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Journal of Visceral Surgery (2012) 149, e97—e103
Available online at
www.sciencedirect.com
REVIEW
Repeat hepatectomy for liver metastases fromcolorectal primary cancer: A review of the literature
P. Lopez, E. Marzano, T. Piardi, P. Pessaux ∗
Pôle des pathologies digestives, hépatiques et de la transplantation, hôpital de Hautepierre,hôpitaux universitaires de Strasbourg, université de Strasbourg, avenue Molière, 67098Strasbourg, France
KEYWORDSHepatectomy;Metastasis;Colorectal;Repeat hepatectomy
SummaryIntroduction: After hepatectomy for metastases from colorectal cancer (CRC), approximately50% to 70% of patients develop recurrent hepatic metastases. This recurrence is limited to theliver in about one-third of cases. The purpose of this study is to report a comprehensive reviewof the literature concerning the results of repeat hepatectomy for recurrent liver metastases
from CRC.Methods: An electronic literature search was conducted to identify all medical articles pub-lished concerning repeat hepatectomy for liver metastases of colorectal origin during the periodJanuary 1990 to December 2010.Results: After a second hepatectomy, the mean mortality was 1.4% and the mean morbidity ratewas 21.3%. The 5-year survival ranged from 16% to 55%. After a third or fourth hepatectomy, themean mortality rate was 0% and the mean morbidity rate was 24.5%. After a third hepatectomy,the 5-year survival ranged from 23.8% to 37.9%. After a fourth hepatectomy, the 5-year survivalwas 9.3% to 36%.Conclusion: Repeat hepatectomy seems justified, since it may result in prolonged survivalwith acceptable rates of morbidity and mortality, results similar to those seen after initialhepatectomy.© 2012 Elsevier Masson SAS. All rights reserved.Introduction
In Europe, as in the United States, colorectal cancer (CRC) is the second leading cause ofcancer death (In France, CRC is the third most common cancer in men and the second mostcommon in women) [1,2]. Over 50% of patients with CRC develop liver metastases over thecourse of their disease. At the time of diagnosis, synchronous liver metastases are presentin 15—20% of cases [3]. Metachronous liver metastases occur in 25—50% of cases within 3years after resection of the primary CRC [4].
∗ Corresponding author. Tel.: +33 3 88 12 72 63; fax: +33 3 88 12 72 86.E-mail address: [email protected] (P. Pessaux).
1878-7886/$ — see front matter © 2012 Elsevier Masson SAS. All rights reserved.doi:10.1016/j.jviscsurg.2012.01.001
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Although there are no prospective randomized studies,etrospective comparative studies have shown that surgi-al resection of liver metastases with curative intent is thenly treatment that provides prolonged survival. The 5-yearurvival after resection of hepatic metastases from CRC isetween 25% and 44% [5,6]. For many years, multiple orilobar liver metastases were considered a contraindica-ion to surgical resection. At the present time, progressn liver surgery in terms of morbidity and mortality, theevelopment of new strategies (neoadjuvant chemother-py combined with targeted therapies, portal embolization,adio frequency or cryotherapy ablation, two-stage hepate-tomy), and improvements in preoperative assessment haveed surgeons to consider wider and more complex resec-ions. Most recurrences occur within 2 years of the initialepatic resection, but recurrence is limited to the liver innly a third of cases. Treatment of hepatic recurrence is nottandardized and may vary from palliative chemotherapy toomplex surgical re-resection. Various expert surgical cen-ers have reported their experience with the performance ofepeat hepatectomy, and have demonstrated the feasibilitynd safety of the procedure with survival results similar tohose achieved by initial hepatectomy.
The purpose of this study was to report a comprehensivenalysis of results from the surgical literature concerninghe performance of repeat hepatectomy for liver metastasesrom CRC.
aterials and methods
trategy of the literature search
n electronic search of the medical literature waserformed to identify all published articles reporting hepa-ectomy for liver metastases originating from CRC.
