CHAPTER
Complications of Cerebral Revascularization o. Howard Reichman, M.D. This report is based upon a 5-year experience (August 1970 to August 1975) with surgical anastomosis between the superficial temporal artery (STA) and a cortical branch of the middle cerebral artery (MCA) in 70 patients. An effort has been made to include all instances wherein less than ideal long term results have been achieved, for in the failures of the present lie the opportunities for future progress. (However, those patients with completed stroke and fixed neurological deficit, who were operated upon to prevent further worsening of neurological function and failed to improve after surgery, have not been considered since this situation is viewed as a separate problem.) An evaluation of suboptimal results should be prefaced by a discussion of the prevalence of risk factors and other coexisting diseases in the population under consideration. RISK FACTORS
As precursors of cerebral vascular disease, risk factors have been considered paramount (6), and their frequency as a major factor leading to subsequent morbidity and mortality was recognized early in this experience (10).
Hypertension In this series significant hypertension was recognized in 30 patients. Seven were considered to have severe hypertension and another seven were considered to have moderately severe hypertension. Severe hypertension was recognized as a major factor leading to the death of three patients. Cases 4 and 10 have been reported (10-12). Case 34 is reported herein.
Cardiac Disease Significant cardiac disease was recognized in 13 patients of this series. Eleven patients had previous myocardial infarction indicated by clinical manifestations and EKG findings. Two of these demonstrated left 318
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Diabetes Fourteen patients of this series had diabetes. Its medical management was not a difficult problem "in most cases, but it undoubtedly contributed to the development of cerebral arterial disease. Hyperlipoproteinemia Abnormal lipid metabolism was demonstrated in only seven patients of this series because this laboratory determination was not performed routinely. However, it was abnormal in the young patients with isolated intracranial occlusive arterial lesions. COEXISTING DISEASES
Patients with occlusive vascular disease were found frequently to harbor other disease processes which vitally effected their long term outcome. Systemic Diseases Significant chronic pulmonary disease was recognized in three patients of this series. One patient had chronic idiopathic thrombocytopenia. One patient had chronic osteomyelitis in a lower extremity. Others had evidence of mild renal disease or minor abnormalities in' hepatic function. Cancer Two patients were demonstrated subsequently to have cancer. One died 3 months postoperatively of pancreatic carcinoma, and the other died 5 months postoperatively of pulmonary carcinoma. Atherosclerosis of Abdominal Aorta Two of three patients with occlusion of the abdominal aorta had symptoms of the Leriche syndrome. Another patient had undergone resection of an abdominal aortic aneurysm. Intracranial Aneurysm During preoperative angiography, an asymptomatic intracranial aneurysm was demonstrated in two patients. One patient had transient
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bundle branch block, one having had prior surgery for anastomosis between an internal mammary artery and the anterior descending branch of the left coronary artery. Three patients had experienced atrial fibrillation which was under control with quinidine sulfate. One patient had rheumatic heart disease and prior mitral valvuloplasty.
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NONFATAL COMPLICATIONS
Permanent Worsening of Neurological Status Three patients are currently worse in comparison with their preoperative clinical status: Case 15. Patient had a giant aneurysm of the left middle cerebral artery. An STA-cortical MCA anastomosis was performed and the middle cerebral artery ligated distal to the aneurysm. As dissection was carried medially, the aneurysm ruptured. Hemostatic measures required clipping of the internal carotid artery resulting in no available source of irrigation for the lenticulostriate vessels. Postoperatively, the patient was dysphasic and hemiplegic. Arteriography 10 days after surgery demonstrated excellent perfusion of the middle cerebral territory by the STA bypass graft. Case 31. Patient had extensive bilateral arterial occlusive disease which was interpreted by various observers as fibromuscular dysplasia, cerebrovascular "moyamoya" disease, or both. This patient had experienced transient ischemic attacks involving both cerebral hemispheres over a 3-year period, followed by a severe left cerebral insult manifest by aphasia and right hemiplegia. The patient made substantial improvement and STA-cortical MCA anastomosis was performed. The operation was tolerated well and the patient made further improvement over several months. Arteriography, performed 6 months after surgery, demonstrated excellent flow through the STA bypass graft with extensive perfusion of the left middle cerebral territory. Because of widespread arterial occlusive disease and previous ischemic events involving the right cerebral hemisphere, the possibility of surgery on the second (right) side was considered. However, the presence of an asymptomatic aneurysm of the basilar artery raised concern that subsequent surgery, if required by the aneurysm, would be complicated by the presence of bilateral STA bypass grafts. After extensive consultation, it was decided ultimately to proceed with elective surgery to obliterate the aneurysm (14 months after STA-cortical MCA anastomosis). The operation progressed smoothly, but, for unknown reasons, the patient did not tolerate the procedure and developed aphasia with hemiplegia on the left side. Case 45. Patient developed aphasia and right hemiplegia after a 2-month history of transient ischemic events involving the left cerebral hemisphere. Considerable improvement followed during the next few months and an arteriogram demonstrated occlusion of the left internal carotid artery. Perfusion of the left middle cerebral territory resulted from a small posterior communicating artery which was irregularly stenosed by atherosclerotic disease. Right-to-left cross filling extended to the left anterior cerebral artery but not into the left middle cerebral artery, and there was no filling from the ophthalmic artery. Because it was supposed that disease of the posterior communicating artery placed the left cerebral hemisphere in jeopardy, STA-cortical MCA anastomosis was performed. The operation was tolerated well and the patient's condition was satisfactory following surgery. However, aphasia and right hemiplegia developed the next day. Arteriography demonstrated that the posterior communicating artery had closed and there was poor filling through the STA bypass graft.
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ischemic attacks (TIA) with mild residual dysphasia and right hemiparesis associated with stenosis of the left middle cerebral artery and recent subarachnoid hemorrhage from an aneurysm of the left internal carotid artery at its posterior communicating branch. Two patients had a giant intracranial aneurysm as the primary reason for STA-cortical MeA anastomosis.
