J Neurosurg 72:35-41, 1990
Saphenous vein graft bypass of the cavernous internal carotid artery LALIGAM N . SEKHAR, M.D., CHANDRA N. SEN, M.D., AND HAE DONG JHO, M . D .
Department of Neurological Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania ~" Saphenous vein graft reconstruction was performed from the petrous to the supraclinoid internal carotid artery (ICA) to replace the cavernous ICA in six patients during direct intracavernous operations. Four of these patients had intracavernous neoplasms with invasion of the ICA and two had intracavernous ICA aneurysms that could not be clipped or occluded with intraluminal balloons. All but one patient had evidence of poor collateral flow reserve in a balloon occlusion test of the ICA. The superficial temporal artery was not present in four patients, was minuscule in one, and was damaged during the initial dissection in another, making it unsuitable for superficial temporal-to-middle cerebral artery branch anastomosis. Blood flow within the graft could not be established intraoperatively in one patient (who had excellent collateral circulation) due to the small size of the vein (3 mm). In all others, the grafts were patent on followup arteriography and transcranial Doppler studies. Three patients who had severe reduction of cerebral blood flow during test occlusion of the ICA exhibited temporary hemispheric neurological deficits postoperatively; the deficits were related to the duration of temporary ICA occlusion. All three recovered completely without evidence of infarction on computerized tomography (CT). One patient who clinically could not tolerate the balloon occlusion test of the ICA also had temporary neurological deficits with good recovery but showed evidence of border-zone infarction on CT scans. The present role of saphenous vein graft bypass of the cavernous ICA is discussed. KEY WORDS graft bypass
"
cavernous carotid artery
D
URING direct surgical treatment of neoplastic and vascular lesions involving the cavernous sinus, the surgeon sometimes is faced with the inability to preserve the internal carotid artery (ICA). In such instances, collateral circulation may be adequate to permit occlusion of the ICA without consequence. In some patients, however, some form of revascularization will be necessary, either because of the inadequacy of the collateral circulation or because of the desire to preserve the ipsilateral cerebrovascular flow in a young patient with a long life expectancy. In the past, revascularization has been accomplished by a superficial temporal artery (STA)-io-middle cerebral artery (MCA) branch anastomosis, an external carotid artery-MCA long venous graft, an STA-MCA branch venous graft, or an extracranial ICA-intracranial ICA long v e n o u s graft. 2'4-6'8-I1,18-20In this article, the use of a short venous graft from the petrous to the supraclinoid ICA, directly bypassing the cavernous ICA, is described as an alternative means of revascularization. The feasibility of such grafting (in cadavers) was first described by Sekhar, et al. 14 Since then, the procedure has been
J. Neurosurg. / Volume 72/January, 1990
9 internal carotid artery
9 saphenous vein
9
used clinically by our group and also by Fukushima (T Fukushima: personal communication, 1988). Clinical Material and M e t h o d s
Patient Population From 1983 to 1988, the first author has been involved in the direct surgical treatment o f the petrous or cavernous ICA in 170 patients with neoplastic or vascular lesions. Vein grafting from the cervical to the petrous ICA or graft reconstruction of the petrous ICA was used in seven of these patients.15 In six patients, vein grafting was performed from the petrous to the supraclinoid ICA, bypassing the cavernous sinus. The latter group is the subject of this report. Direct vein graft bypass o f the intracavernous ICA was used in four patients with neoplasms (three meningiomas and one squamous-cell carcinoma) and in two patients with intracavernous aneurysms (one congenital and the other presumably iatrogenic) (Table 1). All patients were evaluated preoperatively by physical and neurological examination, computerized tomog35
L. N. Sekhar, C. N. Sen, and H. D. Jho TABLE 1
Summary of six patients with graft bypass of the cavernous ICA*
Case No.
Age (yrs), Sex
Pathology & Location
Result of BTO
Type of Anastomosis SupraPetrous clinoid 1CA ICA
Patency
AnastoICA New mosis Occlusion Postoperative Time Time Deficits
64, F meningioma: cavernous sinus, clivus, sella
tolerated clinically; bifrontal CBF decrease
end-to- end-to- patent: angio end side 3 mos, TCD 14 mos
1 89hrs 5 hrs (proximal end redone)
48, F meningioma: cavernous sinus, clivus, sella
tolerated clinically; marked CBF reduction
end-to- end-to- patent: angio end side 3 mos, TCD 3 mos
17I hrs
3
44, F meningioma: cavernous sinus, clivus, sella
not done; good collaterals on angio
end-to- end-to- occluded 2 hrs at surgery end side
4
48, M squamouscell ca: cavernous sinus, ethmoid, maxilia, orbit 68, F intracavernous giant aneurysm
tolerated clinically; CBF reduction
end-to- end-to- patent: angio end end 2 mos, TCD 2
tolerated clinically; marked CBF reduction
end-to- end-to- patent: angio end side 3 days, TCD 2
38, F iatrogenic aneurysm
failed clinically; end-to- end-totemporary hemi- end side plegia, aphasia, seizures
5
171 hrs
permanent occlusion
temporary hemiparesis & abulia; worsened III function; delayed VII palsy temporary hemiparesis; memory problems; VI palsy; delayed VII paresis III, V paresis; IV, VI palsies; diabetes insipidus
Follow-Up Findings
Postop CT Scan at 2 mos
14 mos: normal mentation; partial III palsy; VII palsy recovered 7 mos: normal mentation, motor exam, & VII function; VI palsy
no cerebral infarction; residual clival tumor (gamma knife)
8 mos: III, IV paresis; VI palsy; diabetes insipidus improved 3 mos: died of metastatic disease
no cerebral infarction; no tumor
no new cerebral infarction; residual clival tumor (gamma knife)
12I hrs
2 hrs
none
1~ hrs
3 89hrs
temporary hemiparesis; III palsy
2 mos: III no cerebral palsy; 3 mos: infarction; died suddenlyt aneurysm thrombosed
2 hrs
2 hrs
temporary hemiparesis; dysphasia; memory loss; III palsy
7 mos: norborder-zone mal speech & infarction mentation, mild III paresis
no cerebral infarction; recurrent tumor
mos
mos
6
patent: angio 7 mos, TCD 6 mos
* ICA = internal carotid artery; BTO = balloon test occlusion; CBF --- cerebral blood flow; TCD = transcranial Doppler ultrasound; CT = computerized tomography; angio = angiogram; ca = carcinoma. Roman numerals denote cranial nerves. t Autopsy revealed myocardial infarction, a patent vein graft, and no cerebral infarction.
r a p h y ( C T ) , a n d m a g n e t i c r e s o n a n c e i m a g i n g . In a d d i t i o n , all p a t i e n t s h a d c e r e b r a l a n g i o g r a p h y a n d five u n d e r w e n t a b a l l o o n o c c l u s i o n test o f t h e I C A . I n t h e b a l l o o n o c c l u s i o n test, t h e ipsilateral I C A w a s o c c l u d e d for 15 m i n u t e s i f n e u r o l o g i c a l l y t o l e r a t e d . T h i s was followed by a xenon-CT examination of cerebral blood flow (CBF) with and without temporary ICA occlusion. I n o n e p a t i e n t ( C a s e 3), a b a l l o o n o c c l u s i o n test was not performed because the patient could not tolerate a l e n g t h y a n g i o g r a p h i c p r o c e d u r e a n d b e c a u s e angiogr a p h y d e m o n s t r a t e d a p p a r e n t l y e x c e l l e n t c o l l a t e r a l circulation.
