triangle of Calot [5, 10, 20, 29]. Thequality of the surgical dissection is obviously of the mostimportance in preventing BTI. We advocated strict adher-ence to the principles of surgical dissection described byFrench [13, 25] and American experts [1, 5, 8, 10, 16, 17,20, 27, 29, 33, 40]. These guidelines for safe LC with theFrench technique included (1) adequate exposure and visu-alization of the operative field, (2) opening of Calot’s tri-angle by lateral and inferior traction on the gallbladder neck,(3) blunt dissection of Calot’s triangle avoiding overuse ofelectrocautery, (4) starting the dissection at and clear iden-tification of the cystic duct–gallbladder junction, freeingboth ventral and dorsal aspects of the Calot’s triangle and ofthe upper part of the gallbladder neck, (5) avoiding exces-sive traction on the gallbladder infundibulum to preventtenting of CBD, (6) avoiding blind use of clip or cautery tocontrol bleeding, (7) routine performance of IOC after com-plete dissection of all structures in Calot’s triangle and be-fore any division, and finally and mostly important, (8)

liberal conversion to open cholecystectomy (OC) when theanatomy remains unclear during the surgical dissection.

Intraoperative detection of ductal injury appears to havecontributed to success in the final outcome of patients in thisseries. Hospital mortality, postoperative biliary complica-tions, and reintervention rate were all reduced in the groupof patients with intraoperative detection and repair, espe-cially when compared with patients with biliary peritonitis.Inexperience of the surgeons and the omission of IOC wereclearly implicated in the nondetection of BTI in this survey.Use of IOC was associated with a statistically significan-timprovement in detection of ductal injury. However, awrong interpretation of the IOC occurred in 23% of patients.The presence of contrast material extravasation, lack ofopacification of the proximal bile duct system, and incom-plete opacification of the right posterior intrahepatic bileducts should raise suspicion of BTI [33, 41]. When theanatomy is unclear during surgical dissection, cholangiog-raphy must also be performed to give the surgeon an ana-tomic ‘‘road map’’ [3, 33]. IOC also has the advantage ofalerting the surgeon to the problem of tenting of the com-mon bile duct during clip placement [8], which is also oneof the mechanisms of BTI encountered in this series.

It has been reported that the use of IOC should decreasethe severity of ductal injury [26, 40, 41] but this was notconfirmed in all cases in our study. However, in four pa-tients misidentification between the common bile duct andthe cystic duct during IOC led to the detection of a lateralductal injury and prevented further transsection or wide ex-cision. These patients successfully underwent simple repairwith T-tube insertion and suture. A normal IOC can also beassociated with undetected BTI (1) if the injury occurs laterduring cholecystectomy, after the performance of cholangi-ography, or (2) if there is thermal injury due to electrocau-tery, leading to postoperative localized biliary necrosis orlate stricture, as described in this series. Finally, a correctlyinterpreted IOC increases the chance of detecting BTI [8,12, 30, 40, 41], and its routine use should be advised espe-cially during the learning experience of the surgeons. Thetiming and precise means of performing IOC are of the mostimportance. Cholangiography should be performed early inthe procedure, after complete blunt dissection of the Calottriangle and the upper part of the gallbladder neck—anteriorly and posteriorly—with clear identification and ad-equate clipping of arterial and ductal cystic structures, be-

Table 7. Incidence of biliary tract injury during laparoscopic cholecystectomy in various multicenterEuropean surveys

Country ReferenceYear ofpublication

No. ofoperations

Incidenceof injury (%)

Belgium 37 1992 3,244 0.50France 34 1992 3,606 0.78France 11 1992 6,512 0.44Holland 14 1993 6,076 0.86France 7 1993 3,673 0.60Austria 39 1993 7,351 0.50Holland 15 1994 2,932 1.1Switzerland 31 1994 3,722 0.60Italy 9 1994 6,865 0.26Spain 38 1994 2,342 0.28Norway 32 1995 2,612 0.61

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fore any definitive division is undertaken [10, 16, 17]. Thistype of dissection offers the best chance of preventing BTI.With this approach, inadvertent clipping of an aberrant oraccessory right posterior bile duct will be immediately de-tectable by IOC, preventing a definitive injury and allowingclip removal and repeat cholangiographic examination. Thisoccurred in one patient in this survey, who was therefore notincluded in the study as a true case of BTI. The role of IOCremains controversial regarding its ability to prevent BTI [5,18, 40]. Indeed, in our opinion, the major advantage of IOCis not in preventing injury to the extrahepatic portion of thebiliary tract but in detecting such ductal injury and thereforereducing early postoperative and late complications [41].Multivariate statistical analysis demonstrated that the occur-rence of biliary peritonitis was predictive for mortality, aswas the patient’s age. On the other hand, it is important tostress that the quality of preoperative biliary workup in thisseries had only a minor role in preventing intraoperativeBTI. Indeed, 20% of the patients in this series underwentpreoperative endoscopic retrograde cholangiopancreatogra-phy, and in one of these patients a biliary anomaly wasdetected preoperatively, but subsequent injury during a dif-ficult surgical dissection was not avoided.

Finally, the most striking features in this series were thehigh mortality (9%) and morbidity and the late recurrentstricture rate (33%). These disastrous results, which hadbeen observed as well in a previous Dutch survey [15], areclearly a result of nonoptimal primary treatment. The prob-lems are related to the technical difficulties of restoringbiliary continuity in patients with normal-sized bile ductsand to difficult local conditions caused by biliary peritonitis,especially when biliary repair is performed by nonexpertsurgeons. The inclusion of patients anonymously in thisseries made the reporting of such results possible, and webelieve they are representative of daily surgical practice.Late complications could still be underestimated, as 10–15years of follow-up are mandatory before definitive conclu-sions can be drawn. However, to the best of our knowledge,the follow-up achieved in this series is one of the longestreported in the literature on biliary repair after LC. Theimportance of an optimal initial primary repair in the patientwith BTI is highlighted in this series by the significantrelation, shown by the multivariate statistical analysis, be-tween the occurrence of postoperative biliary complicationsafter the initial repair and the occurrence of late biliarystricture. For optimal care, such difficult patients shouldthus be treated in specialized referral centers, where expertmultidisciplinary teams are available [30, 33, 40].

Acknowledgments.The following members of B.G.E.S. are acknowledgedfor their substantial contribution to the present study: Raymond Aerts,M.D., (Leuven), Thierry Ballet, M.D., (Brussels), Claude Bertrand, M.D.,(Haine-St-Paul), Dany Burnon, M.D., (Brussels), Bernard Dallemagne,M.D., (Liege), Robert de Keuleneer, M.D., (Auvelais), Johan de Mol,M.D., (Kortrijk), Frans Deweer, M.D., (Bonheiden), Claude Desaive,M.D., (Liege), Marc Domb, M.D. (Brussels), Jean-Marie Doumont, M.D.,(Malmedy), Marie-Lou Druart, M.D., (Brussels), Jose´ Etienne, M.D.(Namur), Didier Fortunati, M.D., (Lobbes), Michel Gelin, M.D., (Brus-sels), Jean-Franc¸ois Gigot, M.D., (Brussels), Yves Hoebecke, M.D.,(Haine-St-Paul), Marc Huyghe (Antwerpen), Paul-Jacques Kestens, M.D.,(Brussels), Andre´ Lantin, M.D., (Brussels), Marc Legrand, M.D., (Lie`ge),Baudouin Mansvelt, M.D., (Haine-St-Paul), Michel Meessen, M.D., (Au-velais), Benoıˆt Navez, M.D., (Gilly), Freddy Penninckx, M.D., (Leuven),Jean Saey, M.D., (Mons), Baki Topal, M.D. (Leuven), Jean Vandestadt,

M.D. (Brussels), Patrick van Reepinghen, M.D., (Namur), Etienne vanVyve, M.D., (Brussels), Ludo Vereecken, M.D., (Gent), Paul Vincent,M.D., (Frameries), Ernest Wibin, M.D., (Ottignies), and Jean-PierreYvergneaux, M.D., (Gent). The authors acknowledge Dr. W. Heidel foreditorial assistance and Mrs. N. Thiebaut for secretarial assistance.

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VATS-guided epicardial pacemaker implantation

Hand-sutured fixation of atrioventricular leads in an experimental setting

M. Furrer, 1 J. Fuhrer,2 H. J. Altermatt, 3 H.-B. Ris,1 D. Mettler,4 U. Althaus,1 T. Carrel 1

1 Department of Thoracic and Cardiovascular Surgery, Inselspital, University of Berne, CH-3010 Bern, Switzerland2 Division of Cardiology, Inselspital, University of Berne, CH-3010 Bern, Switzerland3 Institute of Pathology, Inselspital, University of Berne, CH-3010 Bern, Switzerland4 Surgical Research Unit, Inselspital, University of Berne, CH-3010 Bern, Switzerland

Received: 14 October 1996/Accepted: 14 April 1997

AbstractBackground:In neonates and infants epicardial stimulationmay be preferred to endocardial stimulation because ofgrowth-associated lead problems and the risk of vascularcomplications associated with transvenous electrodes. Thisstudy analyzes the feasibility of atrioventricular implanta-tion of a new epicardial lead using the video-assisted tho-racic surgical (VATS) technique in an animal model.Methods:Bipolar steroid-eluting epicardial leads were im-planted in seven young white pigs. In five animals bipolaratrial and ventricular pacing leads (n 4 10) were insertedand fixed by the VATS technique, while two animals servedas controls and underwent implantation through anterolat-eral thoracotomy. Surgical feasibility, pacing, and sensingthresholds of the leads as well as hemodynamic parametersduring pacing were studied. Histological changes beneaththe electrodes were evaluated 1 week after the implantation.Results:All animals survived the pacemaker lead implan-tation. One animal which underwent thoracotomy died be-cause of irreversible ventricular fibrillation induced by rapidventricular pacing. One animal in the VATS group exhib-ited intraoperative herniation of the heart through the peri-cardial window. All animals with left-sided VATS implan-tations demonstrated good individual pacing and sensingthreshold values. The mean cardiac output was 1.6 timeshigher during AAI-mode pacing as compared to VVI-modepacing at a heart rate of 140/min. One animal died postop-eratively due to respiratory failure. No displacements of thepacemaker leads were observed in the survivors.Conclusion:While VATS-guided implantation of epicardi-al, atrial, and ventricular leads is feasible, technical im-provements of the system are mandatory for safe clinicalapplication.