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Temporary Worsening of Neurological Status Three patients were worse immediately after surgery than they had been preoperatively. One had experienced temporary worsening after previous arteriography and similarly, awakened from anesthesia with significantly increased right hemiparesis and dysphasia. This improved promptly and ultimately cleared beyond the preoperative status (minimal residual). The other two patients experienced only minimally increased weakness, which possibly was related to sacrifice of penetrating branches of the cortical artery selected for anastomosis (8). Both patients improved quickly and became essentially asymptomatic.
"RIND" Only one patient (with long standing occlusion of the left internal carotid artery) experienced transient ischemic attacks after surgery. These were infrequent, but this individual did experience a moderately severe episode of reversible ischemic neurological deficit (RIND) 5 months after surgery even though arteriography demonstrated abundant flow through the STA bypass graft.
Pulmonary Em bolus . Four patients developed a pulmonary embolus after surgery. Fortunately, none of these cases resulted in mortality. The circumstances of these patients are summarized in Table 23.1. This incidence is similar to that reported by Warlow and co-workers (13) in a series following stroke. The ever present threat of pulmonary embolus is emphasized by this experience and by recent studies of the frequent incidence of deep vein thrombosis following neurosurgical procedures (1, 4, 5). Perhaps with increased facility in performing STA-cortical MCA anastomosis and reduction of operating time, the incidence of pulmonary embolus will decrease. These patients were treated initially with heparin and subsequently maintained on warfarin. Case 38 developed a subdural hematoma which became symptomatic 7 weeks after surgery (Fig. 23.1).
Subdural Hematoma Cases 38 and 44 developed chronic subdural hematomas after surgery (Fig. 23.1). Both had received anticoagulant therapy. Drainage of the hematoma was accomplished through burr holes in each case and a prompt recovery followed.
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Comment: This case suggests some similarities to Case 7 reported by Ojemann and co-workers wherein a right middle cerebral stenosis became symptomatic after endarterectomy for a left internal carotid artery stenosis (7).
45/M
58/M
88/F
74/F
29
38
53t
63
Angiographic Features
Clinical Results
Duration of Surgery
Dysphasia and right hemiparesis-20 mos. (operated large farm)
ICA stenosis (supra- Unchanged 11 hrs. 50 min. (douclinoid) ble branch anastoMCA stenosis mosis) MCA branch occlusion (lesions on left) Unchanged Dysphasia and right hemipare- ICA occlusion (left) 7 hrs. 35 min. sis-fi years (operated janitorial service) Bilateral visual loss (counted Giant ICA aneurysm Right, slight improvement 9 hr. 35 min. (occipiI (right) (counts fingers accurately) tal artery graft) fingers inaccurately) Left, marked improvement Insertion of Crutchfield clam p(reads newspaper) 25 days after bypass surgery (in bed several weeks as clam p was closed) Slight improvement (not am- 6 hrs. 25 min. Right hemiparesis-17 days (in MCA stenosis (left) bulating) bed-weak right leg)
Clinical Features
22 days
58 days
4 days
14 days
Interval between Surgery and Pulmonary Embolus
* Cases 1-26, aspirin used for analgesia, 27-70, acetaminophen (Tylenol, McNeal Laboratories, Inc., Fort Washington, Pa.) used for analgesia. t Placed on sulfinpyrazone (Anturane, Geigy Pharmaceuticals, Ardsley, N.Y.) at the time of bypass surgery.
Agel Sex
Case No.*
TABLE 23.1 Pulmonary Embolus
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FIG. 23.1. Case 38. Frontal projection (subtraction version) of selective left external carotid arteriogram. Large avascular space over convexity of brain results from chronic subdural hematoma. Abundant left middle cerebral filling is derived from superficial temporal artery through anastomosis (arrow). Filling of internal carotid (intracranial) and anterior cerebral arteries is derived from ophthalmic and meningohypophyseal arteries. Patient had cervical occlusion of left internal carotid artery.
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Five patients experienced seizures preoperatively and again postoperatively. These cases are cited to indicate that in some individuals it is difficult, if not impossible, to distinguish between TIA and minor focal seizures. It is well known that both can result from cerebral ischemia and may coexist in the same patient. Treatment requires anticonvulsant medication in addition to the efforts designed to enhance cerebral perfusion.
Fever One patient developed fever on the 5th postoperative day which continued for 4 days. This subsided spontaneously and no cause was identified, however, it resulted in a few additional days of hospitalization. There were no wound infections in this series.
Scalp Necrosis Initially, when the major blood supply to the scalp was disconnected for use in developing new collateral circulation to the brain it was feared that scalp necrosis would be a frequent occurrence. Actually, this was
FIG. 23.2. Case 19. Scalp flap necrosis. Both frontal and parietal branches of the superficial temporal artery were used for separate anastomosis. To facilitate dissection of low lying frontal branch, the anterior limb of the incision was carried posteroinferiorly around the orbit, depriving the flap of circulation from supraorbital branches.
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Seizures
43/M 57/M
57IM 62/F 59/M
37 47 51
80IF
+ +
+ +
+
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65/M 51/M
Hypertension
Age/Sex
27 30 34
4 5 10
Case Number
+
+
+
Heart Disease
+ +
+
+
Diabetes
23.2 Mortality
+ +
Aortic Disease
TABLE
Acute myocardial infarction Brain stem ischemia Acute bilateral subdural hematomas, spontaneous Pulmonary carcinoma Cerebral infarction, contralateral Acute intracerebral hemorrhage (em bolectomy of cortical artery) Acute myocardial infarction Pancreatic carcinoma Acute myocardial infarction
Cause of Death
13 mos. 3 mos. 5 mos.