Operative Technique T h e c e r v i c a l I C A w a s e x p o s e d in all patients. A f r o n t o t e m p o r a l c r a n i o t o m y w a s f o l l o w e d b y the t e m porary removal of the superior and lateral rims and 36
walls o f t h e o r b i t a n d t h e z y g o m a t i c arch, i n c l u d i n g t h e m a n d i b u l a r fossa. E x t r a d u r a l m i d d l e fossa d i s s e c t i o n was p e r f o r m e d t o e x p o s e a n d u n r o o f t h e m a n d i b u l a r nerve, t h e m i d d l e m e n i n g e a l artery ( w h i c h w a s d i v i d e d ) , t h e g r e a t e r s u p e r f i c i a l p e t r o s a l n e r v e ( w h i c h w a s divided), a n d t h e h o r i z o n t a l s e g m e n t o f t h e p e t r o u s I C A . In all p a t i e n t s , it w a s n e c e s s a r y to r e m o v e t h e b o n e portion of the eustachian tube and expose the genu of the p e t r o u s I C A t o facilitate suturing. F o l l o w i n g d u r a l o p e n i n g a n d initial d i s s e c t i o n , t h e anterior clinoid process was removed, and the optic n e r v e w a s u n r o o f e d b y b o n e r e m o v a l . T h e distal i n t r a c a v e r n o u s I C A w a s d i s s e c t e d after t h e d i v i s i o n o f t h e d u r a l rings at its e x i t f r o m t h e c a v e r n o u s sinus. T h e c a v e r n o u s s i n u s w a s e n t e r e d by s u p e r i o r a n d l a t e r a l i n t r a d u r a l a p p r o a c h e s in t h e p a t i e n t s w i t h b e n i g n tum o r s to d e t e r m i n e i f t h e I C A c o u l d b e d i s s e c t e d free o f
J. Neurosurg. / Volume 72/January, 1990
Graft bypass of cavernous internal carotid artery
FIG. 1. Drawings depicting the saphenous vein graft bypass of the cavernous internal carotid artery (ICA) using an end-to-side anastomosis distally (left) or end-to-end anastomosis distally (right). Although the collateral circulation of the ophthalmic artery usually enables its occlusion without loss of vision, occlusion is best avoided when vision is intact preoperatively. Roman numerals denote cranial nerves.
t u m o r and in the patients with aneurysms to see if the aneurysm could be clipped. However, in the patient with a malignant neoplasm, the contents of the cavernous sinus were excised without entering the sinus. When direct vein grafting was decided upon, the patient was given 1000 mg of methylprednisolone intravenously, 12 and approximately a 7-cm length of the greater saphenous vein was harvested from the thigh. The distal anastomosis was usually completed first. Three temporary vascular clips were placed on the ICA: one in the neck, one distal to the ophthalmic artery, and one just proximal to the posterior communicating artery. For end (vein)-to-side (ICA) anastomosis, a linear arteriotomy was made on the anterior wall of the ICA (Fig. 1 left). Heparinized saline was used to wash the blood and any clot from the ICA and vein, but systemic heparinization was not employed for fear of causing bleeding from the operative wound. For endto-end anastomosis, the ICA was divided just superior to the ophthalmic artery and "fish-mouthed" (Fig. 1 right). The end of the vein was trimmed, denuded of adventitia, and fish-mouthed if necessary. Four 7-0 Prolene or 8-0 nylon sutures were placed to attach the vein to the ICA at diametrically opposite points. The rest of the anastomosis was completed with interrupted sutures. To check the anastomosis for leaks, the vein was irrigated with heparinized saline. A continuous suture technique was used in the first patient and subsequently abandoned in favor of an interrupted suturing technique. The latter took m o r e time but provided better approximation without leakage or stenosis at the suture line. Next, the petrous ICA was divided just proximal to the third division of the trigeminal nerve. There was
J. Neurosurg. / Volume 72/January, 1990
usually some back bleeding from the intracavernous ICA because of the anastomotic connections of the intracavernous branches. This bleeding was stopped by packing the lumen of the cavernous ICA with Surgicel (oxidized regenerated cellulose). The petrous ICA was then irrigated thoroughly with heparinized saline to clear blood or clot. The vein graft was t r i m m e d to a length of 5 to 6 cm and anastomosed end-to-end with 7-0 Prolene interrupted sutures. Before the last stitch was tied, the graft and the ICA were irrigated again with heparinized saline, and the proximal and distal temporary clips were released long enough to wash out any air bubbles. The intracavernous ICA was ligated permanently just proximal to the ophthalmic artery and divided proximal to the ligature. During the petrous anastomosis procedure, a temporary clip can be placed on the cavernous ICA proximal to the ophthalmic artery and on the vein graft. The two distal t e m p o r a r y clips can be removed to continue collateral flow through the ophthalmic artery (as was done in Case 6, see below). A regimen of intermittent subcutaneous heparin was used in the early postoperative period, and antiplatelet agents (aspirin or dipyridamole) were administered orally after 10 days to prevent late graft occlusions. 3'21 If the patient's eustachian tube was excised, a tympanostomy was inserted after 6 weeks.
S u m m a r y o f Cases In four patients the STA was absent as a result of prior surgery, in one it was minuscule, and in another it was injured during the operation. The time required to perform anastomosis of the graft ranged f r o m 60 to 90 minutes; however, in Case 1 the ICA was occluded
37
L. N. Sekhar, C. N. Sen, and H. D. Jho
FIG. 2. Case 2. Left: Preoperative angiogram showing encasement and narrowing of the intracavernous internal carotid artery and an irregularly narrowed posterior communicating artery, which is the dominant supplier to the posterior cerebral circulation. Right: Postoperative carotid angiogram showing patency of the venous graft. Some catheter-induced spasm of the upper cervical internal carotid artery is apparent.
for 5 hours because of thrombosis at the proximal anastomotic end of the graft, which was discovered after t u m o r resection. The anastomosis was reconstructed with a good result. 16 In Case 3 the graft was occluded intraoperatively, probably due to the very small size of the vein (diameter 3 mm). This patient had a good preoperative collateral circulation through the anterior and posterior c o m m u n i c a t i n g arteries and did not suffer any hemispheric neurological deficits postoperatively. One patient (Case 4), who had a large squamous-cell carcinoma, recovered well from the operation but died 3 months later of metastatic disease. In Case 5 a giant intracavernous aneurysm could not be clipped upon direct exploration, because it was an eccentric dilatation of the ICA. Graft replacement of the ICA took 2 hours to perform; however, the ICA was temporarily occluded for 3 89hours, because preparations for grafting had not been made. The patient recovered well from the procedure but died suddenly at home 3 months later. Autopsy revealed the cause o f death to be myocardial infarction. The graft was patent, and no cerebral infarction was found. Cases 2 and 6 are described below. Four patients tolerated balloon occlusion test of the ICA without neurological deficit but exhibited significant ipsilateral or bilateral reductions o f CBF ranging from 15 to 30 cc/100 g m / m i n . Three of these patients had temporary hemispheric deficits postoperatively, presumably related to intraoperative ICA occlusion for 2, 3 89and 5 hours. Another patient developed temporary hemiplegia, aphasia, and seizures during test occlu38
sion of the ICA. This patient manifested hemispheric neurological deficits postoperatively, related to temporary intraoperative ICA occlusion. She made a good recovery, but CT revealed evidence of cerebral infarction. Postoperative angiography demonstrated patent saphenous vein grafts in all five of these patients.
