Comparison of Blood Flow and Patency inArterial and Vein Grafts to Basilar ArteryBY C. J. WHANG, M.D., J. ROBERT MOZINGO, M.D.,

AND A. L. RHOTON, JR., M.D.

Abstract:Comparisonof BloodFlow andPatency inArterialand VeinGrafts toBasilarArtery

• Blood flow and patency rates obtained by lingual to basilar artery anastomosis were com-pared with those obtained by saphenous vein bypass graft from the carotid to the basilar arteryin two groups of ten dogs. Flow was measured by an electromagnetic technique while bloodpressure and blood gases were monitored. Graft patency also was determined by angiographyand histological examination. The arterial and venous grafts carried more than enough blood tomaintain a normal flow (9.5 ml per minute) through the basilar system of dogs.

Immediately after anastomosis, average flow through the vein grafts was 15.5 ml perminute (range 10 to 20 ml per minute) and through the arterial anastomosis 15.6 ml per minute(range 10 to 24 ml per minute). Six weeks later, average flow through the vein graft was 11.5 mlper minute and through the arterial graft 13 ml per minute. With induced hypertension, flow in-creased in the arterial grafts to an average of 26.2 ml per minute and in the vein grafts 24 ml perminute. Hypercarbia increased arterial graft flow to an average of 27.8 ml per minute and veingraft flow to 23.5 ml per minute.

By angiography, graft patency was shown in only 80% of the grafts at one week and in 60%at six weeks postoperatively, even though all grafts were patent by flow and histological deter-minations. This failure of angiography represents a limitation of the radiographical resolutionin millimeter-sized vessels.

Additional Key Wordsmicrovascular surgery

cerebral revascularizationvascular grafts

angiography

• The increased accuracy of suture placementprovided by microsurgical technique now permitsdirect surgical anastomosis of extracranial to in-tracranial arteries and the construction of bypass veingrafts from extracranial to intracranial arteries. Ex-amples of such procedures which have been done inman are superficial temporal artery to middle cerebralartery anastomosis and vein grafts between cervicalcommon carotid artery and supraclinoid internalcarotid artery.1"3 Cerebral revascularizationprocedures have been limited largely to the carotid cir-culation in man, although revascularization with thebasilar system has been tried in animals. Experimentalstudies have demonstrated that such anastomotic orbypass procedures involving small vessels remain pa-tent for a year or longer and that these anastomoses orbypass grafts provide an adequate blood flow throughthe new system.3- *

Although microsurgery has made bypassprocedures between intracranial and extracranialarteries feasible, few studies have been done toevaluate the physiological and clinical results of thesesurgical approaches to cerebral revascularization. The

From the Division of Neurological Surgery, University of FloridaHealth Center, Gainesville, Florida 32610.

Supported by the Veterans Administration Hospital,Gainesville, Florida, and the Heart Association of Broward County,Florida.

following reports quantitative measurements of bloodflow in a basal state and the effects of physiologicalvariables on flow, and compares flow and patencyrates obtained by two experimental methods aimed atre-establishing flow in the canine basilar artery.

MethodsProcedures evaluated are lingual artery to basilar arteryanastomosis and autogenous saphenous vein graft betweencommon carotid artery and basilar artery. All blood flowmeasurements were recorded with an electromagnetic bloodflow meter (Statham 2202).

GROUP 1: LINGUAL ARTERY-BASILAR ARTERY ANASTOMOSIS

Ten healthy mongrel dogs weighing 17 to 22 kg wereanesthetized with sodium pentothal (25 mg per kilogram in-travenously) and maintained with an endotracheallydelivered methoxyflurane/oxygen mixture. Ventilation wasadjusted to maintain normocarbia during the procedure.With the animal in the supine position, using sterile tech-nique, a 6 cm right paramedian incision was made at themandibular angle. After the carotid sheath was separatedfrom the midline structures, the hypoglossal nerve was iden-tified and a 5 to 6 cm segment of subjacent lingual artery wasmobilized just distal to its origin from the external carotidartery. Blood flow was measured in the intact lingual artery.All branches of the lingual artery were ligated and divided.The trachea and esophagus were retracted medially. Thepaired longus colli muscles were separated to expose theclivus (basioccipital bone) from the tympanic bullaesuperiorly to the condylar notches inferiorly. The

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pharyngeal cavity was not entered with this approach. Theremainder of the operative procedure was performed usingsurgical magnification of X16 and X25.

