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Treatment of Intracranial Aneurysms by Combined Proximal Ligation and Extracranial-Intracranial Bypass with Vein Graft Michael Morgan, M.B., B.S., Michael BesSer, M.B., B.S., F.R.A.C.S., F.R.C.S.(C), Nicholas Dorsch, M.B., B.S., F.R.C.S., and John Segelov, M.B., B.S., F.R.C.S., F.R.A.C.S. Department of Neurosurgery, The Children's Hospital, and Department of Neurosurgery, Royal Prince Alfred Hospital, Sydney, Australia
Morgan M, Besser M, Dorsch N, Segelov J. Treatment of intracranial aneurysms by combined proximal ligation and extracranial-intracranial bypass with vein graft. Surg Neurol 1986;26:85-91.
Seven patients with internal carotid artery aneurysms, and one patient with a middle cerebral artery aneurysm, were managed by combining proximal ligation with an extracranial-intracranial bypass procedure. Five bypasses were done with an interposed vein graft between the external carotid artery and the distal middle cerebral artery (vein graft), and three were superficial temporal-middle cerebral artery bypasses (superficial temporal artery grafts). As demonstrated in postoperative angiograms, all eight patients had patent bypasses with nonfilling of the aneurysm. One patient developed transient dysphasia, but there were no permanent neurological deficits associated with carotid occlusion. Four patients had resolution of their neurological problems, and another three patients improved. The distribution of flow from vein grafts is more extensive than from superficial temporal artery grafts. This offers increased protection against ischemia, and increases the likelihood of internal carotid artery aneurysm thrombosis by reducing the turbulence in the distal internal carotid artery. KEYWOgDS: Intracranial aneurysm; Carotid ligation; Vein graft; Superficial temporal artery-middle cerebral artery bypass
Since the advent of cerebral vascular bypass surgery for the prevention of stroke [18], there have been many Variations of the procedure [8,10,12,14,15] for a wide range of clinical situations. Perhaps the most clearly defined role of the technique is in the management of anticipated ischemi~ resulting from surgical occlusion of the internal carotid artery or middle cerebral artery. The risk of stroke after ligation of the middle cerebral artery Address reprint requests to: Dr. M. Morgan, Department of Neurosurgery, The Children's Hospital, P. O. Box 34, Camperdown, N.S.W. 2050, Australia.
© 1986 by Elsevier Science Publishing Co., Inc.
is very high in the absence of an established bypass. Common carotid ligation, considered the most benign of the ligation procedures [9], carries a 15% incidence of early ischemic morbidity [11] and a 6% incidence of delayed ischemic morbidity [1]. There are also the possible complications of contralateral aneurysm formation [5,6] and hypertension [17]. Carotid ligation has been in the armamentarium of neurosurgeons for the management of aneurysms [11] since it was first performed by Sir Astley Cooper in 1805 [2] for a cervical internal carotid artery aneurysm. Recently, several authors have presented a series of combined proximal ligations and extracranial-intracranial bypasses for the management of certain aneurysms [3,4,7,13]. The conclusion from these reports is that this mode Of therapy is safe and effective for aneurysms where direct surgery is too difficult or dangerous, The present series of cases supports the efficacy of extracranial-intracranial bypass combined with proximal ligation for certain aneurysms and, in addition, suggests that the use of a vein graft between the external carotid and distal middle cerebral artery lessens the need for collateral supply via the circle of Willis. There is an extra margin of safety against ischemia, and in the distal internal carotid artery flow, and hence turbulence is reduced.
Case R e p o r t s Eight patients were operated on between May 1981 and December 1983. Their aneurysms had been considered inoperable on angiographic grounds (cases 1,2,4,6, and 8) or after exploration (cases 3,5, and 7), for direct exclusion [16].
Case I A 67-year-old woman presented with a 5-month history of diplopia. Neurological examination revealed a complete right sixth nerve palsy but was otherwise unre0090-3019/86/$3.50
Figure 1. Preoperative angiogram of case 1 demonstrating giant internal carotid artery aneurysm.
Figure2. Postoperativeangiogram of case l demonstratingfilling of middle cerebral artery branches through "double-barreled" superficial temporal artery-middle cerebral artery bypass.
Figure 3. Angiogram of case 3 after clipping of the internal carotid artery aneurysm.