Illustrative Case Reports Case 2 This 48-year-old w o m a n with an extensive basal meningioma had undergone two prior t u m o r operations. The intracavernous ICA was encased and narrowed by the t u m o r (Fig. 2 left). The posterior communicating artery was the dominant supplier of the posterior cerebral artery territory and w a s irregularly narrowed by the tumor. The CBF decreased bilaterally during balloon occlusion test of the ICA, especially at the upper levels. At surgery, the t u m o r was excised along with the poorly functioning third through sixth cranial nerves. The ICA was replaced with a vein graft. Postoperatively, the patient had a mild hemiparesis for 2 days. Follow-up arteriography revealed a patent vein graft (Fig. 2 right). Seven months after the operation, the patient had a Karnofsky score of 80. A small t u m o r remnant in the clival area was treated with g a m m a knife radiotherapy. Case 6 This 38-year-old w o m a n presented with several severe episodes of epistaxis. She had an aneurysm arising J. Neurosurg. / Volume 72/January, 1990
Graft bypass of cavernous internal carotid artery
FIG. 3. Case 6. Left: Left internal carotid arteriogram revealing an aneurysm arising from the internal carotid artery and projecting into the sphenoid sinus. Right: Postoperative arteriogram showing a healthy vein graft.
from the intracavernous ICA and projecting medially into the sphenoid sinus (Fig. 3 left). This was presumed to have resulted from two prior transsphenoidal operations and one transethmoidal pituitary procedure for Cushing's disease. Arteriography showed the STA to be absent, but cross flow through the anterior communicating artery was present after ipsilateral c o m m o n carotid artery compression. Permanent balloon occlusion of the ICA was planned. However, the patient developed hemiplegia, aphasia, and seizures after test occlusion of the ICA and recovered slowly. An urgent operation was performed with electroencephalographic (EEG) monitoring. The intracavernous aneurysm was explored directly but not clipped because the cavernous sinus was found to be filled with granulation tissue. It was elected to perform vein graft bypass of the cavernous ICA. During the 2-hour temporary ICA occlusion for vein grafting, the blood pressure was elevated 40 torr, and no EEG changes were observed. However, postoperatively the patient suffered hemiplegia (which resolved in 5 days), dysphasia (which resolved in 14 days), and memory problems (which resolved slowly). Angiography revealed a patent graft (Fig. 3 right). Results of a CBF study on the 1st postoperative day were normal, but another study 1 week later revealed hyperemic areas in the border zone between the anterior, middle, and posterior cerebral arteries. These regions evolved into CT-defined infarcts. Seven months later, the patient had made a nearly complete recovery of her neurological deficits and had a Karnofsky score of 80. Discussion
Technical Factors The advantages and disadvantages of using vein grafts as arterial conduits, important technical points
J. Neurosurg. / Volume 72/January, 1990
regarding graft harvesting and anastomosis, and postoperative management were reviewed extensively by Sundt and Sundt. 21 When vein grafting is used to reconstruct the ICA, the shortest possible length of the graft and end-to-end anastomosis at both ends o f the graft are preferable to reduce turbulent flow. However, because of the position of the ophthalmic artery, an end-to-side anastomosis is technically easier to carry out at the distal end. An end-to-end distal anastomosis can be performed if the ophthalmic artery is sacrificed (because of orbital exenteration) or if there is an adequate length of healthy intracavernous ICA proximal to the ophthalmic artery. It proved easier to perform the distal anastomosis first. When the proximal anastomosis was undertaken first, blood ran down from the skull-base area along the graft and made the distal anastomosis more difficult. In Case 3 the proximal anastomosis was achieved first and the temporary clip was opened to check graft flow, because the vein was small. This resulted in clotting of the graft, because systemic heparinization was not used and the volume of flow was small. In this series, intraluminal shunts were not utilized because of technical difficulties and for fear of embolic complications.
Postoperative Neurological Deficits In three of the four patients who had a reduced CBF (but no neurological deficits) after balloon occlusion test of the ICA, temporary neurological deficits were observed postoperatively, corresponding to the areas of CBF reduction. In the patient with the poorest preoperative collateral circulation, hyperemia and subsequent infarction were demonstrated in the border-zone areas between vascular territories. No embolic occlusions of distal vessels were seen on postoperative arteriography.
39
L. N. Sekhar, C. N. Sen, and H. D. Jho TABLE 2 Revascularization alternatives after cavernous ICA occlusion*
Passed Preop BTO; CBF > 35 cc/100 gm/min no reconstruction
STA-MCA bypass plus direct venous graft
Passed Preop BTO; CBF 15-35 cc/100 gm/min STA-MCA bypass
long saphenous vein graft ECA-MCA
direct venous graft with brain protection
Failed Preop BTO or or
or
or
O?"
direct venous graft
long saphenous vein graft ECA-MCA direct venous graft with brain protection * Alternatives based on preoperative balloon test occlusion (BTO) results. ICA = internal carotid artery; CBF = cerebral blood flow; STA = superficial temporal artery; MCA = middle cerebral artery; ECA = external carotid artery. Brain protection: intraoperative high-dose barbiturate or etomidate therapy to achieve burst suppression on electroencephalogram.
