Middle
Superficial Temporal to Cerebral Artery Anastomosis
Clinical Outcome in Patients With Ischemia of Infarction in Internal Carotid Artery Distribution Myoung C. Lee, MD; James
\s=b\ The clinical outcome of our first 40 with transient ischemic attacks, 22 with mild ischemic infarctions, and 12 with moderate ischemic infarctions) treated with a superficial temporal artery-middle cerebral artery anastomosis was analyzed. All cerebral ischemias or infarctions occurred in the internal carotid artery distribution. An independent neurologist observer recorded the patient's preoperative and postoperative medical and neurological histories and objective
patients (six
neurological findings. There was no operative mortality. During the period of observation (up to 36 months), four patients died of probable myocardial infarction. No patient suffered
from recurrent cerebral infarction. Three patients experienced a single ischemic event postoperatively. Neurological deficits were either unchanged (21 patients) or improved (19 patients). Postoperative angiograms showed patency in 97% of the
anastomoses. (Arch Neurol 36:1-4,
1979)
"establishment of an anastomosis ^ between the middle cerebral ar¬ tery (MCA) and the superficial tempo¬ ral artery (STA), often called the extracranial-intracranial bypass or ce¬ rebral revascularization procedure, has been used with increasing fre¬ quency since its introduction in 1967. ' '- The purpose of this operation is to provide additional channels for collateral circulation to the brain in patients suffering from ischemie cere¬ bral vascular disease. The procedure has been applied to various types of Accepted for publication June 13, 1978. From the Departments of Neurology (Drs Lee, Geiger, Klassen, and Resch), Neurosurgery (Drs Ausman and Chou), and Radiology (Dr Latchaw), University of Minnesota Hospitals, Minneapo-
lis. Read in part before the third Joint Meeting on Stroke and Cerebral Circulation, New Orleans,
February 1978. Reprint requests to Department of Neurology, University of Minnesota Hospitals, 420 Delaware St SE, Minneapolis, MN 55455 (Dr Lee).
I. Ausman, MD, PhD; Jonathan D. Arthur C. Klassen, MD; Shelley N.
intracranial disorder, but most often is used in patients with occlusive cere¬ bral vascular disease in whom carotid endarterectomy is not technically fea¬ sible.'" Neurosurgical literature sup¬ ports the beneficial value of this oper¬ ation and records a very low morbidity and mortality.'" However, this form of treatment for ischemie cerebral vascular disease has not received universal acceptance because of insuf¬ ficient objective data accumulated
during long-term
studies. To determine its clinical value, longterm controlled studies are needed using a large series of patients. The patients should be carefully selected and matched on the basis of clinical manifestations and laboratory find¬ ings. Such studies can adequately compare the frequency of transient ischemie attacks (TIAs), recurrent strokes, and neurologic findings in
operated
vs nonoperated on pa¬ However, such a controlled study was not possible before enough favorable clinical experience had been accumulated to justify a randomized trial. There was some skepticism in the neurological community about the early studies, which were reported by neurosurgeons who were assessing the results of their own procedures. Therefore, in 1974 at the University of Minnesota, a carefully designed study was initiated using a well-defined population clinically assessed by an independent examiner. It was ex¬ pected to provide useful and definitive
tients."
'"
information on the clinical value of this procedure. The purpose of this report is to present the clinical results of the first 40 STA-MCA anastomoses in patients with ischemie episodes or infarction in internal carotid artery distribution. PATIENTS AND METHODS Patients
A description of the patient population is given in Table 1. The median age was 56
Geiger, MS; Richard E. Latchaw, MD; Chou, MD, PhD; Joseph A. Resch, MD
(range, 29 to 71 years). There were 32 and eight women who had suffered from cerebral ischemia or infarction in the internal carotid artery distribution. Pa¬ tients with TIAs included only those who experienced such episodes and had normal findings on neurological examination at the time of inclusion in this study. Patients with severe neurological deficits, such as severe global aphasia or dementia or both, years men
depressed sensorium, or complete paralysis with inability to walk even with assistance, were excluded from this study and were not considered for the procedure. Patients with neurological deficits were divided into categories of mild or moderate to moder¬ ately severe ischemie cerebral infarction. In addition, these patients may have had TIAs or prolonged reversible ischemie neurologic deficits (PRINDs) superim¬ posed on evidence of cerebral infarction. Neurological deficits in this population were evaluated by a neurologist just prior to the operation. Five of these 40 patients had experi¬ enced amaurosis fugax. In two patients, this symptom was the only manifestation of cerebral vascular disease. The other three patients had histories of mild ischemie cerebral infarction in addition to amaurosis fugax. Since most patients with completed ischemie infarctions spontaneously im¬ proved, a waiting period of at least two months before surgery was considered important. This period was chosen to allow the infarcted area to heal before revascularization to diminish the chance of hemor¬ rhage into the affected area. Also, since we were interested in comparing the preoper¬ ative and postoperative neurologic status of the patient, it was thought that the patient's neurologic improvement would have occurred within three months after infarction. The median time between the patient's last ischemie episode and opera¬ tion was two months (range, two weeks to 48 months). The relationship of clinical diagnosis to preoperative angiographie abnormality is given in Table 2. Most of these patients underwent four-vessel angiography via the femoral artery approach for adequate visualization of both extracranial and intracranial circulation. If this approach could not be used, direct carotid or brachial angiography was employed. The angio-
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abnormalities in decreasing order of occurrence were as follows: unilateral carotid occlusion, 60%; bilateral internal carotid artery occlusion, 23%; multiple arterial occlusions in the internal carotid artery distribution, 10%; and inoperable high internal carotid artery or middle cere¬ bral artery stenosis or occlusion, 7%. Of the 40 patients included in this study, six had had TIAs and 22 had had mild cerebral infarction with or without TIAs or PRINDs but with mild neurological defi¬ cits. Twelve patients were classified as having had moderate or moderately severe cerebral infarction with or without TIAs or PRINDs, but with moderate to moderately severe neurological deficits. The frequency of associated medical diseases in this population is given in Table 3.
graphie
Study
Method
Operative Procedure and Postoperative Evaluation.—The STA-MCA procedure was performed by a surgical team led by the same neurosurgeon (J.I.A.) in all cases.