Key words: VATS — Hand suture — Pacemaker implan-tation

Transvenous implantation of permanent atrial or ventricularpacing leads is the method of choice in adults: It is a well-tolerated procedure that is generally performed with localanesthesia under fluoroscopic control [7]. In neonates andinfants, however, epicardial stimulation may be preferablebecause of growth-associated lead problems and the risk ofvascular complications with transvenous electrodes [6, 8,13, 15]. Left-sided cardiac pacing might be advantageousfor optimizing hemodynamics, especially when intraatrialconduction disturbances prevent physiological electricalstimulation [3, 9, 11]. Unfortunately an endocavitary ap-proach to the left side of the heart for pacing is not presentlyfeasible, but it remains an interesting theoretical option.

For patients requiring epicardial placement of atrial orventricular pacing leads, thoracoscopy presents an interest-ing alternative to more extensive surgical approaches (e.g.,midline superior laparotomy with a subxiphoid approach tothe ventricles, left anterolateral thoracotomy or sternotomy).Thus, a thoracoscopic technique has already been advocatedfor the implantation of monopolar epi-/myocardial screw-inor fish-hook-type electrodes [4, 10] as well as for the place-ment of epicardial patches of implantable cardioverter-defibrillator systems [1, 2, 5, 12, 14].

This study analyzes the feasibility of hand suturingatrioventricular implants of a new steroid-eluting epicardiallead to the left and right heart cavities using the VATS(video-assisted thoracic surgery) technique in an animalmodel. Hemodynamic parameters during ventricular pacing(VVI-mode) and atrial stimulation (AAI-mode) were re-corded. Histological changes of the epicardium and myo-cardium beneath these new electrodes were evaluated 1week after implantation.

Methods

Animals/types of interventions

This study was performed on young white pigs weighing between 20 and25 kg. A complete pacemaker system was inserted in seven animals. TwoCorrespondence to:M. Furrer

Surg Endosc (1997) 11: 1167–1170

SurgicalEndoscopy

© Springer-Verlag New York Inc. 1997

control animals underwent anterolateral thoracotomy for lead placement. Infive animals bipolar atrial and ventricular pacing leads were implantatedusing the VATS technique (thoracoscopic fixation of 20 leads). The right-sided VATS approach was abandoned after one case because anatomicconsiderations created technical difficulties for this technique.

Pacemaker system

Steroid-eluting epicardial leads (Medtronic CapSure Epi10366, Minneapo-lis, Inc., Fig. 1) were implanted. The pacing system analyzer was PSA 5311B, Medtronic, Inc., Minneapolis. In the animals which underwent thora-cotomy (No. 1 and 2) monopolar hook electrodes were used as atrial leads(4951 M, Medtronic, Minneapolis, Inc.).

Perioperative management and anesthesia

Perioperative care of the animals was performed according to the guide-lines of the Committee on Animal Care of the University of Berne. Theoperation was performed in the lateral decubitus position. Perioperativeantibiotic prophylaxis consisted of 1 g amoxycillin. The animals werepremedicated with ketamine hydrochloride 10 mg/kg and standard endo-tracheal intubation was performed. A Fogarty catheter was introducedthrough the endotracheal tube and positioned in the left or right mainbronchus, under direct vision using a flexible bronchoscope (Olympus BFtype P10), which allowed selective blockage of one lung. Inhalation anes-thesia consisted of O2 and NO2-halothane. Perioperative monitoring wasperformed with on-line invasive measurements of arterial blood pressureobtained by cannulation of the common carotid artery. Cardiac output wasassessed by thermodilution using a Swan-Ganz catheter introduced throughthe internal jugular vein.

Surgical technique

VATS technique was performed with three lateral incisions of 7–10 mmand an anterior minithoracotomy in the fourth intercostal space (maximallength of 4 cm without rib spreading). A 10-mm rigid trocar sleeve (Au-tosuture Company Division, United States Surgical Corporation, Norwalk,CT) was inserted in the sixth intercostal space posteriorly for the introduc-tion of an endoscopic needle holder and two 7-mm flexible trocar sleeves(Richard Wolf, GmbH, Knittlingen/Germany) were introduced in theeighth intercostal space. One was placed laterally for introduction of a 0°7-mm telescope and a more anterior trocar was for endoscopic clamps andforceps. The endoscopic picture was transmitted to two television screenssituated on either side of the animal. Two control animals underwentanterolateral thoracotomies which included division of the intercostalmuscles and spreading the ribs up to 7 cm.

Pericardial fenestration (3 × 3 cm) was performed anterior to thephrenic nerve at the atrioventricular junction. A first stitch of 5-0 polypro-pylene suture was placed in the ventricle avoiding epicardial vessels. This

suture was passed through the two holes of the pacemaker lead outside ofthe thoracic cavity and a second stitch was placed in the heart more cau-dally. The first ventricular pacemaker lead was then introduced through theminithoracotomy incision and fixed by tightening the suture using theextracorporal technique. The second lead of the bipolar system was fixedin an analogous fashion, respecting a minimal distance of 2 cm from thefirst lead. Bipolar atrial leads were fixed using a similar technique (Fig. 1).For the endoscopic sutures applied to the beating heart we used an endo-scopic needle holder introduced through the lateral trocar sleeve and aconventional forceps introduced through the minithoracotomy wound tocontrol the needle after it passed the ventricular and atrial myocardium.Subcutaneous placement of the leads was performed using a separate ab-dominal incision of approximately 3 cm.

A Charriere 18 G chest tube was introduced and the minithoracotomyand the abdominal incisions were closed in two layers: The trocar incisionswere closed using skin sutures only. Before extubation and removal of thechest tube complete expansion of the lung was confirmed by chest X-ray.All operations were performed by the same surgeon (M.F.).

Postoperative assessment

The following endpoints were assessed:

1. Primary endpoint:● Successful lead placing● Intraoperative mortality and morbidity

2. Secondary endpoints:● Operating time (including pacemaker assessment)● Assessment of pacing and sensing thresholds● Hemodynamic parameters relative to the stimulation mode

Stimulation was performed in the AAI and VVI modes at a rate of 140beats/min. Three measurements of cardiac output were performed beforeand during atrial or ventricular stimulation.

The following parameters were assessed intraoperatively: R- and P-wave reading (baseline/peak; mV), the slew rates (V/s), resistance (V; 2.5V/0.5 ms output) and the stimulation threshold (V; width: 0.5 ms).

After extubation the animals were observed for 7 days to assess theirgeneral condition and eating behavior.

Before sacrificing the animals, complete assessment of the pacemakersystem was repeated under general anesthesia. The implantation sites of thepacemaker leads were examined macroscopically and histologically.

Results

All animals survived the pacemaker lead implantation. Onecontrol animal operated on through a left thoracotomy diedbecause of irreversible ventricular fibrillation, probably in-duced by rapid ventricular pacing.

One animal in the VATS group operated on through theright side exhibited intraoperative herniation of the heartthrough the pericardium with subsequent cardiac arrest:Successful resuscitation was performed with restoration ofsinus rhythm. Because of prolonged low cardiac output fol-lowing the cardiac resuscitation this animal was sacrificedat the end of the operation. Postmortem examination dem-onstrated that the Swan-Ganz catheter had been fixed tightlyintraatrially by one suture of the right atrial leads.

In two animals additional sutures were necessary toclose small lesions of the very thin atrial wall caused by thefixation sutures of the pacemaker leads.

The correct placement of the leads to the surface of thebeating heart and tightening the sutures was time consumingand this maneuver had to be repeated in one-third of theimplanted leads. The operating time (including the assess-ment of pacing and sensing thresholds and hemodynamicmeasurements) ranged from 105 to 120 min for the twocontrol animals. In the left-side VATS group operating time

Fig. 1. Bipolar atrioventricular pacing leads (Medtronic CapSure Epi10366, Minneapolis, Inc.).

1168

decreased during the study period from 195 to 170 (mean179) min (Table 1). The main parameters of pacemakerassessment are summarized in Table 2.

The systemic mean arterial pressure (MAP) and the pul-monary artery pressure (PAP) remained stable after pacingat a rate of 140 (mean prepacing heart rate 101 ± 11). Thecardiac output (CO) did not significantly differ before andduring AAI pacing (2.9 ± 1.0 vs 3.0 ± 1.1 l/min.). However,VVI pacing induced a significant decrease in cardiac outputas compared with AAI pacing—2.0 ± 0.9 vs 3.1 ± 1.4 l/min(p < 0.05, pairedt-test)—in four animals operated on usingthe VATS technique on the left side (Table 3). Animal No.3 suffered from severe postoperative respiratory failurecaused by bronchial obstruction and died after extubation.Postmortem examination of another animal (No. 5) revealeda severe left side bronchopneumonia with significant pleu-ritic and pericarditic changes. Optimal pacemaker functionwas maintained in the surviving animals with uneventfulpostoperative recoveries. No displacement of the pacingleads occurred and histology of the myocardium beneath theleads showed a mild inflammatory infiltrate. Animal No. 5had a severe postoperative infection involving the entirethoracic cavity and the granulocytic infiltration beneath theleads might have been responsible for the pacemaker dys-function observed 1 week postoperatively.

Discussion

The epicardial pacemaker system represents the most prom-ising option in newborns, small infants, and children be-cause of growth-associated lead problems inherent to theendocardial pacemaker system [3, 6, 8, 9, 11, 13, 15]. Thisstudy examines the feasibility of thoracoscopic implantationof a new epicardial pacing lead system, avoiding more ex-tensive surgical approaches like anterior thoracotomy, sub-xiphoid laparotomy, or sternotomy.

In the past, several attempts have been made to mini-mize surgical trauma, (e.g., to insert epicardial patches forimplantable cardioverter defibrillators (ICD) [1, 2, 5, 12,14] or to place monopolar sutureless screw-in or hook leadsby the pericardioscopic or the left thoracoscopic route [4,10]). However, the feasibility of adequate placement usinghand-sutured epicardial fixation of this new generation ofbipolar steroid-eluting leads by the VATS technique has notyet been evaluated. Endoscopic placement of 5.0 sutures inthe beating heart is technically demanding and not only

corresponds to the actual surgical technique used in openheart surgery but may also have some impact on the evo-lution of videoscopic assisted coronary artery bypass sur-gery.

Despite the successful implantation of 10 bipolar pacingleads (endoscopic fixation of a total of 20 leads) in all fiveanimals operated on using the VATS technique, endoscopiccardiac suturing was judged to be difficult. Suturing of theatrial wall is a delicate procedure in this animal model.Small lesions of the atrial wall following fixation of theleads can induce substantial bleeding; this occurred in twoanimals but was managed by additional endoscopic sutures.