These facts reinforce t h e b e l i e f t h a t the t e m p o r a l neurological deficits were c a u s e d b y i n t r a o p e r a t i v e flow r e d u c t i o n d u e to I C A o c c l u s i o n a n d n o t by e m b o l i from the a n a s t o m o t i c site. In this g r o u p o f patients, h y p e r t e n s i o n was i n d u c e d d u r i n g t e m p o r a r y I C A occlusion, b u t drugs to protect the b r a i n against i s c h e m i a , such as high-dose barbiturates, e t o m i d a t e , o r t h e " S e n d a l cocktail," were not u s e d . IA7'22 S u b s e q u e n t l y t r e a t e d p a t i e n t s who have und e r g o n e p r o l o n g e d t e m p o r a r y I C A occlusion have been given i n t r a o p e r a t i v e t h i o p e n t a l s o d i u m intravenously to achieve b u r s t s u p p r e s s i o n o n E E G recordings, with better results. Direct Vein Graft Reconstruction
of Cavernous ICA
W h e n the i n t r a c a v e r n o u s I C A m u s t be excised in a p a t i e n t w h o has a l o n g life e x p e c t a n c y , it is preferable to revascularize the b r a i n , even w h e n the preoperative collateral c i r c u l a t i o n is a d e q u a t e . T h e reasons for this are the following: 1) t h e ipsilateral cerebrovascular reserve is preserved b y r e v a s c u l a r i z a t i o n ; 2) m a n y intrac a v e r n o u s lesions, especially m e n i n g i o m a s a n d aneurysms, t e n d to i n v o l v e b o t h sides; a n d 3) there appears to be a n i n c r e a s e d risk o f a n e u r y s m f o r m a t i o n after u n i l a t e r a l I C A occlusion. 7 M a n y m e t h o d s o f c e r e b r a l revascularization are available to the surgeon. D i r e c t v e n o u s reconstruction o f the c a v e r n o u s I C A has the a d v a n t a g e o f providing a high-flow c o n d u i t i m m e d i a t e l y w i t h the shortest possible length o f vein, l e a d i n g f r o m a large artery to a n o t h e r large artery. T h e d i s a d v a n t a g e s are a 90- to 120-minute p e r i o d o f t e m p o r a r y I C A o c c l u s i o n a n d the potential for graft occlusion. T h e l o n g - t e r m status o f these grafts in t e r m s o f p a t e n c y a n d o t h e r p a t h o l o g i c a l changes such as a n e u r y s m f o r m a t i o n at b r a n c h sites is u n k n o w n at present. R e v a s c u l a r i z a t i o n t e c h n i q u e s using the STA still carry the lowest risk to t h e p a t i e n t a n d m u s t be used w h e n e v e r possible. 4,6,8 H o w e v e r , t h e S T A - M C A bypass alone m a y be i n a d e q u a t e to p r e v e n t a stroke after acute I C A o c c l u s i o n in p a t i e n t s with a very p o o r preoperative collateral circulation. 13 Possible alternatives for revascularization, d e p e n d i n g o n the status o f the preoperative collateral circulation, a r e o u t l i n e d in T a b l e 2. 40
Acknowledgments
Dr. Howard Yonas critiqued the manuscript, and the cerebral blood flow studies were performed under his supervision. Dr. Carl Snyderman participated in some of the surgical procedures. Judy Campbell prepared the manuscript, and Helene Marion edited it. References
1. Batjer HH, Frankfurt AI, Purdy PD, et al: Use of etomidate, temporary arterial occlusion, and intraoperative angiography in surgical treatment of large and giant cerebral aneurysms. J Neurosurg 68:232-240, 1988 2. Brown WE Jr, Ansell LV, Story JL: Technique of saphenous vein bypass from the common carotid artery to the middle cerebral artery, in Erickson DL (ed): Revascularization of the Ischemic Brain. New York: Futura Press, 1988, pp 167-199 3. Chesebro JH, Clements IP, Fuster V, et al: A plateletinhibitor drug trial in coronary-artery bypass operations. Benefit of perioperative dipyridamole and aspirin therapy on early postoperative vein-graft patency. N Engl J Med 307:73-78, 1982 4. Collice M, Arena O, Fontana RA: Superficial temporal artery to proximal middle cerebral artery anastomosis: clinical and angiographic long term results. Neurosurgery 19:992-997, 1986 5. Diaz FG, Pearce J, Ausman JI: Complications of cerebral revascularization with autogenous vein grafts. Nenrosurgery 17:271-276, 1985 6. Diaz FG, Umansky F, Mehta B, et al: Cerebral revascularization to a main limb of the middle cerebral artery in the Sylvian fissure. An alternative approach to conventional anastomosis. J Nearosurg 63:21-29, 1985 7. Dyste GW, Beck DW: D e novo aneurysm formation following carotid ligation: case report and review of literature. Neurosurgery 24:88-92, 1989 8. Jack CR Jr, Sundt TM Jr, Fode NC, et al: Superficial temporal-middle cerebral artery bypass: clinical pre- and postoperative angiographic correlation. J Neurosurg 69: 46-51, 1988 9. Little JR, Furlan AJ, Bryerton B: Short vein grafts for cerebral revascularization. J Neurosurg 59:384-388, 1983 10. Lougheed WM, Marshall BM, Hunter M, et al: Common carotid to intracranial internal carotid bypass venous graft. Technical note. J Neurosurg 34:114-118, 1971 11. Morimoto T, Sakaki T, Kakizaki T, et al: Radial artery graft for an extracranial-intracranial bypass in cases of J. Neurosurg. / V o l u m e 7 2 / J a n u a r y , 1990
Graft bypass of cavernous internal carotid artery
12. 13.
14.
15.
16. 17.
internal carotid aneurysms. Report of two cases. Surg Neurol 30:293-297, 1988 Pearce JE, Dujovny M, Ho KL, et al: Acute inflammation and endothelial injury in vein grafts. Neurosurgery 17: 626-634, 1985 Samson DS, Neuwelt EA, Beyer CW, et al: Failure of extracranial-intracranial arterial bypass in acute middle cerebral artery occlusion: case report. Neurosurgery 6: 185-188, 1980 Sekhar LN, Burgess J, Akin O: Anatomical study of the cavernous sinus emphasizing operative approaches and related vascular and neural reconstruction. Neurosurgery 21:806-816, 1987 Sekhar LN, Schramm VL Jr, Jones NF, et al: Operative exposure and management of the petrous and upper cervical internal carotid artery. Neurosurgery 19: 967-982, 1986 Sekhar LN, Sen CN, Jho HD, et al: Surgical treatment of intracavernous neoplasms: a four-year experience. New rosurgery 24:18-30, 1989 Spetzler RF, Hadley MN, Rigamonti D, et al: Aneurysms of the basilar artery treated with circulatory arrest, hypo-
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18. 19.
20. 21. 22.
thermia, and barbiturate cerebral protection. J Neurosurg 68:868-879, 1988 Spetzler RF, Rhodes RS, Roski RA, et al: Subclavian to middle cerebral artery saphenous vein bypass graft. J Neurosurg 53:465-469, 1980 Sundt TM Jr, Piepgras DG, Houser OW, et al: Interposition saphenous vein grafts for advanced occlusive disease and large aneurysms in the posterior circulation. J Neurosurg 56:205-215, 1982 Sundt TM Jr, Piepgras DG, Marsh WR, et al: Saphenous vein bypass grafts for giant aneurysms and intracranial occlusive disease. J Neurosurg 65:439-450, 1986 Sundt TM III, Sundt TM Jr: Principles of preparation of vein bypass grafts to maximize patency. J Neurosurg 66: 172-180, 1987 Suzuki J (ed): Advances in Surgery for Cerebral Stroke. Tokyo: Springer-Verlag, 1988, pp 3-12
Manuscript received December 16, 1988. Address reprint requests to: Laligam N. Sekhar, M.D., Neurological Surgery, 9402 Presbyterian-University Hospital, 230 Lothrop Street, Pittsburgh, Pennsylvania 15213.