Standard postoperative care was provided and patients were closely observed for complications. A total of 45 procedures (right side, 25; left side, 20) were on
these 40
patients.
Follow-up Studies
Following discharge
from the hospital, administered by refer¬ ring physicians or in the outpatient clinics of the University of Minnesota Hospitals. Treatment of associated medical disease as well as cerebral vascular disease was indi¬ vidualized. The majority of the patients received antiplatelet aggregating agents: aspirin or dipyridamole or both. All patients were seen for follow-up neurological examination every three to six months. At these times, detailed informa¬ tion as to recurrent TIAs, recurrent strokes, status of associated systemic diseases, and neurological deficits was recorded. continued
care was
Follow-up angiograms
were
performed
in 38 (95%) of the 40 patients. The patients who failed to appear for examination as scheduled were contacted by telephone; all of them eventually did return. Information as to cause of death was obtained from the family physician or previously treating physicians in respect to the four patients who died.
and
Diagnosis
Age
Distribution Median
Clinical
TIA* Mild cerebral infarction with/without TIAs or PRINDs* Moderate to moderately severe cerebral infarction with/without TIAs or PRINDs Total
Table 2.—Clinical
Diagnosis
and
50
29-65
22
57
33-71
12
55 56
38-69 29-71
40
*TIA indicates transient ischemie attack; PRIND, deficit.
Age,
_yr_Age Range, yr
No. of Patients
Diagnosis
prolonged
reversible ischemie
neurologic
Preoperative Angiographie Abnormalities No. (%) of Patients Moderate
Transient
Angiographie
Preoperative Evaluation.—All patients considered for STA-MCA anastomosis were evaluated according to a detailed protocol for comprehensive medical and neurological assessment. In consultation with cardiologists and other specialists, patients with advanced cardiac or other medical diseases that were considered to carry a grave prognosis or that would be associated with a high surgical risk for this procedure were excluded from the study. An independent neurologist examined all of these patients preoperatively. Medi¬ cal information, frequency and severity of cerebral vascular disorders, and detailed neurological findings were recorded on precoded standardized protocol sheets.
performed
Table 1.—Clinical
Abnormalities Internal carotid artery occlusion(s) Unilateral Bilateral Inoperable ICA or MCA* stenosis or occlusion(s) Multiple artery occlusions Total
Ischemie Attack
Mild Cerebral Infarction
to
Moderately
Severe Cerebral Infarction
Total
24 (60)
13
9(23) 3(7) 12
22
4(10) 40(100)
"ICA indicates internal carotid artery; MCA, middle cerebral artery.
Table 3.—Incidence of
Significant Cerebrovascular
Risk Factors Incidence
Risk Factors
No. 32
Smoking Hypertension Obesity Myocardial infarction Hyperlipidemia Peripheral vascular disease
80 58
23 11
28 25
10
15
10
Diabetes mellitus
RESULTS
Perioperative Complications There was no operative mortality. Minor perioperative complications, however, were encountered. One pa¬ tient suffered from mild subendocardial infarction ten hours after opera¬ tion that cleared, while another devel¬ oped transient and asymptomatic atrial fibrillation. In one patient, a subdural hematoma that developed on the operated side was evacuated
percutaneously. Three patients had single episodes of focal seizures. Twenty-five percent of the 20 pa¬ tients with left-sided anastomoses
experienced transitory dysphasia postoperatively that cleared in all cases.
Duration of Observation
The mean duration of follow-up (from time of operation until last neurological evaluation) was 12 months, ranging from 3 to 36 months (Table 4). The average time lapsed
from the last cerebral vascular episode neurological evaluation was 20 months. to the last
Clinical Status
comparison of the number of episodes of amaurosis fugax and TIAs in these patients before and after operation shows a striking reduction A
in the number of recurrent TIAs (Table 5). One patient who had a histo¬ ry of multiple TIAs experienced an episode of expressive aphasia approxi¬ mately three months after the proce¬ dure. One patient with a history of multiple episodes of amaurosis fugax and hemispheral TIAs prior to the operation suffered complete and per¬ manent amaurosis of the same eye two months after the operation but had no further TIAs. In another patient, there was a mild recurrent episode of amaurosis fugax in the same eye two months after the opera¬ tion. No patient suffered cerebral infarction with persistent focal deficit
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Table 4.—Duration of
Table
Follow-up
No. of Postoperative
of
mo_Patients 12(30)
6
10(25) 13(33) 5(12) 40(100)
6-12 13-24 25-36 Total
Table
of Ischemie
Episodes
No. of
No. (%)
Duration,
5.—Frequency
Before and After
Surgery
Preoperative Attacks/Patients
,-
Total Attacks/Patients_1_2-3_4-5_> 5 _0_9_15_5_8_37 1
Total
6.—Neurological
2
10 5 16
0 9
3 40
Ï5
Status Before and After STA-MCA Anastomosis
Postoperative Status
Neurologic Findings
Clinical Diagnosis Transient ischemie attack Mild cerebral infraction
Moderate to moderately severe cerebral infarction
0 Normal 1 Subjective
Preoperatlve
objective weakness 2 Mild sensory and/or motor weakness; mild speech and/or visual impairment; no gross functional
icits before and after STA-MCA anas¬ tomosis is given in Table 6. Neurolog¬ ical findings in all patients remained unchanged or improved. Of those 34 patients who had focal neurological deficits before the operation, findings remained unchanged in 15 (44%) during the follow-up period, and improved in the other 19 patients (56%). No patient experienced in¬ creased neurological deficits, except for the one patient who suffered further impairment in visual acuity of one eye. No significant improvement was noted in patients who had severe motor deficits prior to the operation. Postoperative angiograms were ob¬ tained in 38 of the 40 patients. Ninetyseven percent of the anastomoses
patent angiographically. Eighty-
six percent showed enlargement of the superficial temporal artery on
postoperative
Change
Improved
no
21
10
40
21
disturbance 3 Moderate sensory and/or motor weakness; moderate speech and/or visual impairment; moderate functional disturbance 4 Severe sensory and/or motor weakness; severe speech and/or visual impairment; gross functional disturbance, but able to ambulate
during the entire follow-up period. The comparison of neurological def¬
subsequent
No
0
weakness;
Total
were
Status
Worse
angio¬
grams. In the one case in which paten¬ cy was not confirmed, the angiogram was performed within one week of surgery, showing slow filling of the
superficial temporal artery but no filling. This patient did not return for repeated angiography. In our experience with two other pa¬ tients, this finding suggested vascular spasm; on subsequent angiography cortical
three to six months later, patency of the anastomosis and cortical filling weraevident. Radiologie changes have been reported in part." Four patients died during the