The two-dimensional view and the limited freedom ofguiding the instruments (limitations of endoscopic surgicaltechniques) were responsible for the difficulties encoun-tered in placing sutures with precision and in correctly po-sitioning the four leads on the beating heart.

Nevertheless, the operation time decreased continuouslyin the left-side VATS group from 195 to 170 min. It wassignificantly shorter in the control animals which underwentconventional thoracotomies (105–120 min).

Table 1. Technique, operating time, intra- and postoperative complications

AnimalNo. Technique Side

Operationtime (min)

Intraop.complications Remarks

1 Conv. Right 120 No2 Conv. Left 105 Yes Ventricular fibrillation after ventr.

stimulation3 VATS Left 195 No4 VATS Left 180 No5 VATS Left 170 No6 VATS Right 235 Yes Intraop. herniation of the heart

through the pericardium,inadverted fixation of Swan-Ganzcatheter

7 VATS Left 170 No

Table 2a. Assessment of atrial leads (P wave, slew rate, resistance, andstimulation threshold): mean value of all animals, individual values for theleft-side VATS implantation group (animal No. 3, 4, 5, and 7)

P wave(mV)

Slew rate(V/s)

Impedance(W)

Threshold(V)a

Mean 3.5 0.89 582 1.3Animal No. 3 6.6 1.56 382 0.7

4 4.6 2.04 424 1.15 2.0 0.31 1,021 0.67 1.8 0.90 625 0.8

a Width: 0.5 ms.

Table 2b. Assessment of ventricular leads (R wave, slew rate, resistance,and stimulation threshold): mean value of all animals, individual values forthe left-side VATS implantation group (animal No. 3, 4, 5, and 7)

R wave(mV)

Slew rate(V/s)

Impedance(W)

Threshold(V)a

Mean 13.9 2.46 935 0.7Animal No. 3 22.2 3.20 1,022 0.6

4 9.0 1.48 714 0.65 22.0 2.57 714 0.77 10.2 4.00 1,190 1.0

a Width: 0.5 ms.

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According to the results of the intraoperative pacemakerassessment it was not necessary to change the position ofthe leads to improve the pacing or sensing threshold. Allleads of the left-sided VATS group revealed good pacingand sensing threshold values.

The cardiac output was approximately 1.6 times higherduring AAI-mode as compared to VVI-mode pacing at aheart rate of 140 beats/min. This corresponds to the well-known beneficial effect of AV-sequential dual-chamberpacing systems on hemodynamics.

The narrow right thoracic cavity in these small animalsbarely allowed placement of the pacing leads to the rightatrium and right ventricle. The right-sided VATS implanta-tion technique was therefore abandoned because of theseanatomic difficulties, as well as the risk of heart herniationthrough a large pericardial window and the risk of fixationof central endovenous catheters during placement of thesutures in the right atrial wall.

The limited survival rate of animals after successfulpacemaker implantations by the VATS technique was re-lated to postoperative respiratory problems, most probablydue to the single lung ventilation. One animal had a severepostoperative infection. In none of the survivors did dis-placement of the pacemaker leads occur. Close contact be-tween the pacemaker leads to the myocardium was docu-mented by histology.

Conclusions

This study demonstrates that video-assisted implantation ofepicardial atrial and ventricular pacemaker leads is feasible.However, there are many technical difficulties which stillneed to be overcome with additional experience and tech-nical improvement of the system. The VATS technique hasthe potential to minimize the surgical trauma associatedwith open implantation of atrioventricular pacemaker sys-tems in children, especially if the left ventricle needs to bestimulated.

References

1. Bielefeld MR, Yano OJ, Cabreriza SE, Treat MR, Kirby TJ, SpotnitzHM (1993) Thoracoscopic placement of implantable cardioverter-defibrillator patch leads in sheep. Circulation 88/5 II: 447–451

2. Brodman RF, Furman S, Fell SC, Foxx MJ, Frame RA, Fisher JD, KimSG, Roth JA, Ferrick KJ (1994) ICD implantation via thoracoscopy,‘‘mailslot’’ thoracotomy, and subxiphoid incision. Ann Thorac Surg57(2): 475–476

3. Burke RP, Wernovsky G, van der Velde M, Hansen D, Castaneda AR(1995) Video-assisted thoracoscopic surgery for congenital heart dis-ease. J Thorac Cardiovasc Surg 109(3): 499–508

4. Cuschieri A (1994) Technique of thoracoscopic insertion of epicardialpacemaker. In: Cuschieri A, Buess G, Pe´rissat J (eds) Operativemanual of endoscopic surgery 2. Springer-Verlag, Berlin, pp 121–129

5. Ely SW, Kron IL (1993) Thoracoscopic implantation of the implant-able cardioverter defibrillator. Chest 103(1): 271–272

6. Esperer H-D, Singer H, Riede FT, Blum U, Mahmoud FO, Weniger J(1993) Permanent epicardial and transvenous single- and dual-chamber cardiac pacing in children. Thorac Cardiovasc Surg 41: 21–27

7. Furman S, Hayes DL, Holmar DR (1993) A practice of cardiac pacing.Futura, Mount Kisco, pp 261–308

8. Gilette PC, Zeigler VL, Winslow AT, Kratz JM (1992) Cardiac pacingin neonates, infants, and preschool children. PACE Pacing Clin Elec-trophysiol 15: 2046–2049

9. Hesslein PS, Williams WG, Finaly CD (1987) Dual chamber pacing inchildren: transvenous versus epicardial leads. PACE Pacing Clin Elec-trophysiol 10: 441–449

10. Kolesov EV, Lukashev SN, Gaiduk AI (1993) Pericardioscopic im-plantation of electrodes for myocardial electrocardiostimulation. En-dosc Surg Allied Technol 1: 275–276

11. Kratz JM, Gilette PC, Crawford FA, Sade RM, Zeigler VL (1992)Atrioventricular pacing in congenital heart disease. Ann Thorac Surg54: 485–489

12. Mack MJ, Acuff TE, Ryan WH (1993) Implantable cardioverter defi-brillator: the role of thoracoscopy. Ann Thorac Surg 56(3): 739–740

13. Molina JE, Dunnigan AC, Crosson JE (1995) Implantation of trans-venous pacemakers in infants and small children. Ann Thorac Surg 59:659–694

14. Obadia JF, Lehot JJ, Thevenet F, Kirkorian G, Touboul P, Chassign-olle JF (1994) New approach for implantation of automatic defibril-lators using videothoracoscopy. Ann Cardiol Angeiol (Paris) 43(7):384–388

15. Walsh CA, Mc Alister HF, Andrews CA, Steeg CN, Eisenberg R,Furman S (1988) Pacemaker implantation in children: a 21-year ex-perience. PACE Pacing Clin Electrophysiol 11: 1940–1944

Table 3. Hemodynamic parameters before and after pacinga

AnimalHR beforestimulation MAP PAP CO

HR afterstimulation PAP CO

No. 1 102 70 17/12 2.9 ± 0.2 139(AAI140) 21/18 3.1 ± 0.1No. 2 98 75 20/10 3.0 ± 0.1 139(AAI140) 19/10 2.7 ± 0.1No. 4 106 73 35/18 3.7 ± 0.3 136(AAI140) 37/19 3.8 ± 0.1

136(VVI140) 34/17 2.6 ± 0.1No. 5 91 67 34/10 4.1 ± 0.2 139(AAI140) 37/16 4.6 ± 0.2

139(VVI140) 31/15 2.8 ± 0.1No. 6* 120 49 21/17 1.2 ± 0.0 139(AAI140) 23/17 1.5 ± 0.0

139(VVI140) 24/16 0.9 ± 0.1No. 7 90 70 30/21 2.5 ± 0.1 140(AAI140) 34/26 2.5 ± 0.1

139(VVI140) 29/20 1.6 ± 0.1

a Cardiac output (CO) was compared after AAI and VVI stimulation in animals No. 4–7. In animal No.3 correct positioning of Swan-Ganz-catheter was not possible and hemodynamic parameters couldtherefore not be assessed. In animal No. 6 (*) hemodynamic parameters were measured after prolongedcardiac arrest and successful resuscitation (low output). HR4 heart rate, MAP4 mean arterial pressure(mmHg), PAP4 pulmonary artery pressure (mmHg), CO4 cardiac output (ml/min).

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Selection of locally advanced gastric carcinoma by preoperativestaging laparoscopy

D. M. D’Ugo,1 R. Persiani,1 F. Caracciolo,2 P. Ronconi,1 C. Coco,1 A. Picciocchi1

1 Department of General Surgery, ‘‘A. Gemelli’’ Hospital, Catholic University of Rome, Largo Gemelli, 8, 00168—Rome, Italy2 Department of General Surgery, ‘‘G. Moscati’’ Hospital, Via Otranto, 2, 83100—Avellino, Italy

Received: 3 April 1997/Accepted: 19 May 1997

AbstractBackground:The present study is a prospective evaluationof immediate preoperative laparoscopy compared to ultra-sound/computed tomography (US/CT) staging for gastriccancer in a series of 100 patients observed at two majorItalian hospitals from April 1995 through September 1996.Methods:After a complete preoperative work-up all c-M0patients underwent laparoscopy immediately prior to aneventual surgical exploration. pTNM was considered as thegold standard for the evaluation of the results.Results:Laparoscopy detected 21 unsuspected M+ cases outof 100. As regards locally advanced tumors, laparoscopyshowed a sensibility of 69.7% for T3 and 89.6% for T4,significantly higher than US/CT staging (23.2% and 48.3%,respectively;p < 0.02). In this series laparoscopic stagingaltered clinical staging in 58% of cases.Conclusions:This procedure plays two crucial roles in thepreoperative evaluation of advanced gastric cancer: Itmakes it possible to avoid unnecessary surgical explorationin M+ cases and, to date, it represents the most reliable andeconomic tool for the selection of locally advanced tumorsin the light of neoadjuvant treatment.

Key words: Laparoscopy — Gastric cancer staging — Neo-adjuvant chemotherapy

Although declining in incidence, gastric cancer remains acommon malignant tumor in Italy and a major cause ofcancer death since most patients (as in the rest of the west-ern world) have locally advanced or metastatic disease onpresentation. These cases are often understaged by a con-

ventional preoperative workup based on ultrasonography(US) and computed tomography (CT) [6, 14, 17], whichimplies a high percentage of unhelpful exploratory laparot-omies. The value of preoperative video-laparoscopy in theprevention of unnecessary surgical exploration has beenevidenced by previous reports [1, 3, 5, 7, 11, 17], but to datean even more crucial task has been given to preoperativelaparoscopy. In fact, after 30 years of adjuvant treatmenttrials, it has been ascertained that patients who present withlocally advanced but resectable disease (T3-4, N-any) havea low chance of cure after a complete surgical resectionfollowed by an adjuvant chemotherapeutic regimen. Con-sequently an increasing number of institutions throughoutthe world are now recommending a neoadjuvant treatmentprotocol for locally advanced gastric cancers, provided thatthese areproperly staged[16]. In this light laparoscopy hasbeen increasingly employed for screening ‘‘high risk’’ pa-tients with resectable advanced disease [6, 12, 16] even ifno published study until 1996 had prospectively evalu-ated the actual diagnostic efficacy of preoperative video-laparoscopy compared to a conventional staging basedupon US and CT scan.