43
Saphenous vein graft bypass of the cavernous internal carotid artery LALIGAM N . SEKHAR, M.D., CHANDRA N. SEN, M.D., AND HAE DONG JHO, M . D .
Department of Neurological Surgery, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania ~" Saphenous vein graft reconstruction was performed from the petrous to the supraclinoid internal carotid artery (ICA) to replace the cavernous ICA in six patients during direct intracavernous operations. Four of these patients had intracavernous neoplasms with invasion of the ICA and two had intracavernous ICA aneurysms that could not be clipped or occluded with intraluminal balloons. All but one patient had evidence of poor collateral flow reserve in a balloon occlusion test of the ICA. The superficial temporal artery was not present in four patients, was minuscule in one, and was damaged during the initial dissection in another, making it unsuitable for superficial temporal-to-middle cerebral artery branch anastomosis. Blood flow within the graft could not be established intraoperatively in one patient (who had excellent collateral circulation) due to the small size of the vein (3 mm). In all others, the grafts were patent on followup arteriography and transcranial Doppler studies. Three patients who had severe reduction of cerebral blood flow during test occlusion of the ICA exhibited temporary hemispheric neurological deficits postoperatively; the deficits were related to the duration of temporary ICA occlusion. All three recovered completely without evidence of infarction on computerized tomography (CT). One patient who clinically could not tolerate the balloon occlusion test of the ICA also had temporary neurological deficits with good recovery but showed evidence of border-zone infarction on CT scans. The present role of saphenous vein graft bypass of the cavernous ICA is discussed. KEY WORDS graft bypass
"
cavernous carotid artery
D
URING direct surgical treatment of neoplastic and vascular lesions involving the cavernous sinus, the surgeon sometimes is faced with the inability to preserve the internal carotid artery (ICA). In such instances, collateral circulation may be adequate to permit occlusion of the ICA without consequence. In some patients, however, some form of revascularization will be necessary, either because of the inadequacy of the collateral circulation or because of the desire to preserve the ipsilateral cerebrovascular flow in a young patient with a long life expectancy. In the past, revascularization has been accomplished by a superficial temporal artery (STA)-io-middle cerebral artery (MCA) branch anastomosis, an external carotid artery-MCA long venous graft, an STA-MCA branch venous graft, or an extracranial ICA-intracranial ICA long v e n o u s graft. 2'4-6'8-I1,18-20In this article, the use of a short venous graft from the petrous to the supraclinoid ICA, directly bypassing the cavernous ICA, is described as an alternative means of revascularization. The feasibility of such grafting (in cadavers) was first described by Sekhar, et al. 14 Since then, the procedure has been
J. Neurosurg. / Volume 72/January, 1990
9 internal carotid artery
9 saphenous vein
9
used clinically by our group and also by Fukushima (T Fukushima: personal communication, 1988). Clinical Material and M e t h o d s
Patient Population From 1983 to 1988, the first author has been involved in the direct surgical treatment o f the petrous or cavernous ICA in 170 patients with neoplastic or vascular lesions. Vein grafting from the cervical to the petrous ICA or graft reconstruction of the petrous ICA was used in seven of these patients.15 In six patients, vein grafting was performed from the petrous to the supraclinoid ICA, bypassing the cavernous sinus. The latter group is the subject of this report. Direct vein graft bypass o f the intracavernous ICA was used in four patients with neoplasms (three meningiomas and one squamous-cell carcinoma) and in two patients with intracavernous aneurysms (one congenital and the other presumably iatrogenic) (Table 1). All patients were evaluated preoperatively by physical and neurological examination, computerized tomog35
L. N. Sekhar, C. N. Sen, and H. D. Jho TABLE 1
Summary of six patients with graft bypass of the cavernous ICA*
Case No.
Age (yrs), Sex
Pathology & Location
Result of BTO
Type of Anastomosis SupraPetrous clinoid 1CA ICA
Patency
AnastoICA New mosis Occlusion Postoperative Time Time Deficits
64, F meningioma: cavernous sinus, clivus, sella
tolerated clinically; bifrontal CBF decrease
end-to- end-to- patent: angio end side 3 mos, TCD 14 mos
1 89hrs 5 hrs (proximal end redone)
48, F meningioma: cavernous sinus, clivus, sella
tolerated clinically; marked CBF reduction
end-to- end-to- patent: angio end side 3 mos, TCD 3 mos
17I hrs
3
44, F meningioma: cavernous sinus, clivus, sella
not done; good collaterals on angio
end-to- end-to- occluded 2 hrs at surgery end side
4
48, M squamouscell ca: cavernous sinus, ethmoid, maxilia, orbit 68, F intracavernous giant aneurysm
tolerated clinically; CBF reduction
end-to- end-to- patent: angio end end 2 mos, TCD 2
tolerated clinically; marked CBF reduction
end-to- end-to- patent: angio end side 3 days, TCD 2
38, F iatrogenic aneurysm
failed clinically; end-to- end-totemporary hemi- end side plegia, aphasia, seizures
5
171 hrs
permanent occlusion
temporary hemiparesis & abulia; worsened III function; delayed VII palsy temporary hemiparesis; memory problems; VI palsy; delayed VII paresis III, V paresis; IV, VI palsies; diabetes insipidus
Follow-Up Findings
Postop CT Scan at 2 mos
14 mos: normal mentation; partial III palsy; VII palsy recovered 7 mos: normal mentation, motor exam, & VII function; VI palsy
no cerebral infarction; residual clival tumor (gamma knife)
8 mos: III, IV paresis; VI palsy; diabetes insipidus improved 3 mos: died of metastatic disease
no cerebral infarction; no tumor
no new cerebral infarction; residual clival tumor (gamma knife)
12I hrs
2 hrs
none
1~ hrs
3 89hrs
temporary hemiparesis; III palsy
2 mos: III no cerebral palsy; 3 mos: infarction; died suddenlyt aneurysm thrombosed
2 hrs
2 hrs
temporary hemiparesis; dysphasia; memory loss; III palsy
7 mos: norborder-zone mal speech & infarction mentation, mild III paresis
no cerebral infarction; recurrent tumor
mos
mos
6
patent: angio 7 mos, TCD 6 mos
* ICA = internal carotid artery; BTO = balloon test occlusion; CBF --- cerebral blood flow; TCD = transcranial Doppler ultrasound; CT = computerized tomography; angio = angiogram; ca = carcinoma. Roman numerals denote cranial nerves. t Autopsy revealed myocardial infarction, a patent vein graft, and no cerebral infarction.
r a p h y ( C T ) , a n d m a g n e t i c r e s o n a n c e i m a g i n g . In a d d i t i o n , all p a t i e n t s h a d c e r e b r a l a n g i o g r a p h y a n d five u n d e r w e n t a b a l l o o n o c c l u s i o n test o f t h e I C A . I n t h e b a l l o o n o c c l u s i o n test, t h e ipsilateral I C A w a s o c c l u d e d for 15 m i n u t e s i f n e u r o l o g i c a l l y t o l e r a t e d . T h i s was followed by a xenon-CT examination of cerebral blood flow (CBF) with and without temporary ICA occlusion. I n o n e p a t i e n t ( C a s e 3), a b a l l o o n o c c l u s i o n test was not performed because the patient could not tolerate a l e n g t h y a n g i o g r a p h i c p r o c e d u r e a n d b e c a u s e angiogr a p h y d e m o n s t r a t e d a p p a r e n t l y e x c e l l e n t c o l l a t e r a l circulation.