A 9 X 12 mm clival craniectomy was made with a 2 mmcutting and diamond dental drill. A temporary clip wasapplied at the origin of the lingual artery. The distal end ofthe lingual artery was sectioned and the lumen was irrigatedwith a heparin-saline solution. The dura was opened andreflected laterally. The basilar artery was thus exposed, freedfrom overlying arachnoid and permanently ligated with 7-0silk at the vertebrobasilar junction. A temporary ligaturewas applied approximately 5 to 6 mm distally. A 1 to 1.5mm elliptical arteriotomy was made in the ventral wall ofthe basilar artery between the ligatures. An end-to-sidelingual artery-basilar artery anastomosis requiring 12 to 16interrupted sutures of 10-0 nylon was done (fig. 1). The distaltemporary ligature was removed from the basilar artery andretrograde filling of the graft initially confirmed anastomoticpatency. The clip from the proximal lingual artery wasremoved. Blood flow through the lingual-basilar arterialanastomosis was recorded at normocarbia. The wound wasclosed in layers. Antibiotics were given for the next sevendays.

GROUP 2i CAROTID-BA3ILAR SAPHINOUS VIIN BYPASS

In this group often healthy mongrel dogs weighing between17 and 23 kg, the anesthesia and operative approach to thebasilar artery were identical to that of Group 1. A 6 to 7 cmsegment of autogenous medial saphenous vein, with a 0.8 to1.5 mm external diameter, was dissected from the hindlimb.Side branches were ligated with 6-0 silk or surgical clips. A1.27 mm (external diameter) silastic tube was passedthrough the lumen of the vein, and the cannulized vein wasplaced in a heparin-saline solution. The carotid artery wasdissected free at the bifurcation. A segment of basilar arterywas isolated between two ligatures as in Group 1. A smallarteriotomy was made in the basilar artery and the proximalend of the vein was anastomosed to the basilar artery in anend-to-side fashion with 12 to 16 interrupted sutures of 10-0nylon.

A segment of the previously isolated common carotidartery at the bifurcation was then temporarily occluded

GRAFT

BRAIN STEM

CLIVUS

BASILAR A.

DURA

FIOUI11

between two Heifetz clips (Week) and a small arteriotomywas made. The lumen of the carotid artery was irrigatedwith heparin-saline solution. The distal end of the vein graftwas anastomosed to the carotid artery in an end-to-sidefashion with 10 to 14 sutures of 10-0 nylon. The temporaryligature in the basilar artery distal to the anastomosis wasremoved to initially confirm anastomotic patency. The twotemporary clips on the carotid artery were then removed.After completion of the anastomosis, blood flow in the veingraft was measured at normocarbia.

Follow-UpAll animals underwent common carotid angiography usingConray-60 to evaluate angiographical evidence of graftpatency at one (fig. 2) and six (figs. 3 and 4) weekspostoperatively. After the second angiographical evaluation,the wound was reopened for blood flow measurements.Blood flow response to hypercarbia and hypertension wasassessed. Pao, was altered by changing ventilatory rate andhypertension induced by intravenous Ephedrine (2.5 mg).Blood pressure was monitored and recorded on a polygraphwith a catheter placed in the abdominal aorta through theleft femoral artery and connected to a Statham pressuretransducer (PnDc). All animals were then killed by a saline-formalin perfusion technique for histological examination ofthe brain and graft.

ResultsNEUROLOGICAL DEFICITS

Neurological evaluation was assessed preoperatively

Surgical magnification view (X 16 setting) of completed lingualartery-basilar artery anastomosis. Basilar artery is permanentlyligated at vertebrobasilar junction. Anastomosis performed with in-terrupted 10-0 nylon sutures.

HOUII3

Right carotid angiogram representative of lingual artery (tj tobasilar artery (~) grafts patent angiographically at one weekpostoperatively.

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BLOOD FLOW AND PATENCY IN BASILAR ARTERY GRAFTS

and during each postoperative day. No permanentneurological deficits occurred in any animal operatedupon. Transient hindlimb paraparesis and tendency tocircle to the left were noted in three animals. Thesetransient neurological deficits cleared within threedays postoperatively. No CSF fistulas or infectionsoccurred.

BLOOD FLOW IN GROUP 1

At normocarbia, average blood flow in the intactlingual artery prior to anastomosis was 16.5 ml perminute with a range of 11 to 21 ml per minute.Immediately after completion of the lingual-basilaranastomosis, average lingual arterial graft blood flowwas 15.6 ml per minute with a range of 10 to 24 ml perminute.

Six weeks postoperatively at normocarbia,average blood flow through the lingual arterial graftswas 13 ml per minute with a range of 10 to 16 ml perminute. With hypercarbia (Paco2 62 to 78) averageblood flow through the arterial graft was 27.8 ml perminute with a range of 17 to 54 ml per minute; and,with Ephedrine-induced hypertension (180 to 200 mmHg, from a baseline of 110 to 120 mm Hg), mean

TABU 1

Graft Blood Flow (Milliliters per Minute) ImmediatelyFollowing Anastomosis and Six Weeks Later

ArterialNormocarbiaHypercarbiaHypertension

VeinNormocarbiaHypercarbiaHypertension

Immtdott

15.6

15.5

Six w»ki

13.027.826.2

11.523.524.0

systemic arterial pressure was 26.2 ml per minute witha range of 18 to 36 ml per minute (table 1).