follow-up period (5 to 27 months). The of death was myocardial infarc¬ tion in all of them. With the exception of one patient who developed amauro¬ cause
sis two months after surgery, the neurological status of these patients was stable at the time of death. Three of these four patients had had a histo¬ ry of previous myocardial infarction(s). Two experienced occasional episodes of angina. All had more than two significant risk factors for cere¬ bral vascular disease. COMMENT
The majority of the patients in¬ cluded in this study had unilateral or bilateral internal carotid artery occlu¬ sion^). There are relatively few data on the long-term outcome of patients who have such vascular disease, and the recorded incidence of recurrent stroke and long-term survivorship is quite disparate. In a retrospective study by Grillo and Patterson,1- four (9%) of 44 patients with internal carot¬ id artery occlusion developed ischemie cerebral infarction in the opposite cerebral hemisphere, but none on the ipsilateral side in five years. Similar very favorable long-term prognosis was noted in other series of patients with internal carotid artery occlu¬ sion."" However, in a small group of patients with transient ischemie epi¬ sodes who were diagnosed angiographically as having internal carotid artery occlusion, 45% had a major stroke within three years of the onset of TIA.1S In a study of 359 patients by
19
Fields and Lemak,1" 25% of survivors from acute internal carotid artery occlusion developed recurrent stroke in 44 months, 70% of which were ipsilateral to the occlusion. Fifty percent of these died of the stroke. Hardy et al'7 reported a high incidence of death (27% in 3.7 years) from subsequent strokes in their patients with internal carotid artery occlusion. The reasons for these apparent discrepancies may be related to sample size, severity of associated cerebral vascular disease, and cardiac status. Fields and Le¬ mak1* provide the most detailed data utilizing the largest sample size. In their study, 70% of the patients had poor or inadequate collateral circula¬ tion demonstrated angiographically. The patients with the poorest collater¬ al circulation had more severe neuro¬ logical deficits. The incidence of recurrent stroke in other types of angiographically stud¬ ied ischemie stroke" in the internal carotid artery distribution has been poorly elucidated. It is generally thought that the incidence of recur¬ rent stroke is higher in patients with a stenotic rather than an occluded inter¬ nal carotid artery. Patients with TIAs carry a 23% chance of having recur¬ rent stroke within a year.18 Of these, approximately 20% to 33% may show surgically inaccessible lesions.1"'20 There has been no definitive form of treatment for the patients with unilateral internal carotid artery oc¬ clusion. Toole et al15 treated four patients with carotid occlusion with
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warfarin sodium (Coumadin); subse¬ quent infarction developed in one during the average follow-up of four years. If patients with stenosis of the opposite carotid artery or other ves¬ sels in addition to the carotid occlusion were included, recurrent stroke with anticoagulation occurred in four21of 11 patients. Fields and Lemak16 re¬ ported that endarterectomy of the carotid artery within the first six weeks of the onset of symptoms was associated with a high operative mortality (50%). Of the successfully opened arteries, only 10% remained patent. These reports suggest that such management offers no signifi¬ cant benefit to patients with internal carotid artery occlusion. The prognosis of neurological defi¬ cit and likelihood of recurrent is¬ chemie neurological events in patients with occlusion or surgically inaccessi¬ ble high-grade stenosis of unilateral or bilateral internal carotid or middle cerebral arteries probably depends on adequacy of collateral circulation and perfusion of the involved area of the brain. An exception to this would be those cases with embolization from the stump of an occluded internal carotid artery.22 Therefore, clinical improvement due to MCA-STA anas¬ tomosis depends on whether this procedure provides enough additional blood flow to the ischemie area of the brain to improve impaired function and prevent recurrent cerebral is¬ chemie infarction and possibly death.23"25 The value of MCA-STA anastomosis in cerebral vascular disease cannot be established unless the outcome of patients subjected to this operation is superior to that of a comparable control group. Our preliminary data have shown no recurrent completed infarction, a striking reduction in the number of TIAs in the internal carot¬ id artery distribution, and an objec¬ tive clinical improvement in many of these patients. These results are encouraging and indicate a positive value of this procedure in appropriate
patients, as previously reported by other investigators.3919 Objective neurological improvement noted on follow-up examinations, however,
could have been related to the natural course following ischemie cerebral infarction, although there was a median duration of two months between stroke and MCA-STA proce¬ dure. Furthermore, postoperative antiplatelet therapy may have dimin¬ ished the incidence of recurrent ischemie attacks or infarction. No significant improvement was noted in
Reichman's4 patients, who had chronic and stable deficits after this proce¬ dure. In support of the favorable clinical outcome recorded in this study by an
independent participating neurologist preoperatively and postoperatively is
the fact that
a
number of these
patients who had poor or almost absent radiologie evidence of collater¬
al circulation to the involved area of the brain showed increased blood flow on postoperative angiograms. Pre¬ vious studies42425 have shown in¬ creased regional cerebral blood flow postoperatively coupled with clinical improvement and reduction in recur¬ rent cerebral ischemia or infarction. It is encouraging to note that this
surgical procedure was accompanied with minimal surgical morbidity, with no mortality, and with a very high
rate. Gratzl et aP have that in patients with acute strokes in evolution and patients with general reduction of regional cerebral blood flow, high mortality was asso¬ ciated with the revascularization pro¬ cedure. Furthermore, no clinical im¬ provement was noted in patients with severe neurologic deficit following this procedure. Selection of patients and timing of the procedure may have been important reasons for the good results in our study. Furthermore, no cases requiring total or near total nursing care were considered for surgery. In spite of careful selection, there were four deaths during the follow-up period related to acute myocardial infarction. A similarly high death rate due to myocardial infarction occurred in Reichman's experience.4 These figures, therefore, point out the importance of systemic risk factors for cerebrovascular dis¬ ease and continued adequate care of these risk factors preoperatively and
patency
reported
postoperatively.