Materials and methods

In April 1995 we started a prospective study on the clinical value ofimmediately preoperative video-laparoscopy for gastric cancer. In Septem-ber 1996 the protocol was closed after the enrollment of 100 eligiblepatients from two major hospitals (‘‘A. Gemelli’’ Medical Center, Rome,Italy; ‘‘G. Moscati’’ Hospital, Avellino, Italy). We proceeded to immediatepreoperative laparoscopy in every patient with proven adenocarcinoma ofthe stomach after a complete diagnostic workup (upper G.I. X-ray, endos-copy, liver US, and abdominal CT); extra information obtained from en-doscopic ultrasound imaging (EUS) in a selected group of patients was notconsidered for the present study. Patients with clear-cut unresectable tu-mors (e.g. evidence of liver metastasis by US or CT scanning, neoplasticascites, pelvic dissemination of tumor, extraabdominal lymphoadenopathy)were excluded from this protocol. Patients with tumors of the gastric cardiawere also excluded. All patients underwent laparoscopic staging undergeneral anesthesia immediately before an eventual surgical exploration.With the patient supine on the operating table a 12-mm Hasson trocar isinserted in the peritoneal cavity at the umbilicus and a 30° angled laparo-

Presented at the annual meeting of the Society of American Gastrointes-tinal Endoscopic Surgeons (SAGES), San Diego, California, USA, 19–22March 1997Correspondence to:D. M. D’Ugo

Surg Endosc (1997) 11: 1159–1162

SurgicalEndoscopy

© Springer-Verlag New York Inc. 1997

scope is passed through it. A second 5-mm port is then inserted under directvision, lateral to the rectus muscle in the left subcostal region. Unlessperitoneal dissemination or neoplastic ascites are evident, a third 10–12-mm trocar is inserted in the right abdominal quadrant over the umbilicalline to provide an alternative angle of view and possibly direct access to thelesser sac [2]; 100–300 ml of saline is then instilled in the subphrenic areaand in the pelvis and then aspirated for delayed cytologic examination.

Laparoscopic staging is conducted following an ‘‘inverted TNM’’mode, evaluating the M factor first, followed by the N and the T factors.The parietal and serosal surfaces of the peritoneum are inspected initiallyfor malignant implants. In female patients the ovaries must be visualized ina Trendelenburg position in order to exclude Krukenberg metastases. Thevisible surfaces of omentum, diaphragm, and liver are then inspected. Apalpating probe passed through the second 5-mm port to the left of themidline permits manipulation of the left liver lobe and the small bowel.Tilting the table facilitates the approach to the area of the stomach that iscovered by the left liver lobe. Before determining the extent of tumorinfiltration on the gastric wall, the perigastric nodes are inspected along thegreater and the lesser curvature, on the gastrohepatic ligament, and at thehepatic hilum. Most of the anterior wall of the stomach can be inspectedwithout further manipulation. Therefore, we did not initially employ a thirdport. During the study, however, it became evident that a supplementaryinstrument is needed for a more accurate evaluation of posterior infiltrationof the tumor. Occasionally the laparoscope may be inserted through thethird 12-mm port in order to penetrate the lesser sac through the foramenof Winslow. More often, when the tumor originates from the posterior wallor a posterior fixity is suspected, one of the probes may be carefullyinserted behind the stomach through an avascular area of the greater omen-tum. The posterior tumor mass may then be lifted to test its mobility.

No laparoscopic ultrasound technique (LUS) was employed in thecourse of the present study.

Conventional clinical staging (c-stage) and preoperative laparoscopicstaging (lap-stage) were registered separately on a database.

Macroscopic exploration, cytology, and pathologic examination of bi-opsies and surgically resected specimens were considered as the gold stan-dard for pTNM staging. The pTNM classification was used to compare theresults obtained from conventional preoperative US and CT staging withthe laparoscopic findings. The agreement of the two diagnostic procedures(c-stage vslap-stage) with the gold standard was statistically verified bythe Cohen test, and their sensitivity was measured.

Results

As regards theM factor, laparoscopy detected 21 M+ casesout of the total 100 cases, all of which had been clinicallystaged as M0 by preoperative US and CT. Compared to thegold standard, there were no false positives and no falsenegatives in this subset, if the macroscopic appearance ofthe tumor is considered. A theoretical exception can berepresented by two out of the 79 patients declared M0 afterlaparoscopic staging, whose peritoneal lavage appeared tobe microscopically contaminated by tumor cells (Table 1).However, the presence of free-floating cancer cells in theperitoneal cavity is not in itself a contraindication to surgi-cal resection; thus our data confirm that laparoscopy can beconsidered the most specific method for detecting a macro-scopic peritoneal dissemination of tumor or unsuspectedsubcapsular liver metastases, ruling out unresectable can-cers from an unnecessary ‘‘open’’ exploration.

As regardsN-stagingsensitivity (Table 2), standard lap-

aroscopy failed to show a statistically significant differencefrom conventional staging. It must be stressed that the use ofLUS with lymph node biopsies was not considered in ourstudy protocol, as it is our current practice to perform a D2lymphadenectomy in all resectable cases.

The N-stage is certainly an important determinant oftumor curability, but in clinical practice the decision onsurgical resectability is mainly guided by assessment of theT-stage.

As regards the evaluation of the T factor alone, laparos-copy correctly evaluated 56 out of 72 locally advanced T3and T4 cases with a specific sensitivity of 69.7% and 89.6%,respectively (Table 3). In this subset of extraserosal tumors,a case-by-case analysis showed that false results were due tosubtle alterations in the gastric serosa over the tumor, whichpathology showed had not been infiltrated, or due to unde-tected posterior extension of the tumor to the transversemesocolon or to the body of the pancreas.

Laparoscopy shows anoverall TNMstaging accuracy of72%, compared to 38% for US/CT. Differences are moremarked as regards locally advanced tumors: If stages IIIa,IIIb, and IV are considered separately, the predictive valueof laparoscopic staging is 87.5% (Table 4). Out of the total100 patients,lap-stage altered c-stage in 58% of the cases.

No perioperative complications were associated with thelaparoscopic procedure.

Discussion

In Europe and in the United States curative resections areperformed in less than 60% of all gastric cancers [4, 18]. Ithas also been stated [1, 6, 14, 15] that more than 25% ofnewly diagnosed gastric cancer patients will be found (atsubsequent laparotomy) to have been understaged, with se-vere ethical, economic, and quality-of-life implications.Perioperative complications occur in 12–23% of unresect-able patients, with a reported mortality ranging up to 21.1%;patients who do not undergo a surgical exploration have alonger mean survival than those who have laparotomy orbypass [7, 18].

Even before the introduction of endocameras, in a seriesof 360 gastric cancer patients who underwent laparoscopy,Possik and others [9, 13] reported a sensitivity of 83% in thedetection of peritoneal metastases and 87% in the detectionof liver metastases. Kriplani and Kaipur [11] performedpreoperative staging video-laparoscopy in a series of 40patients who were considered resectable after US and CTworkup. In their series laparoscopy showed the presence ofunsuspected M+ disease in 11.5% and unresectable T4 can-cer in 27.5% of patients. In a study performed at the Uni-versity of Munich, Germany [5, 15], 23% of 111 patients

Table 1. M-staging: sensitivity oflap-stage in 100 patientsa

M0 M+ Sensitivity

c-stage 100 — —lap-stage 79 21 100%

a C-stage: US/CT staging;lap-stage: laparoscopic staging

Table 2. N-staging: laparoscopy vs US/CT

Agreement withthe gold standard

K(Cohen test)

US/CT 51% 0.321Laparoscopy 58% 0.416p 4 NSa

a NS: Not statistically significant

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staged by laparoscopy were found to have a previously un-detected carcinomatosis. In a recently published prospectiveevaluation of 103 gastric cancers, mainly located in theupper third of the stomach, Stell [17] stresses that both USand CT have severe limitations in staging these tumors; inhis study laparoscopy clearly showed a better accuracy inthe detection of peritoneal and hepatic metastases. As re-gards the detection of M+ disease, the data obtained fromour prospective study [7] confirm the superiority of preop-erative laparoscopy compared to conventional staging. Itsroutine utilization makes it possible to avoid an unnecessarynoncurative operation for many patients, since M+ diseaseshould not be resected in the absence of obstruction orbleeding. However, this is not the only good reason forextending the use of laparoscopy in the staging of gastriccarcinoma. To date, after conclusive reports from extensiveclinical trials [4, 18], postoperative chemotherapy has notshown evident results in ‘‘high risk’’ tumors; such risk isdirectly related to cancer penetration beyond the gastric se-rosa (T3 and T4) [10]. There are sound theoretical bases forthe selection of these locally advanced cases for a neoadju-vant treatment regimen; nevertheless, no published study todate has prospectively and statistically demonstrated the ac-tual efficacy of laparoscopic-based patient selection com-pared to conventional staging techniques. In this particularcontext our prospective study has demonstrated a highlysignificant difference between laparoscopy and US/CT stag-ing as regards locally advanced tumors (69.7% vs 23.2% forT3; 89.6% vs 48.3% for T4). We think that neoadjuvantregimens for technically resectable gastric cancers are to beadministered only in the context of research studies; sincethere is no definite proof of their efficacy [1], patients witha good outcome with surgery alone must be spared thesubstantial toxicities of these treatments. We now believethat there is enough evidence to consider laparoscopy themost accurate and economic tool for detecting serosal in-vasion of a gastric tumor: Preoperative laparoscopic stagingis therefore appropriate to select locally advanced cancersfor primary neoadjuvant chemotherapy in the hope of lo-cally controlling improvement and possibly increasing thepercentage of delayed curative resections with tumor down-staging [8, 19, 20].

Based upon our results, the current algorithm for oper-able gastric cancer at our institution (Fig. 1) attributes pre-

operative laparoscopy a central role. Moreover, the appli-cation of ‘‘second look’’ laparoscopy in selected cases of-fers the unique possibility of verifying the possible sites ofresidual disease after preoperative treatment.