The electronic databases of PubMed, Embase, and theochrane Library were searched for the period from January990 to December 2010. All articles published in French ornglish language were selected. The search was refined, forompleteness’ sake, by a manual search of the identified
rticles. When there were repeated publications based onhe same set of patients, only the last publication containinghe largest number of patients was considered. Articles werelassified by level of evidence according to the analysis gridsethodology described in the recommendations for clinicalractice by the Haute Autorité de Santé (www.has-sante.fr).election criteria
nly patient-based studies were considered; all experimen-al studies, editorials, abstracts and reviews were excluded.epeat hepatectomies performed for causes other than CRCetastases were not included in this review (primary liver
umors or metastases from sites other than CRC). Studieshat exclusively analyzed procedures other than surgicalesection (cryotherapy, radio frequency or microwave abla-ion) were also excluded. However, we did include studiesnvolving ablative techniques as a complement to hepa-ectomy where surgery alone was inadequate to achieveomplete resection.
ata extraction
he criteria chosen for analysis were: mortality, morbid-ty, hospital stay, mean survival at 3 and 5 years, mean
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isease-free survival at 3 and 5 years. Data was abstractedrom the text, tables, and figures available in the articles.or repeat hepatectomy, data analysis was limited to seriesith a minimum of 15 patients in order to obtain clinicallyertinent results. There were only a few publications con-erning third and fourth hepatectomies and data was oftenncomplete: therefore, all such series were analyzed regard-ess of the number of patients included. The mean rates ofortality and morbidity were calculated from the results of
he included series. Extreme values were extracted from theighest and lowest rates reported in the selected series.
esults
econd hepatectomy
elected studieshe search yielded 47 articles involving a total of 1810atients (range five to 246 patients). After excluding articlesnvolving fewer than 15 patients, and excluding duplica-ive publications by the same team, we were left with 28rticles with a total of 1744 patients for analysis (range5—246 patients) (Table 1). Only six studies included over00 patients [11,12,20,22,28,35]. All these studies wereeports of patient series without controls and classified asevel 4 evidence. There was one meta-analysis [36] and oneystematic review of the literature [37].
opulationatients undergoing a second hepatectomy representedrom 5—27% of the patients who had undergone initial hep-tectomy. A major hepatectomy was performed in 18—62%t the first procedure and in 0% and 62% at the second pro-edure [21,7].
ortality and morbidityhe average mortality rate was 1.4% (range: 0—18%). The
eading causes of death were respiratory complications0.6%) and hepatocellular insufficiency (0.6%).
The average morbidity rate was 21.3% (range: 6.9—40%).he main causes of morbidity were pulmonary embolism13%), deep abscess (13%), evisceration (4%), and hepato-ellular insufficiency (3.7%). The rate of biliary fistula was.2% (range: 0.8—10%) [36]. The mean operating time was90 minutes (range: 200—913 minutes) (data was availablen only eight studies). The mean volume of blood loss was44 mL (data was available in only ten studies).
urvivaledian survival ranged from 16 months to 56 months. Overall
urvival at 5 years ranged from 16% to 55%. Disease-free 5-ear survival ranged from 16% to 48%. The rate of recurrencefter a second hepatectomy was 66% [36]. This recurrenceas limited to the liver in 15—67% and extrahepatic in7—64% [37].
hird and fourth hepatectomy
elected studieshe search yielded 28 articles reporting a third hepatectomy
nvolving a total of 217 patients (range: one to 60 patients).fter application of the selection criteria for the exploita-ion of available data and the exclusion of duplicative
Repeat hepatectomy e99
Table 1 Results of second hepatectomy for recurrence of liver metastases from colorectal cancer.