Final and conclusive evidence of the value of the STA-MCA procedure must await the findings of a carefully designed, well-controlled, randomized
study.
This investigation was supported in part by grant NS-03364 from the National Institute of
and Communicative Diseases and Stroke. Ruth Loewenson, PhD, helped in statistical analysis of the data and preparation of the tables.
Neurological
References 1. Yasargil MG: Experimental small vessel surgery in the dog including patching and grafting of cerebral vessels and the formation of functional extra-intracranial shunts, in Donaghy RMP, Yasargil MG (eds): Microvascular Surgery.
St Louis, CV Mosby Co, 1967, pp 87-126. 2. Yasargil MG: Microsurgery Applied to Neurosurgery. Stuttgart, West Germany, Georg Thieme Verlag, 1969, p 105. 3. Gratzl O, Schmiedek P, Spetzler R, et al: Clinical experience with extra-intracranial arterial anastomosis in 65 cases. J Neurosurg 44:313\x=req-\ 324, 1976. 4. Reichman OH: Neurosurgical microsurgical anastomosis for cerebral ischemia: Five years experience, in Scheinberg P (ed): Cerebrovascular Diseases. New York, Raven Press, 1976, pp 311-336. 5. Sundt TM Jr, Siekert RG, Piepgras DG, et al: Bypass surgery for vascular disease of the carotid system. Mayo Clin Proc 51:677-692, 1976. 6. Ausman JI, Lee MC, Klassen AC, et al: Stroke: What's new? Cerebral revascularization. Minn Med 59:223-227, 1976. 7. Yasargil MG, Krayenbuhl HA, Jacobson JH II: Microneurosurgical arterial reconstruction. Surgery 67:221-233, 1970. 8. Yasargil MG, Yonekawa Y: Results of microsurgical extra-intracranial arterial bypass in the treatment of cerebral ischemia. Neurosurgery 1:22-24, 1977. 9. McDowell FH: The extracranial/intracranial bypass study. Stroke 8:545, 1977. 10. Whisnant JP: Extracranial-intracranial arterial bypass. Neurology 28:209-210, 1978. 11. Ausman J, Latchaw RE, Lee MC, et al: Results of multiple angiographic studies on cerebral revascularization patients, in Schmiedek P (ed): Microsurgery for Stroke. New York, Springer Verlag, 1977, pp 222-229. 12. Grillo P, Patterson RH Jr: Occlusion of the carotid artery prognosis (natural history) and the possibilities of surgical revascularization. Stroke
6:17-20, 1975.
13. Dyken ML, Klatte E, Kolar OJ, et al: Complete occlusion of common or internal carotid arteries: Clinical significance. Arch Neurol
30:343-346, 1974.
14. Anderson CA, Rich NM, Collins GJ Jr, et al: Unilateral internal carotid arterial occlusion: Special considerations. Stroke 8:669-671, 1977. 15. Toole JF, Janeway R, Choi K, et al: Transient ischemic attacks due to arteriosclerosis. Arch Neurol 32:5-12, 1975. 16. Fields WS, Lemak NA: Joint study of extracranial arterial occlusion: X. Internal carotid artery occlusion. JAMA 235:2734-2738, 1976. 17. Hardy WG, Lindner DW, Thomas LM, et al: Anticipated clinical course in carotid artery occlusion. Arch Neurol 6:64-76, 1962. 18. Whisnant J, Matsumoto N, Elvebeck LE: Transient cerebral ischemic attacks in Rochester, Minnesota 1945-1969. Mayo Clin Proc 48:194-198, 1973. 19. Chater N, Peters N: Neurosurgical microvascular bypass for stroke. West J Med 124:1-5, 1976. 20. Chater N, Mani J, Tonnemacher K: Superficial temporal artery bypass in occlusive cerebral vascular disease. Calif Med 119:9-13, 1973. 21. Fields WS: Selection of stroke patients for arterial reconstructive surgery. Am J Surg 125:527-529, 1973. 22. Barnett HJM, Peerless SJ, Wei M: The "stump" of the internal carotid artery: A source for further cerebral embolic ischemia, abstracted. Stroke 8:14, 1977. 23. Austin G, Laffin D, Hayward W: Physiologic factors in the selection of patients for superficial temporal artery to middle cerebral artery anastomosis. Surgery 75:861-868, 1974. 24. Schmiedek P, Gratzl O, Spetzler R, et al: Selection of patients for extracranial-intracranial arterial bypass surgery based on rCBF measurements. J Neurosurg 44:303-312, 1976. 25. Heilbrun MP, Reichman OH, Anderson RE, et al: Regional cerebral blood flow studies following superficial temporal-middle cerebral artery anastomosis. J Neurosurg 43:706-716, 1975.