5 mos. 2 mos. 1 day
25 mos. 6 days 17 days
Interval Between Surgery and Death
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observed in only five patients and was significant in only two. Both of these had anatomical variations in the arrangement of scalp vessels which led to the use of an unusual scalp flap. A double branch anastomosis was performed in one (Fig. 23.2). Only a single vessel was used in the other. All scalp problems healed spontaneously without the need for plastic surgery. It is thought that these problems can be avoided in the future.
Subgaleal Fluid Collection One patient experienced subgaleal accumulation of CSF for a few weeks following surgery. This gradually subsided spontaneously.
Impaired Patency Postoperative arteriography was performed in 42 patients (usually 5 to 8 months after surgery). All new collateral channels were patent, but poor filling was demonstrated in five patients. Two of these (Cases 8 and 12) ultimately closed (9, 11). Case 8 had adequate collateral circulation and did not require further surgery. Case 12 developed a recurrence of TIA which clear~d after a second operation using the occipital artery as a
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FIG. 23.3. Case 34. Selective left vertebral arteriogram. (A) Frontal projection. Bilateral middle cerebral perfusion arises from the vertebrobasilar system by posterior communicating arteries. (B) Lateral projection. Posterior communicating vessels are visualized and provide filling of middle cerebral arteries. Pericallosal filling extends anteriorly from posterior cerebral arteries.
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bypass graft. Excellent perfusion was subsequently demonstrated by arteriography (9). MORTALITY
The nine deaths that have occurred in this series are summarized in Table 23.2. Myocardial Infarction
Three patients were asymptomatic and had returned to work prior to developing an acute, fatal myocardial infarction. Case 4 expired 25 months after surgery, Case 37 at 13 months, and Case 51 at 5 months. Cancer
A diagnosis of cancer was made postoperatively in two patients. Case 27 died of pulmonary carcinoma 5 months after surgery and Case 47 of pancreatic carcinoma at 3 months.
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FIG. 23.4. Case 34. Lateral view of selective right external carotid arteriogram. Superficial temporal artery (STA) irrigates entire middle cerebral territory through anastomosis (arrow).
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CLINICAL NEUROSURGERY
Brain Ischemia Two patients expired because of ischemia involving a region of the brain other than that served by the STA bypass graft. Case 5 had experienced frequent transient ischemic attacks of the left cerebral hemisphere while anticoagulated with heparin. Surgery was
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FIG. 23.5. Case 34. Frontal view (subtraction version) of selective right external carotid arteriogram. Superficial temporal artery enters cranial cavity to irrigate the middle cerebral territory through anastomosis (arrow).
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tolerated without difficulty, but sudden death 6 days later was attributed to brain stem infarction (11). Case 30 had dysphasia and right hemiparesis associated with left internal carotid artery occlusion. Surgery (STA-cortical MCA anastomosis) was performed on the left side and gradual improvement followed. A month later the patient became progressively lethargic and developed lack of awareness of the left side. Arteriography demonstrated poor perfusion through the STA bypass graft on the left, but normal findings on the right side. This patient had a progressive downhill course and
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FIG. 23.6. Case 34. Frontal projection of selective left vertebral arteriogram. Significant perfusion of right middle cerebral territory is not present. Perfusion of the left middle cerebral territory is derived from the vertebrobasilar system.
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CLINICAL NEUROSURGERY
expired a month later. Autopsy demonstrated several areas of infarction in both cerebral hemispheres, including a large, recent infarction within the right cerebral hemisphere that was considered responsible for the terminal events.
Intracranial Hemorrhage Two patients died of intracranial hemorrhage. Case 10 was asymptomatic following STA-cortical MCA anastomosis and had been discharged from the hospital. This patient had severe hypertension, but it was elected to treat this gradually. Seventeen days after surgery, the patient was awakened during the night with severe headache and vomited. The patient lapsed into deep coma, became decerebrate after a grand mal seizure, and expired a few hours later.
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FIG. 23.7. Case 34. Operative exposure of cortical surface above left ear as viewed through operating microscope: (1) cortical artery containing embolus; (2) cortical artery selected as recipient for anastomosis.
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Case 34. A 57-year-old man developed momentary weakness of his left leg during October 1973 and fell. Three days later he experienced transient numbness of his left 4th and 5th fingers. Eight days after the first episode, he developed clumsiness of his left hand
FIG. 23.8. Case 34. Higher power view of cortical artery containing embolus after dissection of arachnoidal investments.
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Autopsy demonstrated subdural hematoma over the superior surface of the tentorium and uniformly over both cerebral hemispheres. Thickness of the hematoma was not increased near the STA bypass graft which was not considered the source of bleeding (11). Case 34 expired because of an acute intracerebral hemorrhage and is the only death in this series attributed to surgery. However, in addition to STA-cortical MCA anastomosis, an embolus was removed from a cortical vessel, and reflow into the ischemic brain, in the presence of severe hypertension, is considered the probable cause of hemorrhage. This case report follows.
332
CLINICAL NEUROSURGERY
and was unable to grasp a piece of paper between the thumb and index finger. This problem persisted and he noted numbness of his upper and lower lips on the left side. A week later he developed progressive numbness of his left leg and foot. During his evaluation he was shown to have chronic renal disease and hypertension. An arteriogram, performed January 4, 1974, demonstrated bilateral cervical internal carotid occlusion with some bilateral filling of internal carotid (supraclinoid) and middle cerebral arteries from the respective ophthalmic and posterior communicating arteries (Fig. 23.3). On January 7,1974 an STA-cortical MCA anastomosis was performed on the right side. The patient tolerated the procedure well but was hypertensive (190/110) for the next few days. The left hemiparesis gradually improved. Hypertension remained a difficult management problem because of symptoms of postural hypotension in response to treatment. On March 12, 1974 he developed progressive numbness and weakness of his right hand and foot ("identical to prior difficulties on the opposite side"). On March 27, 1974 arteriography demonstrated that the STA bypass graft irrigated the entire right middle cerebral territory (Figs. 23.4 and 23.5). Significant contributions from the ophthalmic and
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FIG. 23.9. Case 34. Flow re-established in cortical artery after removal of embolus.