BLOOD FLOW IN GROUP 2

At normocarbia, average blood flow in the carotid-basilar vein bypass grafts was 15.5 ml per minute witha range of 10 to 20 ml per minute. Six weekspostoperatively at normocarbia, average blood flowwas 11.5 ml per minute with a range of 10 to 13 ml perminute. With hypercarbia (Paco2 72 to 76), blood flowaveraged 23.5 ml per minute with a range of 18 to 28ml per minute, and with induced hypertension was 24ml per minute with a range of 22 to 26 ml per minute(table 1).

FICHU! 4

FIOU1I3

Right carotid angiogram representative of lingual artery (\) tobasilar artery [-) grafts patent at six weeks postoperatively.

Right carotid angiogram representative of saphenous vein (tj bypassgrafts between common carotid and basilar (-) arteries patent at sixweeks postoperatively.

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ANGIOGRAPHICAl PATENCY

Carotid angiography was done on all animals inGroup 1 and seven animals in Group 2 at one weekpostoperatively. Patency in Group 1 and Group 2 was90% and 70%, respectively. Carotid angiography wasrepeated on nine animals in Group 1 and six animalsin Group 2 at six weeks postoperatively. Patency inGroup 1 and Group 2 was 70% and 50%, respectively,at six weeks.

PATENCY BY ELECTROMAGNETIC FLOW TECHNIQUE

Blood flow in the arterial and vein grafts wasmeasured in all animals in Groups 1 and 2 im-mediately after completion of the anastomosis. Allgrafts were found to be patent. At six weekspostoperatively, blood flow was measured in nine often animals in Group 1 and six of ten animals inGroup 2. All of these grafts were found patent byblood flow measurement.COMPLICATION

One animal of Group 1 had a neck hematoma due torupture of a branch of the lingual artery after the firstangiogram, and was excluded from further study.Four animals of Group 2 were killed 4 to 10 days post-operatively due to hemorrhage from a branch of thevein graft related to migration of a hemoclip.

DiscussionUsing an electromagnetic blood flow meter we havemeasured blood flow quantitatively through arterialand venous grafts between carotid and basilar arteriesin the dog. We have been unable to find in theliterature documented blood flow measurementsthrough the lingual artery in dogs. Our measurementof the average blood flow through the intact lingualartery was 16.5 ml per minute. Average normal bloodflow of the basilar artery in dogs has been recorded as9.5 ml per minute.5

These arterial and venous grafts carried morethan enough blood to maintain a normal flow ratethrough the basilar system of the dogs. Continuous

gradual increase of blood flow through the graft wassignificant with a range of 17 ml per minute to 54 mlper minute in the lingual-basilar arterial anastomoses,and 18 ml per minute to 28 ml per minute in thecarotid-basilar bypass vein grafts with hypercarbia.An increase in mean blood flow through the graftswith hypertension also was significant with a range of18 to 36 ml per minute in the lingual-basilaranastomoses and 22 to 26 ml per minute in the veinbypass grafts. A greater increase in blood flow withhypercarbia and hypertension was found in thearterial grafts than in the venous grafts.

The grafts in all surviving animals were patent byblood flow measurements and by histological ex-amination at six weeks postoperatively, even thoughpatency could not be determined consistently byangiography. This discrepancy of patency ratebetween angiography and flow meter techniquereflects a limitation of the radiographical resolution inthese small arteries. Khodadad4 found angio-graphically that the patency rate was greater in arte-rial grafts compared to vein grafts, both acutely andlong-term. Our study agrees with his angiographicalfindings. At six weeks postoperatively, all grafts werepatent by blood flow measurements, whereasangiography disclosed a patency rate of only 70%.

References1. Lougheed WM, Marshall BM, Hunter M, et al: Common

carotid to intracranial internal carotid bypass venous graft. JNeurosurg 34:114-118, 1971

2. Yasargil MG, Krayenbuhl HA, Jacobson JH: Micro-neurosurgical arterial reconstruction. Surgery 67:221-233,1970

3. Reichman OH: Continued patency of canine lingual-basilarsystem. Stroke 3:586-591, 1972

4. Khodadad K: Sublingual and lingual-basilar arteryanastomoses and carotid-basilar bypass grafts. Surg Neurol1:175-177, 1973

5. Fukuyama GS, Himwich WA: Canine basilar arterial flow andeffects of common carotid occlusion. Amer J Physiol219:525-527, 1970

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Print ISSN: 0039-2499. Online ISSN: 1524-4628 Copyright © 1975 American Heart Association, Inc. All rights reserved.

is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231Stroke doi: 10.1161/01.STR.6.4.445

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