Figure 4. Angiogram of case 3 2 years after clipping of the internal carotid artem aneurysm. Note the recurrence of the aneurysm.
Figure 5. Cross-compression angiogram of case 3 demonstrating goodfilling of the right middle cerebral artery from the left.
Figure 6. Postoperative angiogram of case 3 showing the extent of filling from the vein bypass after internal carotid artery ligation. No aneurysm is seen.
New Treatment of Aneurysm
markable. Angiography demonstrated a giant intracavernous aneurysm of the right internal carotid artery (Figure 1). On May 25, 1981, the patient underwent a "doublebarreled" superficial temporal artery-middle cerebral artery bypass followed by ligation of the right internal carotid artery in the neck. Her postoperative course was uneventful. When last reviewed in January 1984, she had an incomplete recovery of sixth nerve function. Subsequent angiograms revealed nonfilling of the aneurysm with a patent bypass, but with only a small contribution from the bypass (Figure 2).
Case 2 A 52-year-old housewife was admitted with left retroorbital headache and diplopia of 1-week duration. Neurological examination showed left third, fourth, and sixth nerve palsies and hypesthesia of the left forehead. Angiography demonstrated an intracavernous aneurysm, 1.2 cm in diameter, of the left internal carotid artery. On March 23, 1982, a left superficial temporal artery-middle cerebral artery bypass and ligation of the ieft internal carotid artery were performed. Her hypesthesia and third and fourtl~ nerve palsies resolved, but the sixth nerve palsy was still present in January 1984. Postoperative angiography revealed nonfiUing of the aneurysm and a patent bypass, but with filling of the distal middle cerebral artery only.
Case 3 A 60-year-old farmer presented in 1981 with right nasal hemianopsia, deterioration in acuity of the right eye, and right retroorbital headaches. An angiogram demonstrated a right supraclinoid internal carotid artery aneurysm. On August 10, 1981, the aneurysm was clipped; at the time of the operation it was noted that the internal carotid artery was diffusely atherosclerotic. After the operation he recovered quickly, with resolution of his neurological deficits, and angiography revealed that the aneurysm had been well clipped (Figure 3). H e remained well until 1983 when he developed the same symptoms, with deterioratio/l of right visual acuity ".¢# to 6/60. Angmgraphy demonstrated a broad-based aneurysm arising adjacent to the clip on the previous aneurysm (Figure 4). On cross-compression, there was good filling of the right middle and anterior cerebral arteries from the left internal carotid (Figure 5). On April 14, 1983, he underwent a right external carotid-middle cerebral artery bypass with saphenous vein, and ligation of the right internal carotid a~tery. The postoperative course was uneventful, and his neurological deficits resolved again. The postoperative angiogram did not fill
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the aneurysm, and the patent anastomosis filled the middle cerebral artery (Figure 6).
Case 4 A 32-year-old man with stage 3B Hodgkin's disease developed headache and a partial right oculomotor nerve palsy. Carotid angiography revealed an aneurysm, 0.6 cm in diameter, of the cavernous portion of the right internal carotid artery. It was unclear whether the aneurysm or Hodgkin's disease was the cause of his neurological problems, but it was thought initially that the aneurysm was significant. On April 7, 1983, he underwent a right superficial temporal artery'middle cerebral artery bypass and ligation of the right internal carotid artery. There were no complications. Postoperative angiography demonstrated nonfilling of this aneurysm and a patent anastomosis, ~but there was minimal contribution to flow in the middle cerebral artery. His third nerve palsy was unchanged. Three months later he was found to have lymphomatous meningitis and multiple cranial nerve palsies, with evidence of brainstem involvementl
Case 5 A 58-year-old left-handed housewife had been first treated in 1973 for acute onset of headache and dysphasia. She had been found to have a giant aneurysm of the right middle cerebral artery with an overlying subdural hematoma. At craniotomy, the subdural hematoma was evacuated and the aneurysm Coated with cotton wool Figure 7. Angiogram of case 5 demonstrating giant middle cerebralartery aneurysm 10 years after it had been wrapped and glued.