Conclusions

Immediately preoperative staging laparoscopy is a safe,simple, and relatively cheap procedure at most medical in-stitutions.

As regards locally advanced gastric cancer, our datasupport the belief that to date laparoscopy plays two fun-damental roles: On one hand, it undoubtedly represents themost specific method for detecting previously unsuspectedM+ disease, thus sparing unresectable cases from unneces-sary surgical exploration. On the other hand, following theincreasing application of neoadjuvant treatment protocolsfor stage IIIa–IIIb tumors, we have seen that laparoscopypermits the most reliable and accurate selection of T3 andT4 cases, avoiding an unhelpful delay of surgery in nonad-vanced cases. Accurate staging by preoperative video-laparoscopy allows for a more homogeneous evaluation ofthe treatment results in the context of research studies; fi-nally, the application of ‘‘second-look’’ laparoscopy in se-lected cases may offer a chance to verify a possible tumordownstaging and to detect the sites of residual disease afterneoadjuvant chemotherapy.

References

1. Ajani JA, Mansfield PF, Ota DM (1995) Potentially resectable gastriccarcinoma: current approaches to staging and preoperative therapy.World J Surg 19: 216–220

2. Asencio Arana F (1994) Laparoscopic access to the lesser sac in gas-tric cancer staging. Surg Laparosc Endosc 4(6): 438–440

3. Brady PG, Peebles M, Goldshmid S (1991) Role of laparoscopy in theevaluation of patients with suspected hepatic or peritoneal malignancy.Gastrointest Endosc 37(1): 27–30

4. Brennan MF, Karpeh MS (1996) Surgery for gastric cancer: theAmerican view. Semin Oncol 23(3): 352–359

5. Colin-Jones DJ, Rosch T, Dittler HG (1993) Staging of gastric cancerby endoscopy. Endoscopy 25: 30–48

Table 3. T-staging: sensitivity of laparoscopy vs US/CT

Cases verifiedby pathology US/CT Laparoscopy p

Overall 100 40% 81% <0.02T3 43 23.2% 69.7% <0.02T4 29 48.3% 89.6% <0.02

Table 4. TNM staging: sensitivity of laparoscopy vs US/CT

Cases verifiedby pathology US/CT Laparoscopy p

Overall 100 38% 72% <0.02Stage III 36 19.4% 58.3% <0.02Stage IV 31 25.8% 90.3% <0.02

Fig. 1. Treatment algorithm for gastric cancer.

1161

6. Conlon KC, Karpeh MS (1996) Laparoscopy and laparoscopic ultra-sound in the staging of gastric cancer. Semin Oncol 23(3): 347–351

7. D’Ugo DM, Coppola R, Persiani R, Ronconi P, Caracciolo F, Piccioc-chi A (1996) Immediately preoperative laparoscopic staging for gastriccancer. Surg Endosc 10: 996–999

8. Fink U, Stein HJ, Schuhmacher, Wilke HJ (1995) Neoadjuvant che-motherapy for gastric cancer: an update. World J Surg 19: 509–516

9. Gross E, Bancewicz J, Ingram G (1984) Assessment of gastric cancerby laparoscopy. Br Med J 288: 1577

10. Kelsen DP (1996) Adjuvant and neoadjuvant therapy for gastric can-cer. Semin Oncol 23(3): 379–389

11. Kriplani AK, Kaipur BLM (1991) Laparoscopy for preoperative stag-ing and assessment of operability in gastric carcinoma. GastrointestEndosc 37(4): 441–443

12. Lightdale CJ (1992) Laparoscopy for cancer staging. Endocopy 24:682–686

13. Possik RA, Franco EL, Pires DR, Wohnrath DR, Ferreira EB (1986)Sensitivity, specificity and predictive value of laparoscopy for thestaging of gastric cancer and for the detection of liver metastases.Cancer 58: 1–6

14. Rohde H, Gebbensleben B, Bauer P (1989) Has there been any im-provement in the staging of gastric cancer? Findings from the GermanGastric Cancer TNM Study Group. Cancer 64: 245–2481

15. Sendler A, Dittler HJ, Feussner H (1995) Preoperative staging of gas-tric cancer as precondition for multimodal treatment. World J Surg19(4): 501–508

16. Siewert JR, Maruyama K (1995) What’s new in gastric cancer? (Edi-torial) World J Surg 19: 483

17. Stell DA, Carter CR, Stewart I, Anderson JR (1996) Prospective com-parison of laparoscopy, ultrasonography and computed tomography inthe staging of gastric cancer. Br J Surg 83: 1260–1262

18. Wanebo HJ, Kennedy BJ, Chmiel J, Steele GJ, Winchester D, OsteenR (1993) Cancer of the stomach. A patient care study by the AmericanCollege of Surgeons. Ann Surg 218(5): 583–592

19. Wils J (1996) The treatment of advanced gastric cancer. Semin Oncol23(3): 397–406

20. Yonemura Y, Sawa T, Kinashita K, Matsuki N, Fushida S, Tanaka S,Omijama S, Takashima T, Kimura H, Kamata T, Fujimura T, Sugi-jama K, Shima K, Miyazaki I (1993) Neoadjuvant chemotherapy forhigh-grade advanced gastric cancer. World J Surg 17: 256–252

1162

Hand-assisted laparoscopic vertical banded gastroplasty

Initial report

D. I. Watson, P. A. Game

The Royal Adelaide Centre for Endoscopic Surgery, Department of Surgery, Level 6, Royal Adelaide Hospital,Adelaide, South Australia, 5000, Australia

Received: 4 March 1997/Accepted: 25 March 1997

Abstract. Laparoscopic approaches to surgery for morbidobesity offer to reduce the morbidity associated with con-ventional weight reduction surgery. This paper describes ahand-assisted laparoscopic technique for vertical bandedgastroplasty, a method which shortens and simplifies thelaparoscopic approach to this established open surgical pro-cedure.

Key words: Morbid obesity — Vertical banded gastro-plasty — Hand-assisted technique

Because nonsurgical methods of weight control usually failto achieve desired weight reduction targets, and morbid obe-sity is a significant health problem associated with poorself-esteem and an increased risk of premature death [13],patients continue to present to interested surgeons for gas-tric restriction procedures. A variety of operative techniqueshave been developed and evaluated, and studies now dem-onstrate good long-term outcomes following both gastricbypass and vertical banded gastroplasty [5, 8].

Following the recently demonstrated advantages of re-duced hospital stay, reduced wound-related morbidity andshortened convalescence following other laparoscopic pro-cedures [10, 15], interest has been generated in laparoscopicvariants of gastric restriction procedures for morbid obesity.Due to the simplicity of the placement procedure, the lap-aroscopic placement of an adjustable gastric band has gen-erated most interest [1, 3, 9]. However, the equivalent opensurgical procedure was not widely used before the advent oflaparoscopic placement, and long-term results followinglaparoscopic placement are not yet available. An incidenceof gastric obstruction requiring surgical revision has beenreported following this laparoscopic procedure [12, 14].

In comparison, vertical banded gastroplasty performed

through an upper midline abdominal incision has been usedwidely for the operative treatment of morbid obesity, andhas a well-established role [8]. Lonroth et al. [6] have re-cently described a laparoscopic technique for verticalbanded gastroplasty. Our own early experience with a simi-lar technique applied after initial laboratory development(unpublished data) found this to be a technically demandingprocedure, particularly with the current limitations of lapa-roscopic instrumentation which can make establishing aninitial gastric window with a circular stapling instrumentdifficult.

However, with the recent development of equipmentwhich enables surgeons to introduce their own hand into theinsufflated peritoneal cavity during laparoscopic surgery[2], we have developed a modified technique for laparo-scopic vertical banded gastroplasty, which simplifies theperformance of this procedure.

Methods

Surgical technique

Following the induction of general anesthesia, the patient is placed in thereverse Trendelenburg position with both legs extended in stirrups and withthe hips minimally flexed. The surgeon stands between the patient’s legsand an assistant on the patient’s left. Initial insufflation achieved througha Veress needle inserted immediately below the left costal margin in themidclavicular line is followed by the insertion of three laparoscopic ports(Fig. 1). A 12-mm port (A) is inserted immediately above the umbilicus,providing access for either the laparoscope or a dissecting instrument. Asecond 12-mm port (B) is placed in the left midclavicular line just abovethe level of the umbilicus, providing alternative access for the laparoscopeor for dissecting and suturing instruments. The third port (C) is a 5-mm portwhich is placed laterally in the left flank just below the level of the um-bilicus. A 5-mm incision is made in the epigastrium, for the passage of alarge ‘‘Nathanson’’ liver retractor (Cook Medical Technology, Eight MilePlains, Queensland, Australia) which is then attached to a self-retainingretraction system. This provides excellent exposure of the operative fieldand eliminates the need for an extra assistant.

A 7-cm-long transverse incision is made, approximately 3–5 cm abovethe level of the umbilicus, and centered over the right midclavicular line.Correspondence to:D. I. Watson

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This is deepened through all layers of the abdominal wall to allow theplacement of a Dexterity Pneumo Sleeve (Pilling-Weck USA, ResearchTriangle Park, NC). This allows the repeated introduction of the surgeon’sleft hand as well as a circular stapling instrument into the peritoneal cavitywithout the loss of pneumoperitoneum and laparoscopic exposure. Theassistant manipulates the laparoscope and assists with a grasping instru-ment placed through the left flank port (C) while the surgeon uses his lefthand for manipulation and dissection and manipulates laparoscopic instru-ments through either of the 12-mm ports.

Surgery commences by using left-hand-finger dissection to open anavascular window in the lesser omentum below the hepatic branch of thevagus nerve, thereby rapidly accessing the lesser sac. The surgeon’s indexand middle finger are passed behind the body and cardia of the stomach,toward the angle of His, digitally checking for retrogastric adhesions andlifting the upper part of the gastrosplenic mesentery forward to facilitatedissection of a window at the angle of His, above the uppermost shortgastric vessel. This ensures that stapling instruments can be easily passedbehind the upper stomach for later gastric partitioning.