Year Number of patients Mortality Morbidity Median survival Survival rate
n (%) (%) (Months) 3 years (%) 5 years (%)
Vaillant et al. [7] 1993 16 6.25 40 33 57 30Elias et al. [8] 1993 41 2.4 44 30 33 NRQue et al. [9] 1994 21 5.0 0 20 60 43a
Fong et al. [10] 1994 25 0 28 30 34 0Nordlinger et al. [11] 1994 130 0.9 25 NR 33 16Fernandez-Trigo et al. [12] 1995 170 0 19 35 45 32Riesener et al. [13] 1996 25 0 26 NR 24 NRTuttle et al. [14] 1997 23 0 22 40 55 32Adam et al. [15] 1997 66 0 20 46 60 41Kin et al. [16] 1998 15 0 20 16 42 21
.5
.6
.5
Yamamoto et al. [17] 1999 75 0Suzuki et al. [18] 2001 26 0Muratore et al. [19] 2001 29 3Petroswky et al. [20] 2002 126 1Takahashi et al. [21] 2003 22 18Adam et al. [22] 2003 199 2
Zacharias et al. [23] 2004 16 7Tanaka et al. [24] 2004 26 0
Hamy et al. [25] 2005 16 0
Sugawara et al. [26] 2005 27 0
Shaw et al. [27] 2006 66 0
Ishiguro et al. [28] 2006 111 0
Nishio et al. [29] 2006 54 6
Ahmand et al. [30] 2006 19 0
Sa Cunha et al. [31] 2007 40 2.5
Thelen et al. [32] 2007 94 3
Treska et al. [33] 2007 24 0
Brachet et al. [34] 2009 62 0
de Jong et al. [35] 2009 246 0.4
NR: not reported.a At 4 years.
publications by the same team, only 11 articles remainedfor analysis. These involved a total of 159 patients (range:one to 60 patients) (Table 2) and were classified as level 4evidence.
The search yielded ten articles reporting a fourth hep-atectomy involving a total of 29 patients (range: one to
Table 2 Results of third hepatectomy for recurrent hepatic m
Year Number of patients Mortality
n (%)
Vaillant et al. [7] 1993 2 0
Nordlinger et al. [11] 1994 12 0
Tuttle et al. [14] 1997 2 NR
Yamamoto et al. [17] 1999 12 NR
Suzuki et al. [18] 2001 6 NR
Yamada et al. [38] 2001 1 NR
Muratore et al. [19] 2001 1 0
Adam et al. [22] 2003 60 0
Taschieri et al. [39] 2003 2 NR
Brachet et al. [34] 2009 15 0
de Jong et al. [35] 2009 46 0
NR: not reported.
10.7 30.5 48 30.527 31 62 326.9 NR 35.1 NR28 37 51 340 23 49 NR23 NR 54 35
30.8 17 25 NR30 32.3 48.4 48.437 42,3 56.8 28.422 41 63 48.718 56.0 68 4414 43 74 4119 50,3 53 4621 48.0 44 2642.5 31,8 55 3124 26,5 55 38NR NR 34 NR17.7 35 NR 3121 51.1 69.9 47.1nine patients). Application of the selection criteria for theexploitation of available data and the exclusion of duplica-tive publications by the same authors, reduced the numberof articles for analysis to four; these involved a total of 16patients (range: two to nine patients) (Table 3) and wereclassified as level 4 evidence.
etastases from colorectal cancer.
Morbidity Median survival Survival rate
(%) (Months) 3 years (%) 5 years (%)
100 31 NR NRNR 12.5 NR NRNR 23 NR NR16.7 NR 37.9 27.633 NR NR NRNR 25.3 NR NR0 NR NR NR25 NR 46 32NR 20 NR NR26.7 43 NR 4423.7 41 NR 23.8
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Table 3 Results of fourth hepatectomy for recurrent hep
Year Number of patients
Chu et al. [40] 1997 2
Yamamoto et al. [17] 1999 3
Pessaux et al. [41] 2006 2
de Jong et al. [35] 2009 9
NR: not reported.
opulationatients who underwent a third hepatectomy representedetween 1% and 10% of patients who had undergone an ini-ial hepatectomy. A fourth hepatectomy was performed inpproximately 1% of patients with a first hepatectomy. Aajor hepatic resection was performed in 0—50% of cases
f third hepatectomy [7,39] and in 0—11% of cases of fourthepatectomy [17,35].