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and cyanoacrylate glue. After this procedure she experienced recurrent transient attacks of dysphasia and headaches. In 1983 she was admitted to our hospital after a severe transient ischemic attack, with dysphasia and weakness of the left arm. The giant right middle cerebral artery aneurysm (Figure 7) was still present on angiography. On May 4, 1983, a superior thyroid artery-middle cerebral artery bypass with a saphenous vein graft was performed after exploration of the giant aneurysm. A tourniquet was positioned around the middle cerebral artery proximal to the aneurysm and brought out subcutaneously. Angiography the following day demonstrated occlusion of the proximal end-to-end anastomosis, and it was revised by reanastomosing it to the external carotid artery. On the next day the tourniquet was closed to occlusion without any ischemic complications. The postoperative angiogram showed nonfilling of the aneurysm and patency of the graft, with the middle cerebral artery filling back to the point of occlusion (Figure 8). Since the operation the patient has had no headaches or ischemic symptoms.
Morgan et al
Figure 9. Preoperativeangiogram of case 6 demonstrating an aneurysm causing marked stenosis of the left internal carotid artery.
A 31-year-old schoolteacher presented with a 3-week history of headaches, and had noted frequent episodes of dysphasia, right arm paresthesia, and clumsiness in the 10 days prior to admission. She was otherwise well, and there was no history of trauma. Angiography dem-
onstrated an aneurysm, 10 mm in diameter, of the internal carotid artery, associated with 95% stenosis of the internal carotid artery in the petrous bone (Figure 9). On October 27, 1983, a left external carotid-middle cerebral artery bypass with saphenous vein was performed, followed by ligation of the internal carotid artery. There were no complications of the procedure, and her headaches and transient ischemic attacks re-
Figure 8. Right common carotid angiogram of case 5 after z~ein bypass and middle cerebral artery occlusion. Filling of the middle cerebralartery by the bypass is extensive without filling the aneurysm.
Figure 10. Angiography of case 6 after vein bypass and internal carotid artery ligation. Note the extensivefilling of the vein bypass.
Case 6
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solved. A postoperative angiogram demonstrated good filling of the middle cerebral artery and the internal carotid artery, and the aneurysm was not seen (Figure 10). Case 7
A 54-year-old housewife presented with a 12-month history of progressive visual failure in the left eye. On examination, acuity in this eye was 6/36, with no other neurological abnormalities. Angiograms revealed a giant aneurysm of the internal carotid artery in the region of the anterior clinoid process (Figure 11). On July 4, 1983, the patient underwent a left pterional craniotomy and exploration of the giant aneurysm, but it could not be clipped. After the operation the patient developed a subdural hematoma that required evacuation. She recovered, apart from further visual deterioration. On July 13, her visual acuity had deteriorated to 6/60, and by July 21 she had lost sight in the left eye. On October 25, 1983, the patient underwent a left external carotid-middle cerebral artery bypass graft with saphenous vein. For technical reasons, unrelated to flow in the donor vessel, the internal carotid artery was not ligated at this time. In spite of a fully patent left internal carotid artery the visual acuity improved markedly, and by November 21, 1983, visual acuity in the left eye was 6/12. Postoperative angiography demonstrated patency of both graft and internal carotid artery, and the continued filling of the giant aneurysm (Figure 12). Figure 11. Preoperative angiogram of case 7 demonstrating left internal carotid artery aneurysm.
Figure 12. Angiogram of case 7 after vein bypass but before ligation of the internal carotid artery.
Thirty-five days after the bypass procedure she was taken back to the operating room and the left internal carotid artery was ligated in the neck. Since this time her visual acuity has continued to improve; a postoperative angiogram showed a patent bypass, with flow from the bypass to the internal carotid artery and no evidence of filling of the aneurysm (Figure 13).
Figure 13. Postoperative angiogram of case 7 demonstrating the extensive filling of intracranial vesselsfrom the vein bypass and nonfilling of the aneurysm.
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Table 1. Clinical Outcome Case no.