Next, a point adjacent to the lesser curvature of the stomach is identi-fied 6 cm below the gastroesophageal junction and 2 cm lateral to the lessercurve and marked for the passage of the circular stapling instrument usedto fashion a transgastric window. The head of a 20-mm circular stapler withits detachable sharp spike attached (Ethicon Endosurgery, Johnson &Johnson) is then introduced into the peritoneal cavity through the DexterityPneumo Sleeve, manipulated into the lesser sac, and pushed through theposterior and then anterior gastric walls at the previously marked site. Mostof this manipulation is performed using the left hand, aided by laparoscopicdissecting and cutting instruments. Once the stapler head is in place it isheld securely by the assistant using a laparoscopic grasping instrument, andthe sharp spike is removed. The body of the stapler is next introduced,through the Dexterity Pneumo Sleeve, alongside the left hand, joined to thestapler head, and closed. Before firing, a 36 Fr bougie is passed into the

stomach and manipulated past the stapler along the lesser curve aspect toensure that an adequate gastric lumen remains at the future exit point of theproximal gastric pouch.

Once the stapler is fired, access is available for the passage of one ofthe blades of the 30-mm linear cutting stapler (Ethicon ELC-30, Johnson &Johnson) which is used to partition the stomach. With the bougie remainingin place to calibrate the proximal gastric pouch, the blades of the stapler aremanipulated so that they lie parallel to the lesser curve. The gastric wall isretracted laterally to ensure that the volume of the created proximal pouchis not too large. This maneuver is facilitated by the surgeon’s hand. Thestapler is progressively fired two or three times to reach the angle of His,fashioning a divided gastroplasty, whose proximal pouch will contain be-tween 20 and 30 ml of liquid or solid material.

The lesser omentum is next dissected from the lesser curve adjacent tothe distal end of the staple line, creating a small window. This can usuallybe achieved using careful diathermy dissection. A grasper is then passedfrom left to right, behind the distal part of the gastric pouch, through thesmall window adjacent to the lesser curve. A 1-cm-wide, 6-cm-long pieceof Marlex mesh is pulled through the lesser curve window and wrappedaround the distal outlet of the gastric pouch, while the calibrating bougieremains in place. The Marlex band is sutured firmly around the bougiecalibrated stoma with two or three 2/0 polypropylene sutures to restrict theoutlet of the proximal pouch, completing the procedure.

The bougie is removed and a nasogastric tube is passed into the upperstomach. This tube is used to inflate the proximal stomach with 0.9%sterile saline solution while the outlet is compressed between two fingersto check for possible leakage from the staple lines. The nasogastric tube isleft in place overnight.

Postoperative care

A barium contrast X-ray is obtained on the 1st postoperative day to excludea staple line leak and to verify the adequacy of the surgical anatomy. Oralfluids are commenced on the 1st postoperative day, soft food on 2nd, anddischarge from hospital occurs on the 3rd.

Initial experience

Two patients (one male and one female) have undergone hand-assistedlaparoscopic vertical banded gastroplasty. Preoperative weights were 116and 119 kg (body mass index 37 and 50). One of the procedures wascombined with a laparoscopic cholecystectomy. Operating time was 100min for each procedure. Both patients had an uncomplicated postoperativecourse, were discharged on the 3rd postoperative day, and resumed normalphysical activity within 3 weeks of surgery. The first patient, a policeman,returned to work 1 week after surgery. Following short-term follow-up of3 months one patient has lost 27 kg weight and is eating food of normalconsistency including red meat. The other patient has lost 10 kg weightduring the first 2 months following surgery and is eating soft food withoutdifficulty.

Discussion

Since 1993 a number of centers have described laparoscopictechniques for surgery for morbid obesity, including de-scriptions of laparoscopic vertical banded gastroplasty [6],gastric bypass [7], and the laparoscopic placement of anadjustable gastric band [1, 3, 9]. Uncontrolled prospectivefollow-up of patients who have undergone each of theseprocedures has demonstrated reduced respiratory morbidityand more rapid recovery. However, each technique is asso-ciated with potential difficulties. The procedures of totallylaparoscopic vertical banded gastroplasty and gastric bypassare technically demanding and may exceed the laparoscopicskills currently possessed by the average surgeon. Our ownearlier experience with totally laparoscopic vertical bandedgastroplasty (unpublished data) confirmed the technical dif-

Fig. 1. Port placement for hand-assisted vertical banded gastroplasty.A 411 mm,B 4 11 mm,C 4 5 mm, D 4 liver retractor,E 4 DexterityPneumo Sleeve.

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ficulties associated with manipulation of the circular staplerthrough the gastric wall to fashion the initial gastric win-dow, as well as difficulties guaranteeing that the proximalgastric pouch was an appropriate size.

Laparoscopic placement of an inflatable adjustable gas-tric band offers to reduce the complexity of the laparoscopicapproaches and may be simplest laparoscopic procedure forgeneral surgeons with variable laparoscopic skill levels toperform. For this reason, it has recently been taken up bymany surgeons in Australia and Europe. However, unlikevertical banded gastroplasty, it fails to replicate a widelypracticed open surgical technique, and it is associated withspecific problems. An incidence of proximal pouch enlarge-ment due to slippage of the band has been reported. This canlead to proximal gastric obstruction which requires surgicalrevision [12, 14]. Also reported is an incidence of infectionof the implantable prosthesis, and even erosion of the pros-thesis into the lumen of the stomach [4, 11].

The use of the Dexterity Pneumo Sleeve during laparo-scopic vertical banded gastroplasty simplifies the laparo-scopic performance of this established open surgical proce-dure. Similar advantages have been reported for the use ofthis device during laparoscopic colon resection [2]. In ourexperience, the use of the sleeve reduced the operating timerequired for laparoscopic vertical banded gastroplasty byapproximately 1 h and greatly facilitated the establishmentof the gastric window and the proximal gastric pouch. Theuse of the surgeon’s hand may make this laparoscopic op-tion feasible for surgeons with less advanced laparoscopicskills.

Significantly, the use of a muscle-splitting incision toprovide access for the surgeon’s hand did not adverselyimpact on the length of hospital stay. The 3-day postopera-tive stay compares favorably with the 3–7 days reportedfollowing alternative laparoscopic techniques [2, 3, 6, 9]. Incomparison with the placement of an adjustable laparoscop-ic gastric band, the consumable cost for this procedure inour institution is reduced considerably; US$1,900 vsUS$900 including all staplers and the Dexterity PneumoSleeve. Hand-assisted laparoscopic vertical banded gastro-plasty offers a viable alternative to other laparoscopic ap-proaches for patients with morbid obesity.

Acknowledgment.The authors wish to acknowledge the assistance of Mr.Jonathan Meek, Ethicon Endosurgery, Australia, who provided valuableassistance during preliminary animal studies performed before commenc-ing clinical applications of laparoscopic gastric partitioning techniques.

References

1. Belachew M, Legrand MJ, Defechereux TH, Burtheret MP, Jacquet N(1994) Laparoscopic adjustable silicone gastric banding in the treat-ment of morbid obesity. A preliminary report. Surg Endosc 8: 1354–1356

2. Benelman WA, Ringers J, Meijer DW, de Wit CWM, Bannenberg JJG(1996) Laparoscopic-assisted colectomy with the Dexterity™ PneumoSleeve. Dis Colon Rectum 39: S59–S61

3. Cadiere GB, Bruyns J, Himpens J, Favretti F (1994) Laparoscopicgastroplasty for morbid obesity. Br J Surg 81: 1524

4. Chelala E, Cadiere GB, Favretti F, et al. (1996) Laparoscopic gastro-plasty (LASGB). Obesity Surg 6: 316 (Abstract)

5. Hall JC, Watts J McK, O’Brien PE, et al. (1990) Gastric surgery formorbid obesity. The Adelaide study. Ann Surg 211: 419–427

6. Lonroth H, Dalenback J, Haglind E, et al. (1996) Vertical bandedgastroplasty by laparoscopic technique in the treatment of morbidobesity. Surg Laparosc Endosc 102: 107

7. Lonroth H, Dalenback J, Haglind E, Lundell L (1996) Laparoscopicgastric bypass. Another option in bariatric surgery. Surg Endosc 10:636–638

8. Mason EE (1992) Gastric surgery for morbid obesity. Surg Clin NorthAm 72: 501–513

9. Morino M, Toppino M, Garrone C, Morino F (1994) Laparoscopicadjustable silicone gastric banding for the treatment of morbid obesity.Br J Surg 81: 1168–1169

10. Schirmer BD, Edge SB, Dix J, Hyser MJ, Hanks JB, Jones RS (1991)Laparoscopic cholecystectomy. Treatment of choice for symptomaticcholelithiasis. Ann Surg 213: 665–676

11. Susewind M, Klein S, Kunath U (1996) Problems in laparoscopicgastric banding. Obesity Surg 6: 320 (Abstract)

12. Toppino M, Morino M, Garrone C, Comba A (1996) Disappointinglong-term results of laparoscopic adjustable silicone gastric banding.Surg Endosc 10: 572 (Abstract)

13. Van Itallie TB (1979) Obesity: adverse effects on health and longevity.Am J Clin Nutr 32: 2723–2733

14. Vertruyen M, Cadiere GB, Himpens J, Bruyns J (1996) Reoperationfor total and irreversible food intolerance after laparoscopic adjustablesilicone gastroplasty banding (LASGB). Surg Endosc 10: 570 (Ab-stract)

15. Watson DI, Jamieson GG, Baigrie RJ, Mathew G, Devitt PG, GamePA (1996) Laparoscopic surgery for gastro-oesophageal reflux: be-yond the learning curve. Br J Surg 83: 1284–1287

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Laparoscopic and conventional closure of perforated peptic ulcer

We read with interest the paper by Miserez and colleagues(Surg. Endosc.1996; 10: 831–836), in which the authorsconclude from the results of their study that laparoscopicclosure of perforated peptic ulcer is technically feasible.However, the safety of the method and the benefit for thepatient would need proof by means of a randomized con-trolled trial. As we agree with the authors on the need forfurther research in the field we would like to make someremarks concerning the design of such future studies.

While the precise monitoring of pain intensity and con-sumption of analgesics is appreciated in this study, a majorconcern is that a surgical standard of open closure was notmet in the laparoscopic procedure. Open repair of perforatedulcer included local excision of the ulcer formation. In con-trast to the open procedure, the authors neglected local ulcerexcision in the laparoscopic operation. Compromises of sur-gical standards set in conventional open surgery may dis-parage minimal invasive surgery and therefore must not beaccepted.

In an experimental study in the rat we have recentlyreported that carbon dioxide pneumoperitoneum accentu-ates the extent and severity of peritonitis, assessed by his-topathologic peritonitis severity score and microbiologiccultures of abdominal swabs and blood samples, when theinterval between gastric ulcer perforation and pneumoperi-toneum lasts 12 h or longer [1]. As more than 30% ofpatients suffering from peptic ulcer perforation are subjectto surgical intervention with a delay of more than 24 hbetween perforation and surgery [2], this experimental find-ing may be of clinical importance. In the report by Miserezand associates the time lag between ulcer perforation andsurgical intervention is only mentioned indirectly in the datasummarized by the Mannheim Peritonitis Index. We wouldlike to draw attention to the association between duration ofperitonitis and adverse events in laparoscopic surgery forperitonitis-related conditions. Therefore, detailed informa-tion should be given on the time interval between perfora-tion and surgical intervention in future studies.