ortality and morbidityhe average mortality rate was 0% after third and fourthepatectomy. For a third hepatectomy, the mean morbid-ty rate was 24.5% (range: 16.7—100%), and mean operativeime was 275 minutes (range: 240—320 minutes) (data analy-is from four articles). For a fourth hepatectomy, operativeime of 286 minutes was reported in only one study [41].he average blood loss was 932 mL (data available in onlyve studies).
urvivalfter a third hepatectomy, median survival ranged from 23o 43 months. The 5-year survival ranged from 23.8% to7.9%. After a fourth hepatectomy, median survival was 18onths and reported 5-year survival ranged from 9.3% to
6%.
rognostic factors
everal prognostic factors with statistical significance haveeen reported in the literature; they are summarized inable 4. Most factors were related to the initial hepate-tomy and included the following: a low serum level of
Table 4 Factors of good prognosis after repeat hepate-ctomy: literature review.
Prognostic factor Number of seriesreporting this factor(references)
Number of metastasesSingle 2 [19,20]≤ 3 lesions 4 [9,15,20,23]≤ 4 lesions 3 [17,24,28]
Size ≤ 5 cm 6 [20,24,29,30,32,41]Topography: 1 lobe only 3 [24,32,38]Appearance:
metachronous8[7,9,15,24,28,30,31,38]
Laboratory: low CEA 6 [19,21,23,29,34,41]R0 resection 3 [17,24,29]Absence of extrahepatic
metastasis4 [17,23,26,41]
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metastases from colorectal cancer.
tality Morbidity Median survival Survival rate(%) (Months) 5 years (%)
NR 18 NRNR NR NR50 NR 3616.7 18.8 9.3
arcinoembryonic antigen (CEA) (variable threshold: lesshan 50 ng/mL or less than 5 ng/mL), the presence of smallless or equal to 4 cm) liver metastases, initial R0 resection,etachronous metastases, a long interval between the ini-
ial and subsequent hepatectomy (more than 6 months orore than 12 months). Other factors were related to the
epeat hepatectomy including: the absence of extrahepaticisease at the time of repeat hepatectomy, R0 re-resection,ow serum CEA, presence of a single metastasis, and smallless or equal to 5 cm) size of metastases.
iscussion
lthough there is no randomized trial comparing the effi-acy of surgical resection to the administration of systemichemotherapy, hepatectomy is considered the only cura-ive treatment and provides prolonged survival as high as6% at 5 years. This remains true even with the advent ofew combination chemotherapy protocols and more recentargeted therapy, which have resulted in median survivalsetween 25 and 30 months. In 2004, two studies showedhat the addition of targeted therapies increased the objec-ive response rate and the progression-free period [42,43].evertheless, 50% to 70% of patients eventually develop aecurrence after hepatectomy; recurrence is isolated withinhe liver in a third of cases [37,40,44,45]. Surveillance innticipation of liver recurrence must be a constant con-
ern in the management of patients with liver metastasesrom CRC. It is important to note that data on the effective-ess of ‘‘modern’’ systemic chemotherapy is still lacking,pecifically in situations of recurrent liver metastasis.When recurrence is limited to the liver, particularly iniew of the regenerative capacity of the liver, several cen-ers have advocated a surgical approach with curative intentn selected patients. In 1993, Vaillant et al. [7] publishedhe first report of more than 15 patients who underwentepeat hepatectomy; the 5-year survival was 30%. In 1994,he multicenter study of the French Association of SurgeryAFC) confirmed these good results with a 3-year survivalate of 33%, a morbidity rate of 25% and a mortality ratef 0.9% [11]. Because repeat liver resection is technicallyore demanding and difficult due to problems of exposure,
riability, parenchymal regeneration, and anatomic alter-tions involving the vascular and biliary ductal planes, oneight expect an increase in mortality and morbidity rates.
et, the average perioperative morbidity is about 20% withn average mortality rate of about 1.5%. These results areimilar to those obtained for patients undergoing an initialepatectomy. In particular, the incidence of hepatocellularnsufficiency and biliary fistula are similar to those seen withrst hepatectomy. A review of the literature on more than000 hepatectomies for colorectal metastasis reported a 4%
Repeat hepatectomy
rate of biliary fistula, a 3% rate of perihepatic abscess, and a2.8% rate of hepatocellular insufficiency [5]. Technical diffi-culties are evidenced by longer operative time and increasedblood loss. No studies have reported data on quality of life.