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Superficial Temporal to Cerebral Artery Anastomosis
Clinical Outcome in Patients With Ischemia of Infarction in Internal Carotid Artery Distribution Myoung C. Lee, MD; James
\s=b\ The clinical outcome of our first 40 with transient ischemic attacks, 22 with mild ischemic infarctions, and 12 with moderate ischemic infarctions) treated with a superficial temporal artery-middle cerebral artery anastomosis was analyzed. All cerebral ischemias or infarctions occurred in the internal carotid artery distribution. An independent neurologist observer recorded the patient's preoperative and postoperative medical and neurological histories and objective
patients (six
neurological findings. There was no operative mortality. During the period of observation (up to 36 months), four patients died of probable myocardial infarction. No patient suffered
from recurrent cerebral infarction. Three patients experienced a single ischemic event postoperatively. Neurological deficits were either unchanged (21 patients) or improved (19 patients). Postoperative angiograms showed patency in 97% of the
anastomoses. (Arch Neurol 36:1-4,
1979)
"establishment of an anastomosis ^ between the middle cerebral ar¬ tery (MCA) and the superficial tempo¬ ral artery (STA), often called the extracranial-intracranial bypass or ce¬ rebral revascularization procedure, has been used with increasing fre¬ quency since its introduction in 1967. ' '- The purpose of this operation is to provide additional channels for collateral circulation to the brain in patients suffering from ischemie cere¬ bral vascular disease. The procedure has been applied to various types of Accepted for publication June 13, 1978. From the Departments of Neurology (Drs Lee, Geiger, Klassen, and Resch), Neurosurgery (Drs Ausman and Chou), and Radiology (Dr Latchaw), University of Minnesota Hospitals, Minneapo-
lis. Read in part before the third Joint Meeting on Stroke and Cerebral Circulation, New Orleans,
February 1978. Reprint requests to Department of Neurology, University of Minnesota Hospitals, 420 Delaware St SE, Minneapolis, MN 55455 (Dr Lee).
I. Ausman, MD, PhD; Jonathan D. Arthur C. Klassen, MD; Shelley N.
intracranial disorder, but most often is used in patients with occlusive cere¬ bral vascular disease in whom carotid endarterectomy is not technically fea¬ sible.'" Neurosurgical literature sup¬ ports the beneficial value of this oper¬ ation and records a very low morbidity and mortality.'" However, this form of treatment for ischemie cerebral vascular disease has not received universal acceptance because of insuf¬ ficient objective data accumulated
during long-term
studies. To determine its clinical value, longterm controlled studies are needed using a large series of patients. The patients should be carefully selected and matched on the basis of clinical manifestations and laboratory find¬ ings. Such studies can adequately compare the frequency of transient ischemie attacks (TIAs), recurrent strokes, and neurologic findings in
operated
vs nonoperated on pa¬ However, such a controlled study was not possible before enough favorable clinical experience had been accumulated to justify a randomized trial. There was some skepticism in the neurological community about the early studies, which were reported by neurosurgeons who were assessing the results of their own procedures. Therefore, in 1974 at the University of Minnesota, a carefully designed study was initiated using a well-defined population clinically assessed by an independent examiner. It was ex¬ pected to provide useful and definitive
tients."
'"
information on the clinical value of this procedure. The purpose of this report is to present the clinical results of the first 40 STA-MCA anastomoses in patients with ischemie episodes or infarction in internal carotid artery distribution. PATIENTS AND METHODS Patients
A description of the patient population is given in Table 1. The median age was 56
Geiger, MS; Richard E. Latchaw, MD; Chou, MD, PhD; Joseph A. Resch, MD
(range, 29 to 71 years). There were 32 and eight women who had suffered from cerebral ischemia or infarction in the internal carotid artery distribution. Pa¬ tients with TIAs included only those who experienced such episodes and had normal findings on neurological examination at the time of inclusion in this study. Patients with severe neurological deficits, such as severe global aphasia or dementia or both, years men
depressed sensorium, or complete paralysis with inability to walk even with assistance, were excluded from this study and were not considered for the procedure. Patients with neurological deficits were divided into categories of mild or moderate to moder¬ ately severe ischemie cerebral infarction. In addition, these patients may have had TIAs or prolonged reversible ischemie neurologic deficits (PRINDs) superim¬ posed on evidence of cerebral infarction. Neurological deficits in this population were evaluated by a neurologist just prior to the operation. Five of these 40 patients had experi¬ enced amaurosis fugax. In two patients, this symptom was the only manifestation of cerebral vascular disease. The other three patients had histories of mild ischemie cerebral infarction in addition to amaurosis fugax. Since most patients with completed ischemie infarctions spontaneously im¬ proved, a waiting period of at least two months before surgery was considered important. This period was chosen to allow the infarcted area to heal before revascularization to diminish the chance of hemor¬ rhage into the affected area. Also, since we were interested in comparing the preoper¬ ative and postoperative neurologic status of the patient, it was thought that the patient's neurologic improvement would have occurred within three months after infarction. The median time between the patient's last ischemie episode and opera¬ tion was two months (range, two weeks to 48 months). The relationship of clinical diagnosis to preoperative angiographie abnormality is given in Table 2. Most of these patients underwent four-vessel angiography via the femoral artery approach for adequate visualization of both extracranial and intracranial circulation. If this approach could not be used, direct carotid or brachial angiography was employed. The angio-
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abnormalities in decreasing order of occurrence were as follows: unilateral carotid occlusion, 60%; bilateral internal carotid artery occlusion, 23%; multiple arterial occlusions in the internal carotid artery distribution, 10%; and inoperable high internal carotid artery or middle cere¬ bral artery stenosis or occlusion, 7%. Of the 40 patients included in this study, six had had TIAs and 22 had had mild cerebral infarction with or without TIAs or PRINDs but with mild neurological defi¬ cits. Twelve patients were classified as having had moderate or moderately severe cerebral infarction with or without TIAs or PRINDs, but with moderate to moderately severe neurological deficits. The frequency of associated medical diseases in this population is given in Table 3.
graphie
Study
Method
Operative Procedure and Postoperative Evaluation.—The STA-MCA procedure was performed by a surgical team led by the same neurosurgeon (J.I.A.) in all cases.