Operative Technique T h e c e r v i c a l I C A w a s e x p o s e d in all patients. A f r o n t o t e m p o r a l c r a n i o t o m y w a s f o l l o w e d b y the t e m porary removal of the superior and lateral rims and 36
walls o f t h e o r b i t a n d t h e z y g o m a t i c arch, i n c l u d i n g t h e m a n d i b u l a r fossa. E x t r a d u r a l m i d d l e fossa d i s s e c t i o n was p e r f o r m e d t o e x p o s e a n d u n r o o f t h e m a n d i b u l a r nerve, t h e m i d d l e m e n i n g e a l artery ( w h i c h w a s d i v i d e d ) , t h e g r e a t e r s u p e r f i c i a l p e t r o s a l n e r v e ( w h i c h w a s divided), a n d t h e h o r i z o n t a l s e g m e n t o f t h e p e t r o u s I C A . In all p a t i e n t s , it w a s n e c e s s a r y to r e m o v e t h e b o n e portion of the eustachian tube and expose the genu of the p e t r o u s I C A t o facilitate suturing. F o l l o w i n g d u r a l o p e n i n g a n d initial d i s s e c t i o n , t h e anterior clinoid process was removed, and the optic n e r v e w a s u n r o o f e d b y b o n e r e m o v a l . T h e distal i n t r a c a v e r n o u s I C A w a s d i s s e c t e d after t h e d i v i s i o n o f t h e d u r a l rings at its e x i t f r o m t h e c a v e r n o u s sinus. T h e c a v e r n o u s s i n u s w a s e n t e r e d by s u p e r i o r a n d l a t e r a l i n t r a d u r a l a p p r o a c h e s in t h e p a t i e n t s w i t h b e n i g n tum o r s to d e t e r m i n e i f t h e I C A c o u l d b e d i s s e c t e d free o f
J. Neurosurg. / Volume 72/January, 1990
Graft bypass of cavernous internal carotid artery
FIG. 1. Drawings depicting the saphenous vein graft bypass of the cavernous internal carotid artery (ICA) using an end-to-side anastomosis distally (left) or end-to-end anastomosis distally (right). Although the collateral circulation of the ophthalmic artery usually enables its occlusion without loss of vision, occlusion is best avoided when vision is intact preoperatively. Roman numerals denote cranial nerves.
t u m o r and in the patients with aneurysms to see if the aneurysm could be clipped. However, in the patient with a malignant neoplasm, the contents of the cavernous sinus were excised without entering the sinus. When direct vein grafting was decided upon, the patient was given 1000 mg of methylprednisolone intravenously, 12 and approximately a 7-cm length of the greater saphenous vein was harvested from the thigh. The distal anastomosis was usually completed first. Three temporary vascular clips were placed on the ICA: one in the neck, one distal to the ophthalmic artery, and one just proximal to the posterior communicating artery. For end (vein)-to-side (ICA) anastomosis, a linear arteriotomy was made on the anterior wall of the ICA (Fig. 1 left). Heparinized saline was used to wash the blood and any clot from the ICA and vein, but systemic heparinization was not employed for fear of causing bleeding from the operative wound. For endto-end anastomosis, the ICA was divided just superior to the ophthalmic artery and "fish-mouthed" (Fig. 1 right). The end of the vein was trimmed, denuded of adventitia, and fish-mouthed if necessary. Four 7-0 Prolene or 8-0 nylon sutures were placed to attach the vein to the ICA at diametrically opposite points. The rest of the anastomosis was completed with interrupted sutures. To check the anastomosis for leaks, the vein was irrigated with heparinized saline. A continuous suture technique was used in the first patient and subsequently abandoned in favor of an interrupted suturing technique. The latter took m o r e time but provided better approximation without leakage or stenosis at the suture line. Next, the petrous ICA was divided just proximal to the third division of the trigeminal nerve. There was
J. Neurosurg. / Volume 72/January, 1990
usually some back bleeding from the intracavernous ICA because of the anastomotic connections of the intracavernous branches. This bleeding was stopped by packing the lumen of the cavernous ICA with Surgicel (oxidized regenerated cellulose). The petrous ICA was then irrigated thoroughly with heparinized saline to clear blood or clot. The vein graft was t r i m m e d to a length of 5 to 6 cm and anastomosed end-to-end with 7-0 Prolene interrupted sutures. Before the last stitch was tied, the graft and the ICA were irrigated again with heparinized saline, and the proximal and distal temporary clips were released long enough to wash out any air bubbles. The intracavernous ICA was ligated permanently just proximal to the ophthalmic artery and divided proximal to the ligature. During the petrous anastomosis procedure, a temporary clip can be placed on the cavernous ICA proximal to the ophthalmic artery and on the vein graft. The two distal t e m p o r a r y clips can be removed to continue collateral flow through the ophthalmic artery (as was done in Case 6, see below). A regimen of intermittent subcutaneous heparin was used in the early postoperative period, and antiplatelet agents (aspirin or dipyridamole) were administered orally after 10 days to prevent late graft occlusions. 3'21 If the patient's eustachian tube was excised, a tympanostomy was inserted after 6 weeks.
S u m m a r y o f Cases In four patients the STA was absent as a result of prior surgery, in one it was minuscule, and in another it was injured during the operation. The time required to perform anastomosis of the graft ranged f r o m 60 to 90 minutes; however, in Case 1 the ICA was occluded
37
L. N. Sekhar, C. N. Sen, and H. D. Jho
FIG. 2. Case 2. Left: Preoperative angiogram showing encasement and narrowing of the intracavernous internal carotid artery and an irregularly narrowed posterior communicating artery, which is the dominant supplier to the posterior cerebral circulation. Right: Postoperative carotid angiogram showing patency of the venous graft. Some catheter-induced spasm of the upper cervical internal carotid artery is apparent.
for 5 hours because of thrombosis at the proximal anastomotic end of the graft, which was discovered after t u m o r resection. The anastomosis was reconstructed with a good result. 16 In Case 3 the graft was occluded intraoperatively, probably due to the very small size of the vein (diameter 3 mm). This patient had a good preoperative collateral circulation through the anterior and posterior c o m m u n i c a t i n g arteries and did not suffer any hemispheric neurological deficits postoperatively. One patient (Case 4), who had a large squamous-cell carcinoma, recovered well from the operation but died 3 months later of metastatic disease. In Case 5 a giant intracavernous aneurysm could not be clipped upon direct exploration, because it was an eccentric dilatation of the ICA. Graft replacement of the ICA took 2 hours to perform; however, the ICA was temporarily occluded for 3 89hours, because preparations for grafting had not been made. The patient recovered well from the procedure but died suddenly at home 3 months later. Autopsy revealed the cause o f death to be myocardial infarction. The graft was patent, and no cerebral infarction was found. Cases 2 and 6 are described below. Four patients tolerated balloon occlusion test of the ICA without neurological deficit but exhibited significant ipsilateral or bilateral reductions o f CBF ranging from 15 to 30 cc/100 g m / m i n . Three of these patients had temporary hemispheric deficits postoperatively, presumably related to intraoperative ICA occlusion for 2, 3 89and 5 hours. Another patient developed temporary hemiplegia, aphasia, and seizures during test occlu38
sion of the ICA. This patient manifested hemispheric neurological deficits postoperatively, related to temporary intraoperative ICA occlusion. She made a good recovery, but CT revealed evidence of cerebral infarction. Postoperative angiography demonstrated patent saphenous vein grafts in all five of these patients.