Age
Sex
Symptoms
1 2 3 4 5 6 7
67 52 60 32 58 31 54
F F M M F F F
CNP CNP CNP CNP TIAs TIAs CNP
8
66
F
CNP 3
Site of aneurysm
6 3,4,5,6 2 3
Rt-ICA intracavernous Lt-ICA i n t r a c a v e r n o u s R t - I C A supraclinoid Rt-ICA intracavernous Rt-MCA L t - I C A skull base Lt-ICA i n t r a c a v e r n o u s and supraclinoid Lt-ICA intracavernous
2
Clinical result
Residual deficit
Good Excellent Excellent Poor Excellent Excellent Excellent
CNP 6 CNP 6 0 CNP 3 0 0 Improved CNP 2
Good
Transient dysphasia
Abbreviations: CNP, cranial nerve palsy; Rt. right; Lt, left; ICA, internal carotid artery; TIA, transient ischemic attack; MCA, middle cerebral artery.
Case 8
Summary
A 66-year-old librarian presented with a 6-week history of diplopia and ptosis on the left side. On examination it was found that she had had a left third nerve palsy. Angiography demonstrated a fusiform left intracavernous internal carotid artery aneurysm. On December 21, 1983, a saphenous vein graft was inserted between the left external carotid and the angular branch of the middle cerebral artery, and Selverstone clamp on the internal carotid artery was closed to 90%. A patent bypass was shown on angiography, and when the patient awoke the Selverstone clamp was advanced to occlusion. The following day the patient noticed that her diplopia had improved. Forty-eight hours after complete internal carotid artery occlusion she became dysphasic, although Doppler testing and palpation confirmed a patent bypass. A fluent dysphasia was the only manifestation of a completed stroke, from which it took the patient more than 3 months to recover. During this time her third nerve palsy completely resolved.
Eight patients (6 female), aged between 31 and 67 years, received surgical treatment. There were four intracavernous aneurysms, one giant supraclinoid internal carotid artery aneurysm, one giant middle cerebral artery aneurysm, one internal carotid artery aneurysm recurrent after previous clipping, and one internal carotid artery aneurysm in the carotid canal. Six patients presented with cranial nerve palsies and two experienced transient ischemic attacks. Only one of the four intracranial aneurysms had bled.
Table 2. Angiographic Fillingfrom Graft Case no.
STA graft
Vein graft and ICA ligation
1 2 3 4 5 6 7 8
4 MCA branches 2 MCA branches -1 M C A branch -----
--+ --+ + +
MCA
MCA MCA MCA
ICA
ICA ICA ICA
Complications A major neurological complication occurred in one patient, case 8. Immediate postoperative angiography had demonstrated good filling of the middle cerebral artery and internal carotid artery. A computed tomography scan later cnfirmed that the area of infarction was small, and probably in the region supplied by the angular artery. The patient recovered completely over several months.
Clinical Outcome Vein graft and MCA ligation ----MCA ----
Abbreviations: MCA, middle cerebral artery; ICA, internal carotid artery; STA, superficial temporal artery.
Clinical results for all patients appear in Table 1. Both patients with transient ischemic attacks had no further episodes of cerebral ischemia. Five of the six patients with cranial nerve palsies had good results with marked improvement in their deficits, and complete resolution was achieved in two patients. The patient who failed to improve was later found to have another cause for his third nerve palsy. No patient, in this somewhat short period of observation, has had a postoperative aneurysm hemorrhage. Of some interest is case 7, where there was consid-
New Treatment of Aneurysm
erable improvement in visual acuity before ligation of the internal carotid artery and after the high-flow vein bypass had been established. This suggests that the likely mechanism was reduced flow in the internal carotid artery, leading to less turbulence in the aneurysm.
Angiographic Outcome All the patients with superficial temporal artery bypasses underwent angiography at least 6 weeks after their operations. All eight patients were proven to have patent anastomses and nonvisualization of the aneurysm. There appears to be a significantly greater volume of brain perfused from vein grafts compared with the superficial temporal artery to middle cerebral artery anastomoses (Table 2). The arterial bypass contributed minimally to hemisphere flow, whereas the vein grafts appeared to replace most or all of the distribution of the ligated vessel. This occurred even when collateral circulation via the circle of Willis was present before operation (Figures 5 and 6, case 3). Discussion An interposed vein graft between the external carotid and the middle cerebral artery has advantages over the superficial temporal artery-middle cerebral artery anastomosis as a supplementary procedure in the treatment of aneurysms by Hunterian ligation. These advantages stem from the difference in flow between these two grafts, and hence, the lesser reliance on a competent circle of Willis where a vein graft is used. The first advantage is the greater margin of safety against cerebral ischemia after acute proximal ligation. Gelber and Sundt [4] reported on 10 patients undergoing superficial temporal artery-middle cerebral artery bypass and carotid ligation, and found that six had cerebral blood flows after occlusion of 20 ml/100 g per minute or less, three developed transient aphasia, and one patient could not tolerate occlusion. The only postoperative neurological deficit that occurred in the present series was due to a technical fault in the anastomosis with embolism, rather than to inadequate flow through the graft. The second advantage of the vein graft is the reduction of flow in the terminal internal carotid artery from collaterals (posterior communicating artery and ophthalmic artery). It follows that turbulence in this area would be reduced, leading to a reduction in forces propagating aneurysmal growth, so that more complete thrombosis in the aneurysm can occur. This is the probable mechanism of the early clinical improvement in case 7, which took place while the internal carotid artery was still patent.