Standard postoperative care was provided and patients were closely observed for complications. A total of 45 procedures (right side, 25; left side, 20) were on
these 40
patients.
Follow-up Studies
Following discharge
from the hospital, administered by refer¬ ring physicians or in the outpatient clinics of the University of Minnesota Hospitals. Treatment of associated medical disease as well as cerebral vascular disease was indi¬ vidualized. The majority of the patients received antiplatelet aggregating agents: aspirin or dipyridamole or both. All patients were seen for follow-up neurological examination every three to six months. At these times, detailed informa¬ tion as to recurrent TIAs, recurrent strokes, status of associated systemic diseases, and neurological deficits was recorded. continued
care was
Follow-up angiograms
were
performed
in 38 (95%) of the 40 patients. The patients who failed to appear for examination as scheduled were contacted by telephone; all of them eventually did return. Information as to cause of death was obtained from the family physician or previously treating physicians in respect to the four patients who died.
and
Diagnosis
Age
Distribution Median
Clinical
TIA* Mild cerebral infarction with/without TIAs or PRINDs* Moderate to moderately severe cerebral infarction with/without TIAs or PRINDs Total
Table 2.—Clinical
Diagnosis
and
50
29-65
22
57
33-71
12
55 56
38-69 29-71
40
*TIA indicates transient ischemie attack; PRIND, deficit.
Age,
_yr_Age Range, yr
No. of Patients
Diagnosis
prolonged
reversible ischemie
neurologic
Preoperative Angiographie Abnormalities No. (%) of Patients Moderate
Transient
Angiographie
Preoperative Evaluation.—All patients considered for STA-MCA anastomosis were evaluated according to a detailed protocol for comprehensive medical and neurological assessment. In consultation with cardiologists and other specialists, patients with advanced cardiac or other medical diseases that were considered to carry a grave prognosis or that would be associated with a high surgical risk for this procedure were excluded from the study. An independent neurologist examined all of these patients preoperatively. Medi¬ cal information, frequency and severity of cerebral vascular disorders, and detailed neurological findings were recorded on precoded standardized protocol sheets.
performed
Table 1.—Clinical
Abnormalities Internal carotid artery occlusion(s) Unilateral Bilateral Inoperable ICA or MCA* stenosis or occlusion(s) Multiple artery occlusions Total
Ischemie Attack
Mild Cerebral Infarction
to
Moderately
Severe Cerebral Infarction
Total
24 (60)
13
9(23) 3(7) 12
22
4(10) 40(100)
"ICA indicates internal carotid artery; MCA, middle cerebral artery.
Table 3.—Incidence of
Significant Cerebrovascular
Risk Factors Incidence
Risk Factors
No. 32
Smoking Hypertension Obesity Myocardial infarction Hyperlipidemia Peripheral vascular disease
80 58
23 11
28 25
10
15
10
Diabetes mellitus
RESULTS
Perioperative Complications There was no operative mortality. Minor perioperative complications, however, were encountered. One pa¬ tient suffered from mild subendocardial infarction ten hours after opera¬ tion that cleared, while another devel¬ oped transient and asymptomatic atrial fibrillation. In one patient, a subdural hematoma that developed on the operated side was evacuated
percutaneously. Three patients had single episodes of focal seizures. Twenty-five percent of the 20 pa¬ tients with left-sided anastomoses
experienced transitory dysphasia postoperatively that cleared in all cases.
Duration of Observation
The mean duration of follow-up (from time of operation until last neurological evaluation) was 12 months, ranging from 3 to 36 months (Table 4). The average time lapsed
from the last cerebral vascular episode neurological evaluation was 20 months. to the last
Clinical Status
comparison of the number of episodes of amaurosis fugax and TIAs in these patients before and after operation shows a striking reduction A
in the number of recurrent TIAs (Table 5). One patient who had a histo¬ ry of multiple TIAs experienced an episode of expressive aphasia approxi¬ mately three months after the proce¬ dure. One patient with a history of multiple episodes of amaurosis fugax and hemispheral TIAs prior to the operation suffered complete and per¬ manent amaurosis of the same eye two months after the operation but had no further TIAs. In another patient, there was a mild recurrent episode of amaurosis fugax in the same eye two months after the opera¬ tion. No patient suffered cerebral infarction with persistent focal deficit
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Table 4.—Duration of
Table
Follow-up
No. of Postoperative
of
mo_Patients 12(30)
6
10(25) 13(33) 5(12) 40(100)
6-12 13-24 25-36 Total
Table
of Ischemie
Episodes
No. of
No. (%)
Duration,
5.—Frequency
Before and After
Surgery
Preoperative Attacks/Patients
,-
Total Attacks/Patients_1_2-3_4-5_> 5 _0_9_15_5_8_37 1
Total
6.—Neurological
2
10 5 16
0 9
3 40
Ï5
Status Before and After STA-MCA Anastomosis
Postoperative Status
Neurologic Findings
Clinical Diagnosis Transient ischemie attack Mild cerebral infraction
Moderate to moderately severe cerebral infarction
0 Normal 1 Subjective
Preoperatlve
objective weakness 2 Mild sensory and/or motor weakness; mild speech and/or visual impairment; no gross functional
icits before and after STA-MCA anas¬ tomosis is given in Table 6. Neurolog¬ ical findings in all patients remained unchanged or improved. Of those 34 patients who had focal neurological deficits before the operation, findings remained unchanged in 15 (44%) during the follow-up period, and improved in the other 19 patients (56%). No patient experienced in¬ creased neurological deficits, except for the one patient who suffered further impairment in visual acuity of one eye. No significant improvement was noted in patients who had severe motor deficits prior to the operation. Postoperative angiograms were ob¬ tained in 38 of the 40 patients. Ninetyseven percent of the anastomoses
patent angiographically. Eighty-
six percent showed enlargement of the superficial temporal artery on
postoperative
Change
Improved
no
21
10
40
21
disturbance 3 Moderate sensory and/or motor weakness; moderate speech and/or visual impairment; moderate functional disturbance 4 Severe sensory and/or motor weakness; severe speech and/or visual impairment; gross functional disturbance, but able to ambulate
during the entire follow-up period. The comparison of neurological def¬
subsequent
No
0
weakness;
Total
were
Status
Worse
angio¬
grams. In the one case in which paten¬ cy was not confirmed, the angiogram was performed within one week of surgery, showing slow filling of the
superficial temporal artery but no filling. This patient did not return for repeated angiography. In our experience with two other pa¬ tients, this finding suggested vascular spasm; on subsequent angiography cortical
three to six months later, patency of the anastomosis and cortical filling weraevident. Radiologie changes have been reported in part." Four patients died during the