In the study by Miserez and colleagues, conversion toopen surgery was necessary in some patients in which lap-aroscopic surgery was started but proved technically infea-sible. The fact that these patients were redistributed to theconventional surgery group is troubling. In light of our ex-perimental study, patients who have been under the influ-ence of pneumoperitoneum should not be transferred to theconventional surgical group after conversion. This may dis-tort the results. Furthermore, it is questionable whether apatient who underwent BII gastrectomy should be includedin the group for conventional closure of perforated pepticulcer.

We are strongly convinced that further sound experi-mental and clinical studies, which focus on potential risks oflaparoscopic management of peritonitis, are needed to de-fine the impact laparoscopic surgery holds in the therapeuticconcept of peritonitis-related conditions.

References

1. Bloechle C, Emmermeann A, Treu H, Achilles E, Mack D, Zornig C,Broelsch CE (1995) Effect of a pneumoperitoneum on the extent andseverity of peritonitis induced by gastric ulcer perforation in the rat.Surg Endosc 9: 898–901

2. Lanng C, Palnas Hansen C, Christensen A, Thagard CS, Lassen M,Klarke A, Tonnesen H, Ostgard SE (1988) Perforated gastric ulcer. BrJ Surg 75: 758–759

C. BloechleA. EmmermannC. Zornig

Department of SurgeryUniversity of HamburgMartinistr. 5220251 HamburgGermany

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The effect of laparoscopy on the movement of tumor cells andmetastasis to surgical wounds

G. Mathew, D. I. Watson, T. Ellis, N. De Young, A. M. Rofe, G. G. Jamieson

The Royal Adelaide Centre for Endoscopic Surgery, Department of Surgery, Royal Adelaide Hospital, Adelaide, South Australia, 5000, Australia

Received: 17 March 1997/Accepted: 6 June 1997

AbstractBackground:A variety of mechanisms have been proposed toexplain tumor growth in port sites following laparoscopic can-cer surgery. We devised two experimental models to deter-mine whether carbon dioxide (CO2) insufflation during lapa-roscopic surgery influences the movement of tumor cells andleads to tumor implantation and growth in surgical wounds.Methods: Model 1:Viable adenocarcinoma cells were in-troduced into the upper abdomen of six syngeneic immune-competent rats during laparoscopy with CO2 insufflation;the same procedure was followed for a further six rats dur-ing gasless laparoscopy. A length of plastic tubing intro-duced through the anterolateral aspect of the rats’ left lowerabdominal wall was used to vent the insufflation gasthrough the abdomen of a recipient rat for 30 min. After 21days, the peritoneal cavity and surgical wounds of the re-cipient rat were examined for implanted tumor.Model 2:Asuspension of radiolabeled adenocarcinoma cells was intro-duced into the upper abdomen of five rats during laparos-copy with CO2 insufflation and an additional five rats dur-ing gasless laparoscopy. A length of plastic tubing intro-duced through the anterolateral aspect of the left lowerabdominal flank was used to vent the insufflation gasthrough phosphate-buffered saline solution. After 30 min,the solution was counted for radioactivity.Results:Tumor growth occurred at the site of both the in-sufflation and venting ports in the second rat in five of thesix rats from the group undergoing insufflation, but it wasfound in none of the gasless laparoscopy group (p 4 0.015).In the second model, significant transfer of tumor cells tothe vented gas occurred only in the rats undergoing lapa-roscopy with insufflation (median, 2.71% versus 0% of theintroduced labeled cells;p 4 0.008).Conclusions:Carbon dioxide insufflation results in tumordissemination during laparoscopy, leading to port site me-tastasis. Gasless laparoscopy may prevent this problem.

Key words: Laparoscopy—Insufflation—Tumor—Wound—Metastasis

Recent reports of tumor metastasis to the access woundsused for the laparoscopic excision of tumors has raised con-cern about the suitability of laparoscopic techniques for theresection of abdominal and thoracic malignancies [4, 12].Unfortunately, evidence from human studies that might sup-port or refute these concerns remains anecdotal, and is basedprincipally on case reports [9]. However, recent studies us-ing small animal models have found an increased incidenceof wound metastasis following laparoscopy in the presenceof intraabdominal malignancy [6, 7]. In addition, studiesusing large animal models have shown that laparoscopy formalignancy can lead to the contamination of laparoscopicinstruments and trocar shafts with tumor cells [1, 5, 10].

Different mechanisms have been postulated to explainthis phenomenon [7, 9, 10]. Metastasis could be the result ofdirect contact between laparoscopic instruments or trocarsand a tumor, resulting in wound contamination when theinstruments are withdrawn during the laparoscopic proce-dure or the trocars are removed at the end of the operation[1, 10]. Alternatively, the tumor cells might be aerosolizedby the insufflation gas, then transported by the gas to thelaparoscopic wounds, instruments, and trocar shafts, thusresulting in wound contamination without direct physicalcontact with tumor-bearing tissue.

We have previously reported a study of an immune-competent syngeneic rat model that showed an increasedincidence of wound metastasis following laparoscopy withCO2 insufflation [7]. The finding that this adverse effect canbe minimized by use of gasless laparoscopic exposure tech-niques [8, 11] suggests that CO2 insufflation during lapa-roscopy promotes wound metastasis. To investigate this hy-pothesis, we developed two additional models.

Materials and methods

Preparation of viable adenocarcinoma suspension

The tumor cell line (DAMA) used for these studies was originally derivedfrom a spontaneously occurring mammary adenocarcinoma native to theDark Agouti (DA) rat strain [3]. Viable DAMA cells were prepared usingthe standard technique of homogenizing fresh tumors propagated in andresected from the female carrier rats. Subcutaneous tumors of∼5 g wereexcised from the carriers and dissected from any surrounding tissue. TheCorrespondence to:D. I. Watson

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tumor was then diced and washed in phosphate-buffered saline (PBS)(sterile 10 mmol/L sodium phosphate buffer, pH 7.0, containing 0.15mol/L sodium chloride). The tissue was homogenized in a motor-drivenPotter Elvehjen homogenizer (radial clearance, 0.5 mm) (Wheaton Ho-mogenizer, Millville, NJ, USA). The crude debris was removed by filtra-tion through sterile gauze. The cell suspension was then centrifuged fourtimes in 10 volumes of PBS at 400 g, each for 1 min. The viability of thesuspension was assessed by trypan blue exclusion, and the cell number wasdetermined using a Neubauer counting chamber (Improved Neubauer, We-ber, UK; depth 0.1 mm, 1/400 m2). The final concentration was adjusted togive 1 × 108 viable cells in 1.0 ml of sterile PBS. This solution was thenintroduced into the epigastric region of the peritoneal cavity of all animalsat the commencement of each experiment.

Model 1

Under general anesthesia, using a combination of halothane and nitrousoxide supplemented with oxygen via a close-fitting mask, 24 male synge-neic immune-competent DA rats underwent one of two different surgicalprocedures. The respiratory status of each animal was closely monitored,and the procedures were performed under sterile operating conditions.

The model consisted of donor rats that underwent either a laparoscopicprocedure facilitated by conventional CO2 pneumoperitoneum or a gaslesslaparoscopic procedure. A recipient rat was connected to the donor rat bya 14-gauge plastic tube inserted into the abdomen (Fig. 1). This cannulaarrangement provided a conduit for carbon dioxide insufflation gas to bevented first from the donor rat through the peritoneal cavity of the recipientrat and subsequently to the atmosphere in the insufflation group, as well asa control group, using gasless laparoscopic exposure.

Six pairs of rats underwent a laparoscopic procedure facilitated byconventional CO2 pneumoperitoneum. Pneumoperitoneum was initially es-tablished in both the donor and recipient rats using a Veress needle placedthrough a small stab incision in the right anterolateral abdominal wall ofeach rat. We slid a disposable mini-laparoscopy cannula (Imagyn Medical,Laguna Niguel, CA, U.S.A.) over the needle to provide access for a 2-mmmini-laparoscope (Imagyn Medical) attached to a conventional laparoscop-ic camera. Under laparoscopic vision, a second mini-laparoscopy cannulawas introduced through the left lower quadrant of the anterior abdominalcavity of the donor rat only. This cannula was then removed, and the endof a piece of 14-gauge plastic tubing (7 cm in length) was introducedthrough the wound so that 5 mm lay within the peritoneal cavity. A purse-string suture was placed around the cannula to achieve a gas-tight seal.

Under laparoscopic vision, an 18-gauge cannula was introducedthrough the anterolateral aspect of the left lower abdominal wall of therecipient rat. It was left open to allow subsequent venting of the insufflationgas. Once the insufflation tube was disconnected from the recipient, themini-laparoscopy cannula used for initial laparoscopy was removed. Thenthe other end of the plastic tubing, which had been placed earlier in thedonor rat, was introduced through the wound and secured with a purse-string suture. Insufflation was commenced through the mini-laparoscopycannula remaining in the donor. The cannulae and tubes were checkedduring insufflation to ensure that gas leaked through the open cannula inthe recipient rat only.

A 20-gauge intravenous cannula was then introduced through the ab-dominal wall in the epigastric region of the donor, and 1.0 ml of theDAMA cell suspension containing 1 × 108 cells was introduced slowly,before sealing of the cannula to prevent subsequent gas leakage. CO2 gaswas insufflated at a flow rate of 0.2 L/min and a maximum pressure of 6mm Hg for 30 min, achieving a constant circulation of carbon dioxidethrough the peritoneal cavities of the two animals. To prevent direct con-tamination of the cannulae with tumor cells or siphoning of fluid from thedonor to the recipient, care was taken to ensure that the cannula tips in bothrats did not come into contact with the abdominal contents or any intra-abdominal fluid. The insufflation phase was terminated by disconnectingthe plastic tubing from the recipient, before removal of the other 18-gaugecannula. All wounds were closed with 3/0 Prolene sutures.

The donor rats were killed 6 days after surgery. An autopsy was per-formed to establish tumor growth within the peritoneal cavity of these ratsand therefore confirm the viability of the tumor cell suspension. The re-cipient rats were housed in the laboratory for 21 days before being killed.At autopsy, the abdomen was opened and examined for tumor deposits. Allof the surgical access wounds were examined for evidence of tumor im-plantation. Histological examination using hemotoxylin-and-eosin stainingof formalin-fixed, wax-embedded tissue was used to confirm the macro-scopic assessment.