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Comment. This case illustrates that embolization bilateral carotid artery occlusion is possible. A possible an embolic cause of progressing stroke is retrograde thrombus with progressive occlusion of the orifices
above chronic mechanism for propagation of of penetrating
FIG. 23.10. Case 34. Cross section of brain at autopsy. Massive intracerebral hematoma lies beneath surgical site which includes occipital artery (OA) anastomosis.
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posterior communicating arteries into the right middle cerebral territory were no longer visualized (Fig. 23.6). The left side appeared unchanged from the previous examination with middle cerebral perfusion derived primarily from the left posterior communicating artery (Fig. 23.6). After considerable debate and in view of the good response to previous surgery, it was decided to proceed with a bypass graft on the second (left) side. This was performed March 28, 1974 and an excellent occipital artery was prepared for use as the graft artery. Upon exposing the cortical surface, an embolus was found occluding an angular branch of the left middle cerebral artery (Figs. 23.7 and 23.8). This filled a rather long segment of the cortical vessel and had the appearance of having been present for several days. An arteriotomy was performed, the embolus extracted, and flow re-established (Fig. 23.9). The proposed anastomosis was then accomplished between the occipital artery and another cortical branch of the middle cerebral artery. The patient tolerated the procedure well, but once again he had hypertension (250/140) postoperatively. The next morning his clinical condition was identical to that observed before surgery. However, by noon he had developed some slurring of speech and mild right hemiparesis. This gradually worsened during the day and he became comatose. He expired just before midnight. Autopsy demonstrated an enormous intracerebral hematoma beneath the surgical site (Fig. 23.10).
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CLINICAL NEUROSURGERY
CONCLUSIONS
Most patients in this series tolerated STA-cortical MCA anastomosis without difficulty and became asymptomatic. This operation is a reliable and reasonably safe method for establishing new pathways of collateral circulation to the brain. As with all neurosurgical procedures there are risks and potential complications (3). By itself, however, this operation does not pose unusual hazards and the minor problems that occurred during early development of this procedure can probably be eliminated or reduced in the future. The significance of risk factors cannot be overemphasized (6) and, if possible, they should be identified and adequately treated, particularly hypertension (2) and heart disease. The major problems experienced throughout this study have consistently occurred in the presence of complex situations resulting from generalized occlusive arterial disease, risk factors, or other coexisting disease processes. These will present a continuing challenge. REFERENCES 1. Coppola, A. R. Deep vein thrombosis. J. Neurosurg. 43: 510-511, 1975. 2. Freis, E. D. Effect of treatment of hypertension on the occurrence of stroke. In Cerebral Vascular Diseases. Ninth Princeton Conference, edited by J. P. Whisnant and B. A. Sandok, pp. 133-136. Grune & Stratton, New York, 1975. 3. Horwitz, N. H., and Rizzoli, H. V. Postoperative Complications in Neurosurgical Practice, 427 pp. Williams & Wilkins, Baltimore, 1967. 4. Joffe, S. N. Deep vein thrombosis, (Response to A. R. Coppola) J. Neurosurg., 43: 511, 1975. 5. Joffe, S. N. Incidence of postoperative deep vein thrombosis in neurosurgical patients. J. Neurosurg., 42: 201-203, 1975. 6. Kannel, W. B. Current status of the epidemiology of brain infarction associated with occlusive arterial disease. Stroke, 2: 295-318, 1971. 7. Ojemann, R. G., Crowell, R. M., Roberson, G. H., and Fisher, C. M. Surgical treatment of extracranial carotid occlusive disease. Clin. Neurosurg., 22: 214-263, 1975. 8. Penry, J. K., and Netsky, M. G. Experimental embolic occlusion of a single leptomeningeal artery. Arch. Neurol., 3: 391-398, 1960. 9. Reichman, O. H. Extracranial-intracranial arterial anastomosis. In Cerebral Vascular Diseases. Ninth Princeton Conference, edited by J. P. Whisnant and B. A. Sandok, pp. 175-185, Grone & Stratton, New York, 1975. 10. Reichman, O. H., Anderson, R. E., Roberts, T. S., and Heilbrun, M. P. The treatment of intracranial occlusive cerebrovascular disease by STA-cortical MCA anastomosis. In Microneurosurgery, edited by H. Handa, pp. 31-46, Igaku Shoin, Ltd., Tokyo, 1975.
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branches (8). The re-establishment of flow directly into ischemic brain (particularly in the presence of hypertension) is a distinct risk as demonstrated by this case and a case of middle cerebral artery embolectomy (Case H. T.) reported by Yasargil (14). This is the only operative mortality in this series and probably results from reflow into ischemic brain rather than STA-cortical MCA anastomosis.
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11. Reichman, O. H., Davis, D.O., Roberts, T. S., and Satovick, R. M. Anastomosis between STA and cortical branch of MCA for the treatment of occlusive cerebrovascular disease. In Reconstructive Surgery of Brain Arteries, edited by F. T. Merei, pp. 201-218. Akademiai Kiado, Budapest, 1974. 12. Reichman, O. H., Satovick, R. M., Davis, D.O., and Roberts, T. S. Collateral circulation to the middle cerebral territory by anastomosis of superficial temporal and cortical arteries. In Present Limits of Neurosurgery, edited by I. Fusek and Z. Kunc, pp. 369-373. Avicenum, Czechoslovak Medical Press, Prague, 1972. 13. Warlow, C., Ogston, D., and Douglas, A. S. Venous thrombosis following strokes. Lancet, 1: 1305-1306, 1972. 14. Yasargil, M. G. Diagnosis and indications for operations in cerebrovascular occlusive disease. In Microsurgery Applied to Neurosurgery, edited by M. G. Yasargil, pp. 95-119. Georg Thieme Verlag, Stuttgart, 1969.