follow-up period (5 to 27 months). The of death was myocardial infarc¬ tion in all of them. With the exception of one patient who developed amauro¬ cause
sis two months after surgery, the neurological status of these patients was stable at the time of death. Three of these four patients had had a histo¬ ry of previous myocardial infarction(s). Two experienced occasional episodes of angina. All had more than two significant risk factors for cere¬ bral vascular disease. COMMENT
The majority of the patients in¬ cluded in this study had unilateral or bilateral internal carotid artery occlu¬ sion^). There are relatively few data on the long-term outcome of patients who have such vascular disease, and the recorded incidence of recurrent stroke and long-term survivorship is quite disparate. In a retrospective study by Grillo and Patterson,1- four (9%) of 44 patients with internal carot¬ id artery occlusion developed ischemie cerebral infarction in the opposite cerebral hemisphere, but none on the ipsilateral side in five years. Similar very favorable long-term prognosis was noted in other series of patients with internal carotid artery occlu¬ sion."" However, in a small group of patients with transient ischemie epi¬ sodes who were diagnosed angiographically as having internal carotid artery occlusion, 45% had a major stroke within three years of the onset of TIA.1S In a study of 359 patients by
19
Fields and Lemak,1" 25% of survivors from acute internal carotid artery occlusion developed recurrent stroke in 44 months, 70% of which were ipsilateral to the occlusion. Fifty percent of these died of the stroke. Hardy et al'7 reported a high incidence of death (27% in 3.7 years) from subsequent strokes in their patients with internal carotid artery occlusion. The reasons for these apparent discrepancies may be related to sample size, severity of associated cerebral vascular disease, and cardiac status. Fields and Le¬ mak1* provide the most detailed data utilizing the largest sample size. In their study, 70% of the patients had poor or inadequate collateral circula¬ tion demonstrated angiographically. The patients with the poorest collater¬ al circulation had more severe neuro¬ logical deficits. The incidence of recurrent stroke in other types of angiographically stud¬ ied ischemie stroke" in the internal carotid artery distribution has been poorly elucidated. It is generally thought that the incidence of recur¬ rent stroke is higher in patients with a stenotic rather than an occluded inter¬ nal carotid artery. Patients with TIAs carry a 23% chance of having recur¬ rent stroke within a year.18 Of these, approximately 20% to 33% may show surgically inaccessible lesions.1"'20 There has been no definitive form of treatment for the patients with unilateral internal carotid artery oc¬ clusion. Toole et al15 treated four patients with carotid occlusion with
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warfarin sodium (Coumadin); subse¬ quent infarction developed in one during the average follow-up of four years. If patients with stenosis of the opposite carotid artery or other ves¬ sels in addition to the carotid occlusion were included, recurrent stroke with anticoagulation occurred in four21of 11 patients. Fields and Lemak16 re¬ ported that endarterectomy of the carotid artery within the first six weeks of the onset of symptoms was associated with a high operative mortality (50%). Of the successfully opened arteries, only 10% remained patent. These reports suggest that such management offers no signifi¬ cant benefit to patients with internal carotid artery occlusion. The prognosis of neurological defi¬ cit and likelihood of recurrent is¬ chemie neurological events in patients with occlusion or surgically inaccessi¬ ble high-grade stenosis of unilateral or bilateral internal carotid or middle cerebral arteries probably depends on adequacy of collateral circulation and perfusion of the involved area of the brain. An exception to this would be those cases with embolization from the stump of an occluded internal carotid artery.22 Therefore, clinical improvement due to MCA-STA anas¬ tomosis depends on whether this procedure provides enough additional blood flow to the ischemie area of the brain to improve impaired function and prevent recurrent cerebral is¬ chemie infarction and possibly death.23"25 The value of MCA-STA anastomosis in cerebral vascular disease cannot be established unless the outcome of patients subjected to this operation is superior to that of a comparable control group. Our preliminary data have shown no recurrent completed infarction, a striking reduction in the number of TIAs in the internal carot¬ id artery distribution, and an objec¬ tive clinical improvement in many of these patients. These results are encouraging and indicate a positive value of this procedure in appropriate
patients, as previously reported by other investigators.3919 Objective neurological improvement noted on follow-up examinations, however,
could have been related to the natural course following ischemie cerebral infarction, although there was a median duration of two months between stroke and MCA-STA proce¬ dure. Furthermore, postoperative antiplatelet therapy may have dimin¬ ished the incidence of recurrent ischemie attacks or infarction. No significant improvement was noted in
Reichman's4 patients, who had chronic and stable deficits after this proce¬ dure. In support of the favorable clinical outcome recorded in this study by an
independent participating neurologist preoperatively and postoperatively is
the fact that
a
number of these
patients who had poor or almost absent radiologie evidence of collater¬
al circulation to the involved area of the brain showed increased blood flow on postoperative angiograms. Pre¬ vious studies42425 have shown in¬ creased regional cerebral blood flow postoperatively coupled with clinical improvement and reduction in recur¬ rent cerebral ischemia or infarction. It is encouraging to note that this
surgical procedure was accompanied with minimal surgical morbidity, with no mortality, and with a very high
rate. Gratzl et aP have that in patients with acute strokes in evolution and patients with general reduction of regional cerebral blood flow, high mortality was asso¬ ciated with the revascularization pro¬ cedure. Furthermore, no clinical im¬ provement was noted in patients with severe neurologic deficit following this procedure. Selection of patients and timing of the procedure may have been important reasons for the good results in our study. Furthermore, no cases requiring total or near total nursing care were considered for surgery. In spite of careful selection, there were four deaths during the follow-up period related to acute myocardial infarction. A similarly high death rate due to myocardial infarction occurred in Reichman's experience.4 These figures, therefore, point out the importance of systemic risk factors for cerebrovascular dis¬ ease and continued adequate care of these risk factors preoperatively and
patency
reported
postoperatively.