A further six pairs of rats underwent laparoscopic surgery using aprotocol identical to the study using carbon dioxide insufflation, except thatinsufflation was omitted and a gasless technique was used [11]. A Veressneedle without insufflation was used for the introduction of the first trocarin each rat. A working space in the abdominal cavity of each rat wasmaintained by suspending the anterior abdominal wall from a wire frame,using multiple 3/0 silk sutures passed through the abdominal wall skin andanchored to the frame. The experiment was concluded in a fashion similarto the insufflation study, with an autopsy of the donor rat at 6 days (toconfirm the viability of the tumor cell suspension) and the recipient rat at21 days.

Model 2

A suspension of 2 × 108 DAMA cells in 2.0 ml of sterile PBS was preparedusing the methods described earlier. These cells were then radiolabeledwith 51Cr–sodium chromate 1MBq, 0.6mg Cr ions (CRIM4, Radio-isotypes, Australia). The cell suspension was incubated for 60 min with51Cr, and the cells were washed five times in sterile PBS. In all instances,>75% incorporation of the51Cr into the tumor cells was obtained.

A total of 10 DA rats were used for this phase of the study. Five of themunderwent laparoscopy with carbon dioxide insufflation, and five hadgasless laparoscopy. Laparoscopic exposure was achieved using methodsidentical to those in the first model. A Veress needle was introducedthrough a stab incision in the left anterolateral abdominal wall of each rat,and a mini-laparoscopy cannula was used to provide access for the mini-laparoscope (Fig. 2). A second mini-laparoscope cannula was introduced

Fig. 1. Port placement for experiment 1. Arrows indicate the direction ofgas flow during CO2 insufflation. A4 primary insufflation port and mini-laparoscope port, B4 20-gauge cannula for the introduction of tumorsuspension, C4 14-gauge plastic tubing, D4 18-gauge venting cannula.

Fig. 2. Port placement for experiment 2. Arrows indicate the direction ofgas flow during CO2 insufflation. A4 primary insufflation port and mini-laparoscope port, B4 20-gauge cannula for the introduction of tumorsuspension, C4 14-gauge plastic tubing, D4 PBS solution.

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through the left lower quadrant anterior abdominal wall and then removedto allow a 7-cm length of 14-gauge plastic tubing to be introduced throughthe wound, 5 mm into the peritoneal cavity, in a fashion similar to the firstexperiment. A pursestring suture was done to maintain an airtight sealaround the tubing. A 20-gauge intravenous cannula was then introducedthrough the abdominal wall in the epigastrium. The open end of the plastictubing was placed in a container of 4 ml of PBS with its opening 5 mmbelow the fluid’s surface. Laparascopic CO2 insufflation was then com-menced, and the vented gas was bubbled though the PBS solution. Gaslesslaparoscopic exposure was obtained in a fashion similar to our first ex-periment. The cannula and tubing positions were identical to those used inthe insufflation group.

At this point, 1 ml of the radiolabelled DAMA cells (∼1 × 108), pre-measured for radioactivity, was introduced into the peritoneal cavitythrough the 20-gauge cannula in the epigastrium of each rat. The cannulawas then sealed. To prevent siphoning of fluid through the venting tube,care was taken to ensure that the tubing within the peritoneal cavity did notcome into direct contact with the abdominal contents or any intraabdominalfluid.

Thirty minutes after the introduction of the radiolabelled DAMA cells,the rats were killed and the radioactivity of the PBS solution was deter-mined using a gamma counter. It was expressed as a percentage of the totalintroduced radioactivity of the cell suspension at the commencement of thestudy. In addition, 4 ml of a control solution of uncontaminated PBS wasscanned to document background radioactivity levels.

Statistics

Fisher’s exact test was used for the analysis of the data sets expressed by2 × 2 contingency tables in experiment 1; the Mann-Whitney U test wasused for analysis of the radioactivity levels in experiment 2. The protocolfor these studies was approved by the Animal Ethics Committees of theInstitute of Medical and Veterinary Science and the University of Adelaide,Adelaide, South Australia.

Results

In the first experiment, extensive tumor growth was evidentthroughout the peritoneal cavity of all donor rats, irrespec-tive of surgical technique, and at all wound sites. This find-ing confirmed the viability of the cell suspension in allinstances. Nodular tumor metastases were found around thesite of both the venting port and the inflow tubing site infive of six of the recipient rats in the group that underwentcarbon dioxide insufflation. Tumor was not seen at anyother sites within the abdominal cavity of the recipient rats.None of the recipient rats in the gasless laparoscopy groupdeveloped metastatic tumor, either around the venting can-nula site (p 4 0.015, Fisher’s exact test), or elsewhere.

The results from the second model are summarized inTable 1. The recovery of the cells introduced into the peri-toneal cavity in the rats undergoing laparoscopy with insuf-flation was significantly greater than for the rats that hadgasless laparoscopy (p 4 0.008).

Discussion

Even though many surgeons still question the significanceof metastases arising in trocar wounds following laparo-scopic surgery for malignant disease, there is increasingevidence, both clinical and laboratory, to suggest a need forgreater caution in the application of laparoscopy to malig-nant growths [2, 4, 6–9, 12]. It has been postulated thatwound metastasis occurs following the direct contaminationof laparoscopic instruments with tumor cells during the lap-aroscopic manipulation of malignant tumors, with resultantspread to abdominal wall wounds by direct transfer whentrocars and instruments are withdrawn from the peritonealcavity [1, 2, 5, 10]. In this instance, the development ofbarrier strategies to protect the wounds during laparoscopicsurgery may be sufficient to overcome the problem. How-ever, it is also possible that cells are moved around by theinsufflation gas used for laparoscopy and transferred towounds without any direct physical contact with contami-nated instruments [6, 7]. If this is the case, then the phe-nomenon of port site metastasis may be a prognosticmarker, indicating generalized tumor spread due to adverseeffects of the laparoscopic environment.

Previous experimental studies using small animal mod-els in our department and elsewhere [6, 7] have shown anincreased incidence of metastasis to trocar wounds follow-ing laparoscopy in the presence of intraabdominal malig-nancy. Further studies have demonstrated that the use ofgasless laparoscopic techniques during laparoscopic ma-nipulation of solid tumors and tumor cell suspensions re-sults in a reduced incidence of wound metastasis and apattern of tumor spread similar to that seen following con-ventional open laparotomy [2, 8, 11]. This work suggeststhat insufflation is a major contributing factor in the devel-opment of laparoscopic wound metastasis.

Studies by Whelan et al. [13], however, have producedconflicting results. Their studies used a quantity of tumorcells that was 1000 times smaller than that used in thecurrent studies, and insufflation was continued for only 10min. Outcome differences may therefore reflect a dose-response relationship. Our initial cell suspension studies [8]suggested that tumor implantation patterns are influencedby the number of viable cells introduced into the peritonealcavity. It is possible that the duration of exposure to thelaparoscopic environment may also be important.

In the current studies, the presence of wound metastasesin the recipient rat in most of the rats undergoing carbondioxide insufflation, and none of the rats in the gaslesslaparoscopy group, provides additional evidence that insuf-flation is essential for the promotion of wound metastases.However, since it could be argued that the study outcomeswere due to siphoning of fluid between the donor and re-cipient rats, we took care to prevent this from happening.Furthermore, if siphoning of fluid had occurred, metastaseswould be expected in the recipient rat in the gasless lapa-roscopy group, and they should have been more prominentaround the inflow port wound in the recipient rats. How-ever, tumor nodules of equal size occurred at both the in-flow and outflow port wounds in the recipient rats under-going insufflation. These results were reinforced by the sec-ond study, which investigated the movement of cells fromthe donor rat. We found significant numbers of cells in the

Table 1. Recovery of radiolabelled cells in model 2

With insufflation(median; range)

Gasless laparoscopy(median; range)

% Recovery of 2.71% (0.41–17.32) 0.00% (0.00–0.03)introduced cells p 4 0.008

Absolute no. of 2.7 × 106 0.0cells recovered (4.1 × 105 to 1.8 × 107) (0.0 to 3 × 104)

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gas vented from the peritoneal cavity of rats undergoinginsufflation, versus either no cells or very few when usinggasless laparoscopy.

A larger inoculum of tumor cells was introduced into thedonor rats in these studies than that used in earlier studies[8] both to maximize the likelihood of metastases develop-ing in the recipient rats and to optimize the likelihood ofdemonstrating differences in tumor implantation patternsbetween the insufflation and gasless laparoscopy groups.Similarly, because of the possible small tumor load in therecipient rats, a longer latency period of 21 days (previ-ously, 7 days) was used to maximize the likelihood of tumorgrowth being clinically evident in the recipient rats.

The current studies assess a laparoscopic environmentthat may be different from that thought to exist during clini-cal laparoscopic cancer surgery. The CO2 leak of 0.2 L/minin the rat model, when extrapolated to clinical surgery, rep-resents a gas leak of 10–15 L/min. Also, a large number oftumor cells were introduced into the peritoneal cavity, andno operative intervention was performed. Nevertheless, itshould be remembered that during clinical laparoscopic sur-gery, high-volume gas leaks do occur during some proce-dures, and the inadvertent liberation of large numbers oftumor cells into the peritoneal cavity can occur. Althoughcareful laparoscopic technique can help to avoid the libera-tion of tumor cells, this cannot be guaranteed preopera-tively, and tumor cell spillage remains a real possibility. Ifthis spillage is combined with CO2 insufflation and a sig-nificant gas leak, the necessary environment for clinicallysignificant port site metastases may be created.

These new studies employing two additional experimen-tal models suggest that laparoscopy with carbon dioxideinsufflation can transport tumor cells to laparoscopic ac-cess wounds and result in the development of metastases. Itappears that this effect can be prevented by the use ofgasless laparoscopy. The precise mechanism for the phe-nomenon, however, is not clear. Whether the differences aredue to the mechanical effects of insufflation, or a metaboliceffect specific to CO2 gas, or a combination of these two,requires further elucidation. Though our investigation con-firms the need for caution when applying laparoscopic tech-niques to malignant growth in humans, further investigationof gasless laparoscopy in clinical studies is also needed.

Acknowledgment:This work was supported by grants from the Universityof Adelaide Faculty of Health Sciences and from the National Health andMedical Research Council of Australia. Dr. G. Mathew is the recipient ofa grant from the Burnside War Memorial Hospital, Burnside, South Aus-tralia.

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