Median overall survival ranged from 16 to 56 months,with reported 5-year survival from 16—55%. These resultsare no different from those observed after an initial hepa-tectomy. Because of the retrospective nature of the seriesunder study, a selection bias of patients is likely — only thebest cases were candidates for repeat hepatectomy strate-gies.
Various studies have reported factors of poor prognosis:the number and size of metastases, synchronous metas-tases, high CEA level prior to hepatectomy, extrahepaticmetastatic foci, microscopically incomplete resection (R1or R2), and a short interval between the initial hepatectomyand repeat hepatectomy. No factors related to the primarycolorectal tumor have been identified. Most of these factorsare included among the prognostic factors reported for ini-tial hepatectomy in the clinico-biologic scores of Fong [46]or the AFC [47].
High CEA levels may correlate with large tumor volume,but may also be a marker of tumor aggressiveness. It is rea-sonable to believe that most hepatic recurrences are dueto the presence of occult or silent lesions unresected at theinitial hepatectomy. The intrabiliary level of CEA has proveduseless for the detection of possible occult metastases [48].Return of the CEA level to normal after hepatectomy is agood prognostic factor, while the persistence of an elevatedCEA level raises doubts as to the complete resection of alltumor [49] and raises suspicion of the persistence of occultmetastases.
The theoretical concept of curative treatment of col-orectal liver metastases increasingly depends on strategiescombining chemotherapy and surgery. The EORTC study [50]showed an 8.1% progression-free survival benefit at 3 yearsfor patients who received perioperative chemotherapy. Thisstudy should incite to systematically provide perioperativechemotherapy in association with repeat hepatic resectionfor recurrent CRC metastases.
Whether the presence of extrahepatic metastasis is
a contraindication to further hepatic resection remainscontroversial. Several studies have reported extrahepaticmetastasis as a poor prognostic factor. But some authors sug-gest that the presence of an extrahepatic metastatic focusshould not be considered an absolute contraindication torepeat hepatectomy if complete resection of all lesions canbe performed in carefully selected patients [51,52]. Oneargument is that no alternative curative treatment exists. Itwas reported that the number of extra-hepatic lesions wasa worse prognostic factor than the nature or the site of thelesion [53]. The curative determinant is the completenessof the resection.The type of hepatic resection (anatomic or non-anatomic) at the initial or the repeat hepatectomy has notbeen identified as a prognostic factor.
However, the extensiveness of the initial resection maycompromise the feasibility of a future repeat resection.Some authors advocate the sparing of normal hepaticparenchyma for this reason to avoid restricting the possi-bility of anticipated future hepatectomies [54,55].
The use of ablative techniques (radio frequency,cryotherapy, microwave coagulation, and electrolysis) incombination with surgical resection has increased the rateof curative resection. Combined treatment (surgical resec-tion and radio frequency ablation) of metastases that are
e101
unresectable by surgery alone offers a median survival of37.3 months [56]. The development of less-invasive percu-taneous ablative techniques has allowed an increase in thenumber of patients who are eligible for curative resectionand has led some authors to propose this as first-line therapy[57].
All of these studies have limitations and their resultsshould be interpreted with caution. These studies are retro-spective and uncontrolled, and they have patient selectionbias. In addition, the number of patients included is lim-ited and only six studies included more than 100 patients.Finally, the duration over which patients were accrued islong and could not therefore take advantage of technicaladvances, modification of strategies, and the results of newcombination chemotherapy and targeted therapies.
The data suggests that repeat hepatectomy seems jus-tified in the management of recurrent liver metastases ofCRC; in the absence of other alternatives for curative treat-ment, repeat hepatectomy provides a chance of prolongedsurvival with acceptable rates of morbidity and mortality.Generalization from these results, which were achieved atcenters of expertise on a highly selected group of patients,does not allow any definitive conclusion on the true rate ofresectability of hepatic recurrences of CRC.