Complications of Cerebral Revascularization o. Howard Reichman, M.D. This report is based upon a 5-year experience (August 1970 to August 1975) with surgical anastomosis between the superficial temporal artery (STA) and a cortical branch of the middle cerebral artery (MCA) in 70 patients. An effort has been made to include all instances wherein less than ideal long term results have been achieved, for in the failures of the present lie the opportunities for future progress. (However, those patients with completed stroke and fixed neurological deficit, who were operated upon to prevent further worsening of neurological function and failed to improve after surgery, have not been considered since this situation is viewed as a separate problem.) An evaluation of suboptimal results should be prefaced by a discussion of the prevalence of risk factors and other coexisting diseases in the population under consideration. RISK FACTORS
As precursors of cerebral vascular disease, risk factors have been considered paramount (6), and their frequency as a major factor leading to subsequent morbidity and mortality was recognized early in this experience (10).
Hypertension In this series significant hypertension was recognized in 30 patients. Seven were considered to have severe hypertension and another seven were considered to have moderately severe hypertension. Severe hypertension was recognized as a major factor leading to the death of three patients. Cases 4 and 10 have been reported (10-12). Case 34 is reported herein.
Cardiac Disease Significant cardiac disease was recognized in 13 patients of this series. Eleven patients had previous myocardial infarction indicated by clinical manifestations and EKG findings. Two of these demonstrated left 318
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23
COMPLICATIONS OF CEREBRAL REVASCULARIZATION
319
Diabetes Fourteen patients of this series had diabetes. Its medical management was not a difficult problem "in most cases, but it undoubtedly contributed to the development of cerebral arterial disease. Hyperlipoproteinemia Abnormal lipid metabolism was demonstrated in only seven patients of this series because this laboratory determination was not performed routinely. However, it was abnormal in the young patients with isolated intracranial occlusive arterial lesions. COEXISTING DISEASES
Patients with occlusive vascular disease were found frequently to harbor other disease processes which vitally effected their long term outcome. Systemic Diseases Significant chronic pulmonary disease was recognized in three patients of this series. One patient had chronic idiopathic thrombocytopenia. One patient had chronic osteomyelitis in a lower extremity. Others had evidence of mild renal disease or minor abnormalities in' hepatic function. Cancer Two patients were demonstrated subsequently to have cancer. One died 3 months postoperatively of pancreatic carcinoma, and the other died 5 months postoperatively of pulmonary carcinoma. Atherosclerosis of Abdominal Aorta Two of three patients with occlusion of the abdominal aorta had symptoms of the Leriche syndrome. Another patient had undergone resection of an abdominal aortic aneurysm. Intracranial Aneurysm During preoperative angiography, an asymptomatic intracranial aneurysm was demonstrated in two patients. One patient had transient
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bundle branch block, one having had prior surgery for anastomosis between an internal mammary artery and the anterior descending branch of the left coronary artery. Three patients had experienced atrial fibrillation which was under control with quinidine sulfate. One patient had rheumatic heart disease and prior mitral valvuloplasty.
320
CLINICAL NEUROSURGERY
NONFATAL COMPLICATIONS
Permanent Worsening of Neurological Status Three patients are currently worse in comparison with their preoperative clinical status: Case 15. Patient had a giant aneurysm of the left middle cerebral artery. An STA-cortical MCA anastomosis was performed and the middle cerebral artery ligated distal to the aneurysm. As dissection was carried medially, the aneurysm ruptured. Hemostatic measures required clipping of the internal carotid artery resulting in no available source of irrigation for the lenticulostriate vessels. Postoperatively, the patient was dysphasic and hemiplegic. Arteriography 10 days after surgery demonstrated excellent perfusion of the middle cerebral territory by the STA bypass graft. Case 31. Patient had extensive bilateral arterial occlusive disease which was interpreted by various observers as fibromuscular dysplasia, cerebrovascular "moyamoya" disease, or both. This patient had experienced transient ischemic attacks involving both cerebral hemispheres over a 3-year period, followed by a severe left cerebral insult manifest by aphasia and right hemiplegia. The patient made substantial improvement and STA-cortical MCA anastomosis was performed. The operation was tolerated well and the patient made further improvement over several months. Arteriography, performed 6 months after surgery, demonstrated excellent flow through the STA bypass graft with extensive perfusion of the left middle cerebral territory. Because of widespread arterial occlusive disease and previous ischemic events involving the right cerebral hemisphere, the possibility of surgery on the second (right) side was considered. However, the presence of an asymptomatic aneurysm of the basilar artery raised concern that subsequent surgery, if required by the aneurysm, would be complicated by the presence of bilateral STA bypass grafts. After extensive consultation, it was decided ultimately to proceed with elective surgery to obliterate the aneurysm (14 months after STA-cortical MCA anastomosis). The operation progressed smoothly, but, for unknown reasons, the patient did not tolerate the procedure and developed aphasia with hemiplegia on the left side. Case 45. Patient developed aphasia and right hemiplegia after a 2-month history of transient ischemic events involving the left cerebral hemisphere. Considerable improvement followed during the next few months and an arteriogram demonstrated occlusion of the left internal carotid artery. Perfusion of the left middle cerebral territory resulted from a small posterior communicating artery which was irregularly stenosed by atherosclerotic disease. Right-to-left cross filling extended to the left anterior cerebral artery but not into the left middle cerebral artery, and there was no filling from the ophthalmic artery. Because it was supposed that disease of the posterior communicating artery placed the left cerebral hemisphere in jeopardy, STA-cortical MCA anastomosis was performed. The operation was tolerated well and the patient's condition was satisfactory following surgery. However, aphasia and right hemiplegia developed the next day. Arteriography demonstrated that the posterior communicating artery had closed and there was poor filling through the STA bypass graft.
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ischemic attacks (TIA) with mild residual dysphasia and right hemiparesis associated with stenosis of the left middle cerebral artery and recent subarachnoid hemorrhage from an aneurysm of the left internal carotid artery at its posterior communicating branch. Two patients had a giant intracranial aneurysm as the primary reason for STA-cortical MeA anastomosis.