Illustrative Case Reports Case 2 This 48-year-old w o m a n with an extensive basal meningioma had undergone two prior t u m o r operations. The intracavernous ICA was encased and narrowed by the t u m o r (Fig. 2 left). The posterior communicating artery was the dominant supplier of the posterior cerebral artery territory and w a s irregularly narrowed by the tumor. The CBF decreased bilaterally during balloon occlusion test of the ICA, especially at the upper levels. At surgery, the t u m o r was excised along with the poorly functioning third through sixth cranial nerves. The ICA was replaced with a vein graft. Postoperatively, the patient had a mild hemiparesis for 2 days. Follow-up arteriography revealed a patent vein graft (Fig. 2 right). Seven months after the operation, the patient had a Karnofsky score of 80. A small t u m o r remnant in the clival area was treated with g a m m a knife radiotherapy. Case 6 This 38-year-old w o m a n presented with several severe episodes of epistaxis. She had an aneurysm arising J. Neurosurg. / Volume 72/January, 1990
Graft bypass of cavernous internal carotid artery
FIG. 3. Case 6. Left: Left internal carotid arteriogram revealing an aneurysm arising from the internal carotid artery and projecting into the sphenoid sinus. Right: Postoperative arteriogram showing a healthy vein graft.
from the intracavernous ICA and projecting medially into the sphenoid sinus (Fig. 3 left). This was presumed to have resulted from two prior transsphenoidal operations and one transethmoidal pituitary procedure for Cushing's disease. Arteriography showed the STA to be absent, but cross flow through the anterior communicating artery was present after ipsilateral c o m m o n carotid artery compression. Permanent balloon occlusion of the ICA was planned. However, the patient developed hemiplegia, aphasia, and seizures after test occlusion of the ICA and recovered slowly. An urgent operation was performed with electroencephalographic (EEG) monitoring. The intracavernous aneurysm was explored directly but not clipped because the cavernous sinus was found to be filled with granulation tissue. It was elected to perform vein graft bypass of the cavernous ICA. During the 2-hour temporary ICA occlusion for vein grafting, the blood pressure was elevated 40 torr, and no EEG changes were observed. However, postoperatively the patient suffered hemiplegia (which resolved in 5 days), dysphasia (which resolved in 14 days), and memory problems (which resolved slowly). Angiography revealed a patent graft (Fig. 3 right). Results of a CBF study on the 1st postoperative day were normal, but another study 1 week later revealed hyperemic areas in the border zone between the anterior, middle, and posterior cerebral arteries. These regions evolved into CT-defined infarcts. Seven months later, the patient had made a nearly complete recovery of her neurological deficits and had a Karnofsky score of 80. Discussion
Technical Factors The advantages and disadvantages of using vein grafts as arterial conduits, important technical points
J. Neurosurg. / Volume 72/January, 1990
regarding graft harvesting and anastomosis, and postoperative management were reviewed extensively by Sundt and Sundt. 21 When vein grafting is used to reconstruct the ICA, the shortest possible length of the graft and end-to-end anastomosis at both ends o f the graft are preferable to reduce turbulent flow. However, because of the position of the ophthalmic artery, an end-to-side anastomosis is technically easier to carry out at the distal end. An end-to-end distal anastomosis can be performed if the ophthalmic artery is sacrificed (because of orbital exenteration) or if there is an adequate length of healthy intracavernous ICA proximal to the ophthalmic artery. It proved easier to perform the distal anastomosis first. When the proximal anastomosis was undertaken first, blood ran down from the skull-base area along the graft and made the distal anastomosis more difficult. In Case 3 the proximal anastomosis was achieved first and the temporary clip was opened to check graft flow, because the vein was small. This resulted in clotting of the graft, because systemic heparinization was not used and the volume of flow was small. In this series, intraluminal shunts were not utilized because of technical difficulties and for fear of embolic complications.
Postoperative Neurological Deficits In three of the four patients who had a reduced CBF (but no neurological deficits) after balloon occlusion test of the ICA, temporary neurological deficits were observed postoperatively, corresponding to the areas of CBF reduction. In the patient with the poorest preoperative collateral circulation, hyperemia and subsequent infarction were demonstrated in the border-zone areas between vascular territories. No embolic occlusions of distal vessels were seen on postoperative arteriography.
39
L. N. Sekhar, C. N. Sen, and H. D. Jho TABLE 2 Revascularization alternatives after cavernous ICA occlusion*
Passed Preop BTO; CBF > 35 cc/100 gm/min no reconstruction
STA-MCA bypass plus direct venous graft
Passed Preop BTO; CBF 15-35 cc/100 gm/min STA-MCA bypass
long saphenous vein graft ECA-MCA
direct venous graft with brain protection
Failed Preop BTO or or
or
or
O?"
direct venous graft
long saphenous vein graft ECA-MCA direct venous graft with brain protection * Alternatives based on preoperative balloon test occlusion (BTO) results. ICA = internal carotid artery; CBF = cerebral blood flow; STA = superficial temporal artery; MCA = middle cerebral artery; ECA = external carotid artery. Brain protection: intraoperative high-dose barbiturate or etomidate therapy to achieve burst suppression on electroencephalogram.