Final and conclusive evidence of the value of the STA-MCA procedure must await the findings of a carefully designed, well-controlled, randomized
study.
This investigation was supported in part by grant NS-03364 from the National Institute of
and Communicative Diseases and Stroke. Ruth Loewenson, PhD, helped in statistical analysis of the data and preparation of the tables.
Neurological
References 1. Yasargil MG: Experimental small vessel surgery in the dog including patching and grafting of cerebral vessels and the formation of functional extra-intracranial shunts, in Donaghy RMP, Yasargil MG (eds): Microvascular Surgery.
St Louis, CV Mosby Co, 1967, pp 87-126. 2. Yasargil MG: Microsurgery Applied to Neurosurgery. Stuttgart, West Germany, Georg Thieme Verlag, 1969, p 105. 3. Gratzl O, Schmiedek P, Spetzler R, et al: Clinical experience with extra-intracranial arterial anastomosis in 65 cases. J Neurosurg 44:313\x=req-\ 324, 1976. 4. Reichman OH: Neurosurgical microsurgical anastomosis for cerebral ischemia: Five years experience, in Scheinberg P (ed): Cerebrovascular Diseases. New York, Raven Press, 1976, pp 311-336. 5. Sundt TM Jr, Siekert RG, Piepgras DG, et al: Bypass surgery for vascular disease of the carotid system. Mayo Clin Proc 51:677-692, 1976. 6. Ausman JI, Lee MC, Klassen AC, et al: Stroke: What's new? Cerebral revascularization. Minn Med 59:223-227, 1976. 7. Yasargil MG, Krayenbuhl HA, Jacobson JH II: Microneurosurgical arterial reconstruction. Surgery 67:221-233, 1970. 8. Yasargil MG, Yonekawa Y: Results of microsurgical extra-intracranial arterial bypass in the treatment of cerebral ischemia. Neurosurgery 1:22-24, 1977. 9. McDowell FH: The extracranial/intracranial bypass study. Stroke 8:545, 1977. 10. Whisnant JP: Extracranial-intracranial arterial bypass. Neurology 28:209-210, 1978. 11. Ausman J, Latchaw RE, Lee MC, et al: Results of multiple angiographic studies on cerebral revascularization patients, in Schmiedek P (ed): Microsurgery for Stroke. New York, Springer Verlag, 1977, pp 222-229. 12. Grillo P, Patterson RH Jr: Occlusion of the carotid artery prognosis (natural history) and the possibilities of surgical revascularization. Stroke
6:17-20, 1975.
13. Dyken ML, Klatte E, Kolar OJ, et al: Complete occlusion of common or internal carotid arteries: Clinical significance. Arch Neurol
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14. Anderson CA, Rich NM, Collins GJ Jr, et al: Unilateral internal carotid arterial occlusion: Special considerations. Stroke 8:669-671, 1977. 15. Toole JF, Janeway R, Choi K, et al: Transient ischemic attacks due to arteriosclerosis. Arch Neurol 32:5-12, 1975. 16. Fields WS, Lemak NA: Joint study of extracranial arterial occlusion: X. Internal carotid artery occlusion. JAMA 235:2734-2738, 1976. 17. Hardy WG, Lindner DW, Thomas LM, et al: Anticipated clinical course in carotid artery occlusion. Arch Neurol 6:64-76, 1962. 18. Whisnant J, Matsumoto N, Elvebeck LE: Transient cerebral ischemic attacks in Rochester, Minnesota 1945-1969. Mayo Clin Proc 48:194-198, 1973. 19. Chater N, Peters N: Neurosurgical microvascular bypass for stroke. West J Med 124:1-5, 1976. 20. Chater N, Mani J, Tonnemacher K: Superficial temporal artery bypass in occlusive cerebral vascular disease. Calif Med 119:9-13, 1973. 21. Fields WS: Selection of stroke patients for arterial reconstructive surgery. Am J Surg 125:527-529, 1973. 22. Barnett HJM, Peerless SJ, Wei M: The "stump" of the internal carotid artery: A source for further cerebral embolic ischemia, abstracted. Stroke 8:14, 1977. 23. Austin G, Laffin D, Hayward W: Physiologic factors in the selection of patients for superficial temporal artery to middle cerebral artery anastomosis. Surgery 75:861-868, 1974. 24. Schmiedek P, Gratzl O, Spetzler R, et al: Selection of patients for extracranial-intracranial arterial bypass surgery based on rCBF measurements. J Neurosurg 44:303-312, 1976. 25. Heilbrun MP, Reichman OH, Anderson RE, et al: Regional cerebral blood flow studies following superficial temporal-middle cerebral artery anastomosis. J Neurosurg 43:706-716, 1975.
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