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Temporary Worsening of Neurological Status Three patients were worse immediately after surgery than they had been preoperatively. One had experienced temporary worsening after previous arteriography and similarly, awakened from anesthesia with significantly increased right hemiparesis and dysphasia. This improved promptly and ultimately cleared beyond the preoperative status (minimal residual). The other two patients experienced only minimally increased weakness, which possibly was related to sacrifice of penetrating branches of the cortical artery selected for anastomosis (8). Both patients improved quickly and became essentially asymptomatic.
"RIND" Only one patient (with long standing occlusion of the left internal carotid artery) experienced transient ischemic attacks after surgery. These were infrequent, but this individual did experience a moderately severe episode of reversible ischemic neurological deficit (RIND) 5 months after surgery even though arteriography demonstrated abundant flow through the STA bypass graft.
Pulmonary Em bolus . Four patients developed a pulmonary embolus after surgery. Fortunately, none of these cases resulted in mortality. The circumstances of these patients are summarized in Table 23.1. This incidence is similar to that reported by Warlow and co-workers (13) in a series following stroke. The ever present threat of pulmonary embolus is emphasized by this experience and by recent studies of the frequent incidence of deep vein thrombosis following neurosurgical procedures (1, 4, 5). Perhaps with increased facility in performing STA-cortical MCA anastomosis and reduction of operating time, the incidence of pulmonary embolus will decrease. These patients were treated initially with heparin and subsequently maintained on warfarin. Case 38 developed a subdural hematoma which became symptomatic 7 weeks after surgery (Fig. 23.1).
Subdural Hematoma Cases 38 and 44 developed chronic subdural hematomas after surgery (Fig. 23.1). Both had received anticoagulant therapy. Drainage of the hematoma was accomplished through burr holes in each case and a prompt recovery followed.
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Comment: This case suggests some similarities to Case 7 reported by Ojemann and co-workers wherein a right middle cerebral stenosis became symptomatic after endarterectomy for a left internal carotid artery stenosis (7).
45/M
58/M
88/F
74/F
29
38
53t
63
Angiographic Features
Clinical Results
Duration of Surgery
Dysphasia and right hemiparesis-20 mos. (operated large farm)
ICA stenosis (supra- Unchanged 11 hrs. 50 min. (douclinoid) ble branch anastoMCA stenosis mosis) MCA branch occlusion (lesions on left) Unchanged Dysphasia and right hemipare- ICA occlusion (left) 7 hrs. 35 min. sis-fi years (operated janitorial service) Bilateral visual loss (counted Giant ICA aneurysm Right, slight improvement 9 hr. 35 min. (occipiI (right) (counts fingers accurately) tal artery graft) fingers inaccurately) Left, marked improvement Insertion of Crutchfield clam p(reads newspaper) 25 days after bypass surgery (in bed several weeks as clam p was closed) Slight improvement (not am- 6 hrs. 25 min. Right hemiparesis-17 days (in MCA stenosis (left) bulating) bed-weak right leg)
Clinical Features
22 days
58 days
4 days
14 days
Interval between Surgery and Pulmonary Embolus
* Cases 1-26, aspirin used for analgesia, 27-70, acetaminophen (Tylenol, McNeal Laboratories, Inc., Fort Washington, Pa.) used for analgesia. t Placed on sulfinpyrazone (Anturane, Geigy Pharmaceuticals, Ardsley, N.Y.) at the time of bypass surgery.
Agel Sex
Case No.*
TABLE 23.1 Pulmonary Embolus
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FIG. 23.1. Case 38. Frontal projection (subtraction version) of selective left external carotid arteriogram. Large avascular space over convexity of brain results from chronic subdural hematoma. Abundant left middle cerebral filling is derived from superficial temporal artery through anastomosis (arrow). Filling of internal carotid (intracranial) and anterior cerebral arteries is derived from ophthalmic and meningohypophyseal arteries. Patient had cervical occlusion of left internal carotid artery.
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Five patients experienced seizures preoperatively and again postoperatively. These cases are cited to indicate that in some individuals it is difficult, if not impossible, to distinguish between TIA and minor focal seizures. It is well known that both can result from cerebral ischemia and may coexist in the same patient. Treatment requires anticonvulsant medication in addition to the efforts designed to enhance cerebral perfusion.
Fever One patient developed fever on the 5th postoperative day which continued for 4 days. This subsided spontaneously and no cause was identified, however, it resulted in a few additional days of hospitalization. There were no wound infections in this series.
Scalp Necrosis Initially, when the major blood supply to the scalp was disconnected for use in developing new collateral circulation to the brain it was feared that scalp necrosis would be a frequent occurrence. Actually, this was
FIG. 23.2. Case 19. Scalp flap necrosis. Both frontal and parietal branches of the superficial temporal artery were used for separate anastomosis. To facilitate dissection of low lying frontal branch, the anterior limb of the incision was carried posteroinferiorly around the orbit, depriving the flap of circulation from supraorbital branches.
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Seizures
43/M 57/M
57IM 62/F 59/M
37 47 51
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65/M 51/M
Hypertension
Age/Sex
27 30 34
4 5 10
Case Number
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+ +
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23.2 Mortality
+ +
Aortic Disease
TABLE
Acute myocardial infarction Brain stem ischemia Acute bilateral subdural hematomas, spontaneous Pulmonary carcinoma Cerebral infarction, contralateral Acute intracerebral hemorrhage (em bolectomy of cortical artery) Acute myocardial infarction Pancreatic carcinoma Acute myocardial infarction
Cause of Death
13 mos. 3 mos. 5 mos.
5 mos. 2 mos. 1 day
25 mos. 6 days 17 days
Interval Between Surgery and Death
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observed in only five patients and was significant in only two. Both of these had anatomical variations in the arrangement of scalp vessels which led to the use of an unusual scalp flap. A double branch anastomosis was performed in one (Fig. 23.2). Only a single vessel was used in the other. All scalp problems healed spontaneously without the need for plastic surgery. It is thought that these problems can be avoided in the future.