These facts reinforce t h e b e l i e f t h a t the t e m p o r a l neurological deficits were c a u s e d b y i n t r a o p e r a t i v e flow r e d u c t i o n d u e to I C A o c c l u s i o n a n d n o t by e m b o l i from the a n a s t o m o t i c site. In this g r o u p o f patients, h y p e r t e n s i o n was i n d u c e d d u r i n g t e m p o r a r y I C A occlusion, b u t drugs to protect the b r a i n against i s c h e m i a , such as high-dose barbiturates, e t o m i d a t e , o r t h e " S e n d a l cocktail," were not u s e d . IA7'22 S u b s e q u e n t l y t r e a t e d p a t i e n t s who have und e r g o n e p r o l o n g e d t e m p o r a r y I C A occlusion have been given i n t r a o p e r a t i v e t h i o p e n t a l s o d i u m intravenously to achieve b u r s t s u p p r e s s i o n o n E E G recordings, with better results. Direct Vein Graft Reconstruction
of Cavernous ICA
W h e n the i n t r a c a v e r n o u s I C A m u s t be excised in a p a t i e n t w h o has a l o n g life e x p e c t a n c y , it is preferable to revascularize the b r a i n , even w h e n the preoperative collateral c i r c u l a t i o n is a d e q u a t e . T h e reasons for this are the following: 1) t h e ipsilateral cerebrovascular reserve is preserved b y r e v a s c u l a r i z a t i o n ; 2) m a n y intrac a v e r n o u s lesions, especially m e n i n g i o m a s a n d aneurysms, t e n d to i n v o l v e b o t h sides; a n d 3) there appears to be a n i n c r e a s e d risk o f a n e u r y s m f o r m a t i o n after u n i l a t e r a l I C A occlusion. 7 M a n y m e t h o d s o f c e r e b r a l revascularization are available to the surgeon. D i r e c t v e n o u s reconstruction o f the c a v e r n o u s I C A has the a d v a n t a g e o f providing a high-flow c o n d u i t i m m e d i a t e l y w i t h the shortest possible length o f vein, l e a d i n g f r o m a large artery to a n o t h e r large artery. T h e d i s a d v a n t a g e s are a 90- to 120-minute p e r i o d o f t e m p o r a r y I C A o c c l u s i o n a n d the potential for graft occlusion. T h e l o n g - t e r m status o f these grafts in t e r m s o f p a t e n c y a n d o t h e r p a t h o l o g i c a l changes such as a n e u r y s m f o r m a t i o n at b r a n c h sites is u n k n o w n at present. R e v a s c u l a r i z a t i o n t e c h n i q u e s using the STA still carry the lowest risk to t h e p a t i e n t a n d m u s t be used w h e n e v e r possible. 4,6,8 H o w e v e r , t h e S T A - M C A bypass alone m a y be i n a d e q u a t e to p r e v e n t a stroke after acute I C A o c c l u s i o n in p a t i e n t s with a very p o o r preoperative collateral circulation. 13 Possible alternatives for revascularization, d e p e n d i n g o n the status o f the preoperative collateral circulation, a r e o u t l i n e d in T a b l e 2. 40
Acknowledgments
Dr. Howard Yonas critiqued the manuscript, and the cerebral blood flow studies were performed under his supervision. Dr. Carl Snyderman participated in some of the surgical procedures. Judy Campbell prepared the manuscript, and Helene Marion edited it. References
1. Batjer HH, Frankfurt AI, Purdy PD, et al: Use of etomidate, temporary arterial occlusion, and intraoperative angiography in surgical treatment of large and giant cerebral aneurysms. J Neurosurg 68:232-240, 1988 2. Brown WE Jr, Ansell LV, Story JL: Technique of saphenous vein bypass from the common carotid artery to the middle cerebral artery, in Erickson DL (ed): Revascularization of the Ischemic Brain. New York: Futura Press, 1988, pp 167-199 3. Chesebro JH, Clements IP, Fuster V, et al: A plateletinhibitor drug trial in coronary-artery bypass operations. Benefit of perioperative dipyridamole and aspirin therapy on early postoperative vein-graft patency. N Engl J Med 307:73-78, 1982 4. Collice M, Arena O, Fontana RA: Superficial temporal artery to proximal middle cerebral artery anastomosis: clinical and angiographic long term results. Neurosurgery 19:992-997, 1986 5. Diaz FG, Pearce J, Ausman JI: Complications of cerebral revascularization with autogenous vein grafts. Nenrosurgery 17:271-276, 1985 6. Diaz FG, Umansky F, Mehta B, et al: Cerebral revascularization to a main limb of the middle cerebral artery in the Sylvian fissure. An alternative approach to conventional anastomosis. J Nearosurg 63:21-29, 1985 7. Dyste GW, Beck DW: D e novo aneurysm formation following carotid ligation: case report and review of literature. Neurosurgery 24:88-92, 1989 8. Jack CR Jr, Sundt TM Jr, Fode NC, et al: Superficial temporal-middle cerebral artery bypass: clinical pre- and postoperative angiographic correlation. J Neurosurg 69: 46-51, 1988 9. Little JR, Furlan AJ, Bryerton B: Short vein grafts for cerebral revascularization. J Neurosurg 59:384-388, 1983 10. Lougheed WM, Marshall BM, Hunter M, et al: Common carotid to intracranial internal carotid bypass venous graft. Technical note. J Neurosurg 34:114-118, 1971 11. Morimoto T, Sakaki T, Kakizaki T, et al: Radial artery graft for an extracranial-intracranial bypass in cases of J. Neurosurg. / V o l u m e 7 2 / J a n u a r y , 1990
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12. 13.
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internal carotid aneurysms. Report of two cases. Surg Neurol 30:293-297, 1988 Pearce JE, Dujovny M, Ho KL, et al: Acute inflammation and endothelial injury in vein grafts. Neurosurgery 17: 626-634, 1985 Samson DS, Neuwelt EA, Beyer CW, et al: Failure of extracranial-intracranial arterial bypass in acute middle cerebral artery occlusion: case report. Neurosurgery 6: 185-188, 1980 Sekhar LN, Burgess J, Akin O: Anatomical study of the cavernous sinus emphasizing operative approaches and related vascular and neural reconstruction. Neurosurgery 21:806-816, 1987 Sekhar LN, Schramm VL Jr, Jones NF, et al: Operative exposure and management of the petrous and upper cervical internal carotid artery. Neurosurgery 19: 967-982, 1986 Sekhar LN, Sen CN, Jho HD, et al: Surgical treatment of intracavernous neoplasms: a four-year experience. New rosurgery 24:18-30, 1989 Spetzler RF, Hadley MN, Rigamonti D, et al: Aneurysms of the basilar artery treated with circulatory arrest, hypo-
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18. 19.
20. 21. 22.
thermia, and barbiturate cerebral protection. J Neurosurg 68:868-879, 1988 Spetzler RF, Rhodes RS, Roski RA, et al: Subclavian to middle cerebral artery saphenous vein bypass graft. J Neurosurg 53:465-469, 1980 Sundt TM Jr, Piepgras DG, Houser OW, et al: Interposition saphenous vein grafts for advanced occlusive disease and large aneurysms in the posterior circulation. J Neurosurg 56:205-215, 1982 Sundt TM Jr, Piepgras DG, Marsh WR, et al: Saphenous vein bypass grafts for giant aneurysms and intracranial occlusive disease. J Neurosurg 65:439-450, 1986 Sundt TM III, Sundt TM Jr: Principles of preparation of vein bypass grafts to maximize patency. J Neurosurg 66: 172-180, 1987 Suzuki J (ed): Advances in Surgery for Cerebral Stroke. Tokyo: Springer-Verlag, 1988, pp 3-12
Manuscript received December 16, 1988. Address reprint requests to: Laligam N. Sekhar, M.D., Neurological Surgery, 9402 Presbyterian-University Hospital, 230 Lothrop Street, Pittsburgh, Pennsylvania 15213.
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