ESSENTIAL POINTS
• 50—75% of patients who undergo hepatectomyfor metastasis from CRC will develop recurrence;recurrence is limited to the liver parenchyma in athird of cases.
• After repeat hepatectomy, the mean rate ofperioperative morbidity is about 20% and the meanmortality rate is about 1.5%.
• After repeat hepatectomy, the median overallsurvival ranged from 16 to 56 months with a 5-yearsurvival ranging from 16—55%.
• The results for repeat hepatectomy for recurrentmetastases from CRC are no different from thosefor initial hepatectomy.
Disclosure of interest
The authors declare that they have no conflicts of interestconcerning this article.
References
[1] Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2007. CACancer J Clin 2007;57:43—66.
[2] Remontet L, Estève J, Bouvier AM, et al. Cancer incidence andmortality in France over the period 1978—2000. Rev EpidemiolSante Publique 2003;51:3—30.
[3] Fong Y, Kemeny N, Paty P, et al. Treatment of colorectal cancer:hepatic metastasis. Semin Surg Oncol 1996;12:219—52.
[4] Steele GJ, Ravikumar TS. Resection of hepatic metastasesfrom colorectal carcinoma: biologic perspectives. Ann Surg1989;210:127—38.
[5] Simmonds PC, Primrose JN, Colquitt JL, et al. Surgical resec-tion of hepatic metastases from colorectal cancer: a systematicreview of published studies. Br J Cancer 2006;94:982—99.
e
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
[
102
[6] Jaeck D, Bachellier P, Guiguet M, et al. Long-term survival fol-lowing resection of colorectal hepatic metastases: associationfrancaise de chirurgie. Br J Surg 1997;84:977—80.
[7] Vaillant JC, Balladur P, Nordlinger B, et al. Repeat liverresection for recurrent colorectal metastases. Br J Surg1993;80:340—4.
[8] Elias D, Lasser P, Hoang JM, et al. Repeat hepatectomy forcancer. Br J Surg 1993;80:1557—62.
[9] Que FG, Nagorney DM. Resection of recurrent colorectal metas-tases to the liver. Br J Surg 1994;81:255—8.
10] Fong Y, Blumgart LH, Cohen A, et al. Repeat hepatic resec-tions for metastatic colorectal cancer. Ann Surg 1994;220:657—62.
11] Nordlinger B, Vaillant JC, Guiguet M, et al. Survival benefit ofrepeat liver resections for recurrent colorectal metastases: 143cases. J Clin Oncol 1994;12:1491—6.
12] Fernandez-Trigo V, Sharmsa F, Sugarbaker PH, et al. Repeatliver resections from colorectal metastasis. Repeat hepaticmetastases registry. Surgery 1995;117:296—304.
13] Riesener KP, Kasperk R, Winkeltau G, et al. Repeat resectionof recurrent hepatic metastases — improvement in prognosis?Eur J Surg 1996;162:709—15.
14] Tuttle TM, Curley SA, Roh MS. Repeat hepatic resection aseffective treatment for recurrent colorectal liver metastases.Ann Surg Oncol 1997;4:125—30.
15] Adam R, Bismuth H, Castaing D, et al. Repeat hepatectomy forcolorectal liver metastases. Ann Surg 1997;225:51—62.
16] Kin T, Nakajima Y, Kanehiro H, et al. Repeat hepatec-tomy for recurrent colorectal metastases. World J Surg1998;22:1087—91.
17] Yamamoto J, Kosuge T, Shimada K, et al. Repeat liver resec-tion for recurrent colorectal liver metastases. Am J Surg1999;178:275—81.
18] Suzuki S, Sakaguchi T, Yokoi Y, et al. Impact of repeat hep-atectomy on recurrent colorectal liver metastases. Surgery2001;129:421—8.
19] Muratore A, Polastri R, Bouzari H, et al. Repeat hepatectomyfor colorectal liver metastases: a worthwhile operation? J SurgOncol 2001;76:127—32.