Subgaleal Fluid Collection One patient experienced subgaleal accumulation of CSF for a few weeks following surgery. This gradually subsided spontaneously.
Impaired Patency Postoperative arteriography was performed in 42 patients (usually 5 to 8 months after surgery). All new collateral channels were patent, but poor filling was demonstrated in five patients. Two of these (Cases 8 and 12) ultimately closed (9, 11). Case 8 had adequate collateral circulation and did not require further surgery. Case 12 developed a recurrence of TIA which clear~d after a second operation using the occipital artery as a
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FIG. 23.3. Case 34. Selective left vertebral arteriogram. (A) Frontal projection. Bilateral middle cerebral perfusion arises from the vertebrobasilar system by posterior communicating arteries. (B) Lateral projection. Posterior communicating vessels are visualized and provide filling of middle cerebral arteries. Pericallosal filling extends anteriorly from posterior cerebral arteries.
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bypass graft. Excellent perfusion was subsequently demonstrated by arteriography (9). MORTALITY
The nine deaths that have occurred in this series are summarized in Table 23.2. Myocardial Infarction
Three patients were asymptomatic and had returned to work prior to developing an acute, fatal myocardial infarction. Case 4 expired 25 months after surgery, Case 37 at 13 months, and Case 51 at 5 months. Cancer
A diagnosis of cancer was made postoperatively in two patients. Case 27 died of pulmonary carcinoma 5 months after surgery and Case 47 of pancreatic carcinoma at 3 months.
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FIG. 23.4. Case 34. Lateral view of selective right external carotid arteriogram. Superficial temporal artery (STA) irrigates entire middle cerebral territory through anastomosis (arrow).
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CLINICAL NEUROSURGERY
Brain Ischemia Two patients expired because of ischemia involving a region of the brain other than that served by the STA bypass graft. Case 5 had experienced frequent transient ischemic attacks of the left cerebral hemisphere while anticoagulated with heparin. Surgery was
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FIG. 23.5. Case 34. Frontal view (subtraction version) of selective right external carotid arteriogram. Superficial temporal artery enters cranial cavity to irrigate the middle cerebral territory through anastomosis (arrow).
COMPLICATIONS OF CEREBRAL REVASCULARIZATION
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tolerated without difficulty, but sudden death 6 days later was attributed to brain stem infarction (11). Case 30 had dysphasia and right hemiparesis associated with left internal carotid artery occlusion. Surgery (STA-cortical MCA anastomosis) was performed on the left side and gradual improvement followed. A month later the patient became progressively lethargic and developed lack of awareness of the left side. Arteriography demonstrated poor perfusion through the STA bypass graft on the left, but normal findings on the right side. This patient had a progressive downhill course and
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FIG. 23.6. Case 34. Frontal projection of selective left vertebral arteriogram. Significant perfusion of right middle cerebral territory is not present. Perfusion of the left middle cerebral territory is derived from the vertebrobasilar system.
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CLINICAL NEUROSURGERY
expired a month later. Autopsy demonstrated several areas of infarction in both cerebral hemispheres, including a large, recent infarction within the right cerebral hemisphere that was considered responsible for the terminal events.
Intracranial Hemorrhage Two patients died of intracranial hemorrhage. Case 10 was asymptomatic following STA-cortical MCA anastomosis and had been discharged from the hospital. This patient had severe hypertension, but it was elected to treat this gradually. Seventeen days after surgery, the patient was awakened during the night with severe headache and vomited. The patient lapsed into deep coma, became decerebrate after a grand mal seizure, and expired a few hours later.
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FIG. 23.7. Case 34. Operative exposure of cortical surface above left ear as viewed through operating microscope: (1) cortical artery containing embolus; (2) cortical artery selected as recipient for anastomosis.
COMPLICATIONS OF CEREBRAL REVASCULARIZATION
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Case 34. A 57-year-old man developed momentary weakness of his left leg during October 1973 and fell. Three days later he experienced transient numbness of his left 4th and 5th fingers. Eight days after the first episode, he developed clumsiness of his left hand
FIG. 23.8. Case 34. Higher power view of cortical artery containing embolus after dissection of arachnoidal investments.
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Autopsy demonstrated subdural hematoma over the superior surface of the tentorium and uniformly over both cerebral hemispheres. Thickness of the hematoma was not increased near the STA bypass graft which was not considered the source of bleeding (11). Case 34 expired because of an acute intracerebral hemorrhage and is the only death in this series attributed to surgery. However, in addition to STA-cortical MCA anastomosis, an embolus was removed from a cortical vessel, and reflow into the ischemic brain, in the presence of severe hypertension, is considered the probable cause of hemorrhage. This case report follows.
332
CLINICAL NEUROSURGERY
and was unable to grasp a piece of paper between the thumb and index finger. This problem persisted and he noted numbness of his upper and lower lips on the left side. A week later he developed progressive numbness of his left leg and foot. During his evaluation he was shown to have chronic renal disease and hypertension. An arteriogram, performed January 4, 1974, demonstrated bilateral cervical internal carotid occlusion with some bilateral filling of internal carotid (supraclinoid) and middle cerebral arteries from the respective ophthalmic and posterior communicating arteries (Fig. 23.3). On January 7,1974 an STA-cortical MCA anastomosis was performed on the right side. The patient tolerated the procedure well but was hypertensive (190/110) for the next few days. The left hemiparesis gradually improved. Hypertension remained a difficult management problem because of symptoms of postural hypotension in response to treatment. On March 12, 1974 he developed progressive numbness and weakness of his right hand and foot ("identical to prior difficulties on the opposite side"). On March 27, 1974 arteriography demonstrated that the STA bypass graft irrigated the entire right middle cerebral territory (Figs. 23.4 and 23.5). Significant contributions from the ophthalmic and
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FIG. 23.9. Case 34. Flow re-established in cortical artery after removal of embolus.