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Conclusion Whenever direct surgical ablation of an aneurysm of the internal carotid artery or middle cerebral artery is impossible, or is considered to involve a high risk, an effective alternative is an extracranial artery-middle cerebral artery bypass graft with proximal artery ligation. There is clinical and radiologic evidence that the interposition vein graft may be superior to the superficial temporal artery-middle cerebral artery bypass for more effective immediate protection against ischemia and for better promotion of aneurysm thrombosis. References 1. Black SPW, German WJ. The treatment of internal carotid artery aneurysms by proximal arterial ligation. A follow-up study. J Neurosurg 1953;10:590-601. 2, Cooper AP. A case of aneurysm of the carotid artery. Med Chir Tr (London) 1809;1:1-10. 3, Drake CG. Giant intracranial aneurysms: experience with surgical treatment in 174 cases. Clin Neurosurg 1979;26:12-95. 4. Gelber BR, Sundt TM Jr. Treatment of intracavernous and giant carotid aneurysms by combined internal carotid ligation and extra to intracranial bypass. J Neurosurg 1980;52:1-10. 5. Hashimoto N, Handa H, Hazama F. Experimentally induced cerebral aneurysms in rats. Surg Neurol 1978;18:3-8. 6. Hassler O. Experimental carotid ligation followed by aneurysmal formation and other morphological changes in the circle of Willis. J Neurosurg 1963;20:1-7. 7. Hopkins LN, Grand W. Extracranial-intracranial arterial bypass in the treatment of aneurysms of the carotid and middle cerebral arteries. Neurosurgery 1979;5:21-31. 8. Little JR, Furlan AJ, Bryerton B. Short vein graft for cerebral revascularization. J Neurosurg 1983;59:384-8. 9. Love JG, Dart LH. Results of carotid ligation with particular reference to intracranial aneurysms. J Neurosurg 1967 ;27:89-93. 10. Miller CF, Spetzler RF, Kopaniky DJ. Middle meningeal to middle cerebral arterial bypass for cerebral revascularization: case report. J Neurosurg 1979;50:802-4. 11. Schorstein J. Carotid ligation in saccular intracranial aneurysms. Br J Surg 1946;28:50-70. 12. Spetzler RF, Chater N. Occipital artery-middle cerebral anastomosis for cerebral artery occlusive disease. Surg Neurol 1974;2:235-8. 13. Spetzler RF, Schuster H, Roski RA. Elective extracranial-intracranial arterial bypass in the treatment of inoperable giant aneurysms of the internal carotid artery. J Neurosurg 1980;53:22-7. 14. Spetzler RF, Rhodes RS, Roski RA, Likovec MJ. Subclavian t o middle cerebral artery saphenous vein bypass graft. J Neurosurg 1980;53:465-9. 15. Story JL, Brown WE Jr, Eidelberg J, Arom KV, Stewart JR. Cerebral revascularization: common carotid to distal middle cerebral artery bypass. Neurosurgery 1978;2:131-4. 16. Whittle IR, Dorsch NW, Besser M. Giant intracranial aneurysms: diagnosis, management and outcome. Surg Neurol 1984;21:218-30. 17. Winn HR, Richardson AE, Jane JA. Late morbidity and mortality of common carotid ligarion for posterior communicating aneurysms. J Neurosurg 1977;47:727-36. 18. Yasargil MG. Microsurgery applied to neurosurgery. New York: Academic Press, 1969.