20] Petrowsky H, Gonen M, Jarnagin W, et al. Second liver resec-tions are safe and effective treatment for recurrent hepaticmetastases from colorectal cancer. A biinstitutional analysis.Ann Surg 2002;235:863—71.
21] Takahashi S, Inoue K, Konishi M, et al. Prognostic factors forpoor survival after repeat hepatectomy in patients with col-
orectal liver metastases. Surgery 2003;133:627—34.22] Adam R, Pascal G, Azoulay D, et al. Liver resection forcolorectal metastases: the third hepatectomy. Ann Surg2003;238:871—83.
23] Zacharias T, Jaeck D, Oussoultzoglou E, et al. First and repeatresection of colorectal liver metastases in elderly patients. AnnSurg 2004;240:858—65.
24] Tanaka K, Shimada H, Ohta M, et al. Procedures of choicefor resection of primary and recurrent liver metastases fromcolorectal cancer. World J Surg 2004;28:482—7.
25] Hamy A, Bennouna J, Heymann MF, et al. Repeat hepatectomyfor colorectal liver metastases. Int Surg 2005;90:189—97.
26] Sugawara G, Isogai M, Kaneoka Y, et al. Repeat hepatec-tomy for recurrent colorectal metastases. Surg Today 2005;35:282—9.
27] Shaw IM, Rees M, Welsh FK, et al. Repeat hepatic resectionfor recurrent colorectal liver metastases is associated withfavourable long-term survival. Br J Surg 2006;93:457—64.
28] Ishiguro S, Akasu T, Fujimoto Y, et al. Second hepatectomy forrecurrent colorectal liver metastasis: analysis of preoperativeprognostic factors. Ann Surg Oncol 2006;13:1579—87.
29] Nishio H, Hamady ZZ, Malik HZ, et al. Outcome following repeatliver resection for colorectal liver metastases. Eur J Surg Oncol2007;33:729—34.
30] Aziz A, Steven L, Chen, Anton J, Bilchik. Role of repeated hep-atectomy in the multimodal treatment of hepatic colorectalmetastases. Arch Surg 2007;142:526—32.
[
[
[
[
[
[
P. Lopez et al.
31] Sa Cunha A, Laurent C, Rault A, et al. A second liver resec-tion due to recurrent colorectal liver metastases. Arch Surg2007;142:1144—9.
32] Thelen A, Jonas S, Benckert C, et al. Repeat liver resection forrecurrent liver metastases from colorectal cancer. Eur J SurgOncol 2007;33:324—8.
33] Treska V, Skalicky T, Liska V, et al. Repeated proce-dures for colorectal liver metastases. Hepatogastroenterology2007;54:1775—8.
34] Brachet D, Lermite E, Rouquette A, et al. Prognostic factorsof survival in repeat liver resection for recurrent colorectalmetastases: review of sixty-two cases treated at a single insti-tution. Dis Colon Rectum 2009;52:475—83.
35] de Jong MC, Mayo SC, Pulitano C, et al. Repeat cura-tive intent liver surgery is safe and effective for recurrentcolorectal liver metastasis: results from an internationalmulti-institutional analysis. J Gastrointest Surg 2009;13:2141—51.
36] Antoniou A, Lovegrove RE, Tilney HS, et al. Meta-analysis ofclinical outcome after first and second liver resection for col-orectal metastases. Surgery 2007;141:9—18.
37] Yan TD, Sim J, Black D, et al. Systematic review onsafety and efficacy of repeat hepatectomy for recurrentliver metastases from colorectal. Ann Surg Oncol 2007;14:2069—77.
38] Yamada H, Hiroyuki K, Kondo S, et al. Repeat hepatectomy forrecurrent hepatic metastases from colorectal cancer. Hepato-gastroenterology 2001;48:828—30.
39] Taschieri AM, Elli M, Vignati GA, et al. Repeated liver resectionfor recurrent metastases from colorectal cancer. Hepatogas-troenterology 2003;50:472—4.