COMPLICATIONS OF CEREBRAL REVASCULARIZATION
333
Comment. This case illustrates that embolization bilateral carotid artery occlusion is possible. A possible an embolic cause of progressing stroke is retrograde thrombus with progressive occlusion of the orifices
above chronic mechanism for propagation of of penetrating
FIG. 23.10. Case 34. Cross section of brain at autopsy. Massive intracerebral hematoma lies beneath surgical site which includes occipital artery (OA) anastomosis.
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posterior communicating arteries into the right middle cerebral territory were no longer visualized (Fig. 23.6). The left side appeared unchanged from the previous examination with middle cerebral perfusion derived primarily from the left posterior communicating artery (Fig. 23.6). After considerable debate and in view of the good response to previous surgery, it was decided to proceed with a bypass graft on the second (left) side. This was performed March 28, 1974 and an excellent occipital artery was prepared for use as the graft artery. Upon exposing the cortical surface, an embolus was found occluding an angular branch of the left middle cerebral artery (Figs. 23.7 and 23.8). This filled a rather long segment of the cortical vessel and had the appearance of having been present for several days. An arteriotomy was performed, the embolus extracted, and flow re-established (Fig. 23.9). The proposed anastomosis was then accomplished between the occipital artery and another cortical branch of the middle cerebral artery. The patient tolerated the procedure well, but once again he had hypertension (250/140) postoperatively. The next morning his clinical condition was identical to that observed before surgery. However, by noon he had developed some slurring of speech and mild right hemiparesis. This gradually worsened during the day and he became comatose. He expired just before midnight. Autopsy demonstrated an enormous intracerebral hematoma beneath the surgical site (Fig. 23.10).
334
CLINICAL NEUROSURGERY
CONCLUSIONS
Most patients in this series tolerated STA-cortical MCA anastomosis without difficulty and became asymptomatic. This operation is a reliable and reasonably safe method for establishing new pathways of collateral circulation to the brain. As with all neurosurgical procedures there are risks and potential complications (3). By itself, however, this operation does not pose unusual hazards and the minor problems that occurred during early development of this procedure can probably be eliminated or reduced in the future. The significance of risk factors cannot be overemphasized (6) and, if possible, they should be identified and adequately treated, particularly hypertension (2) and heart disease. The major problems experienced throughout this study have consistently occurred in the presence of complex situations resulting from generalized occlusive arterial disease, risk factors, or other coexisting disease processes. These will present a continuing challenge. REFERENCES 1. Coppola, A. R. Deep vein thrombosis. J. Neurosurg. 43: 510-511, 1975. 2. Freis, E. D. Effect of treatment of hypertension on the occurrence of stroke. In Cerebral Vascular Diseases. Ninth Princeton Conference, edited by J. P. Whisnant and B. A. Sandok, pp. 133-136. Grune & Stratton, New York, 1975. 3. Horwitz, N. H., and Rizzoli, H. V. Postoperative Complications in Neurosurgical Practice, 427 pp. Williams & Wilkins, Baltimore, 1967. 4. Joffe, S. N. Deep vein thrombosis, (Response to A. R. Coppola) J. Neurosurg., 43: 511, 1975. 5. Joffe, S. N. Incidence of postoperative deep vein thrombosis in neurosurgical patients. J. Neurosurg., 42: 201-203, 1975. 6. Kannel, W. B. Current status of the epidemiology of brain infarction associated with occlusive arterial disease. Stroke, 2: 295-318, 1971. 7. Ojemann, R. G., Crowell, R. M., Roberson, G. H., and Fisher, C. M. Surgical treatment of extracranial carotid occlusive disease. Clin. Neurosurg., 22: 214-263, 1975. 8. Penry, J. K., and Netsky, M. G. Experimental embolic occlusion of a single leptomeningeal artery. Arch. Neurol., 3: 391-398, 1960. 9. Reichman, O. H. Extracranial-intracranial arterial anastomosis. In Cerebral Vascular Diseases. Ninth Princeton Conference, edited by J. P. Whisnant and B. A. Sandok, pp. 175-185, Grone & Stratton, New York, 1975. 10. Reichman, O. H., Anderson, R. E., Roberts, T. S., and Heilbrun, M. P. The treatment of intracranial occlusive cerebrovascular disease by STA-cortical MCA anastomosis. In Microneurosurgery, edited by H. Handa, pp. 31-46, Igaku Shoin, Ltd., Tokyo, 1975.
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branches (8). The re-establishment of flow directly into ischemic brain (particularly in the presence of hypertension) is a distinct risk as demonstrated by this case and a case of middle cerebral artery embolectomy (Case H. T.) reported by Yasargil (14). This is the only operative mortality in this series and probably results from reflow into ischemic brain rather than STA-cortical MCA anastomosis.
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11. Reichman, O. H., Davis, D.O., Roberts, T. S., and Satovick, R. M. Anastomosis between STA and cortical branch of MCA for the treatment of occlusive cerebrovascular disease. In Reconstructive Surgery of Brain Arteries, edited by F. T. Merei, pp. 201-218. Akademiai Kiado, Budapest, 1974. 12. Reichman, O. H., Satovick, R. M., Davis, D.O., and Roberts, T. S. Collateral circulation to the middle cerebral territory by anastomosis of superficial temporal and cortical arteries. In Present Limits of Neurosurgery, edited by I. Fusek and Z. Kunc, pp. 369-373. Avicenum, Czechoslovak Medical Press, Prague, 1972. 13. Warlow, C., Ogston, D., and Douglas, A. S. Venous thrombosis following strokes. Lancet, 1: 1305-1306, 1972. 14. Yasargil, M. G. Diagnosis and indications for operations in cerebrovascular occlusive disease. In Microsurgery Applied to Neurosurgery, edited by M. G. Yasargil, pp. 95-119. Georg Thieme Verlag, Stuttgart, 1969.