40] Chu QD, Vezeridis MP, Avradopoulos KA, et al. Repeat hep-atic resection for recurrent colorectal cancer. World J Surg1997;21:292—6.
41] Pessaux P, Lermite E, Brehant O, et al. Repeat hepatec-tomy for recurrent colorectal liver metastases. J Surg Oncol2006;93:1—7.
42] Hurwitz H, Fehrenbacher L, Novotny W, et al. Bevacizumab plusirinotecan, fluorouracil, and leucovorin for metastatic colorec-tal cancer. N Engl J Med 2004;350:2335—42.
43] Cunningham D, Humblet Y, Siena S, et al. Cetuximabmonotherapy and cetuximab plus irinotecan in irinotecan-refractory metastatic colorectal cancer. N Engl J Med 2004;351:337—45.
44] Nakamura S, Sakaguchi S, Nishiyama R, et al. Aggressive repeat
liver resection for hepatic metastases of colorectal carcinoma.Surg Today 1992;22:260—4.45] Chiappa A, Zbar AP, Biella F, et al. Survival after repeathepatic resection for recurrent colorectal metastases. Hepato-gastroenterology 1999;46:1065—70.
46] Fong Y, Fortner JG, Sun R, et al. Clinical score for predictingrecurrence after hepatic resection for metastatic colorec-tal cancer: analysis of 1001 consecutive cases. Ann Surg1999;230:309—21.
47] Nordlinger B, Guiguet M, Vaillant JC, et al. Surgical resectionof colorectal carcinoma metastases to the liver. A prognos-tic scoring system to improve case selection, based on 1568patients. Association francaise de chirurgie. Cancer 1996;77:1254—62.
48] Tuech JJ, Pessaux P, Regenet N, et al. Detection of occult livermetastases in colorectal cancer by measurement of biliary car-cinoembryonic antigen concentration: a prospective study. JSurg Oncol 2004;88:27—31.
49] Oussoultzoglou E, Rosso E, Fuchshuber P, et al. Perioperativecarcinoembryonic antigen mesurements to predict curabilityafter liver resection for colorectal metastases: a prospectivestudy. Arch Surg 2008;143:1150—8.
50] Nordlinger B, Sorbye H, Glimelius B, et al. Perioperativechemotherapy with FOLFOX4 and surgery versus surgery alonefor resectable liver metastases from colorectal cancer (EORTCintergroup trial 40983): a randomised controlled trial. Lancet2008;371:1007—16.
[
[
[
[
Repeat hepatectomy
51] Elias D, Ouellet JF, Bellon N, et al. Extrahepatic disease doesnot contraindicate hepatectomy for colorectal liver metas-tases. Br J Surg 2003;90:567—74.
52] de Hass RJ, Wicherts DA, Adam R. Resection of colorectal livermetastases with extrahepatic disease. Dig Surg 2008;25:461—6.
53] Elias D, Liberale G, Vernerey D, et al. Hepatic and extrahepaticcolorectal metastases: when resectable, their localization doesnot matter, but their total number has a prognostic effect. AnnSurg Oncol 2005;12:900—9.
54] Torzilli G, Montorsi M, Donadon M, et al. Radical but con-servative is the main goal for ultrasonography-guided liverresection: prospective validation of this approach. J Am CollSurg 2005;201:517—28.
[
[
[
e103
55] Gold JS, Are C, Komprat P, et al. Increased use ofparenchymal-sparing surgery for bilateral liver metastasesfrom colorectal cancer is associated with improved mor-tality without change in oncologic outcome: trends intreatment over time in 440 patients. Ann Surg 2008;247:109—17.
56] Curley SA, Izzo F, Delrio P, et al. Radio frequency ablationof unresectable primary and metastatic hepatic malignancies:results in 123 patients. Ann Surg 1999;230:1—8.
57] Elias D, De Baere T, Smayra T, et al. Percutaneous radiofrequency thermo ablation as an alternative to surgery fortreatment of liver tumour recurrence after hepatectomy. BrJ Surg 2002;89:752—6.
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