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Middle cerebral artery stenosis—a neglected problem?
44
Surg Neurol 1987;27:44-6
Middle Cerebral Artery Stenosisma Neglected Problem? James F. Toole, M.D. Bowman Gray School of Medicine, Winston-Salem, North Carolina
Toole JF. Middle cerebral artery stenosis--a neglected problem? Surg Neurol 1987;27:44-6.
Transcranial Doppler ultrasonography has great potential for clinical investigations that evaluate flow through the middle cerebral artery in health and disease. This technique will help to elucidate the syndromes of middle cerebral artery stenosis and occlusion, which have been overshadowed by the syndromes of internal carotid artery disease in the past. Middle cerebral artery stenosis; Transcranial Doppler ultrasonography KEY WORDS:
Recent efforts in the prevention of stroke have emphasized diagnosis and management of extracranial arterial atherosclerosis, particularly at the carotid bifurcation. This has overshadowed a less common, but nevertheless important entity--middle cerebral artery stenosis (MCAS), which may occur separately or in conjunction with carotid artery disease. Revived interest in MCAS and the desire to ascertain its presence arise from new diagnostic techniques, particularly transcranial Doppler ultrasound, which can assess disease in the preclinical stage after which risk factor reduction or prophylactic intervention can be undertaken. The advent of transcranial Doppler evaluations of the middle cerebral artery (MCA), along with the prospect of using plasminogen activator for lysis of clot in the MCA, raises the exciting possibility that an emergency approach to diagnosis and aggressive management may lead to salvage of some patients who may be devastated by this catastrophe. However, the prerequisite for identification of symptomatic MCAS is its differentiation from the syndrome of the carotid artery itself. Prior to the introduction of arteriography, it was fashionable to attribute infarction in the distribution of the MCA to occlusion of that artery rather than to internal carotid artery (ICA) disease. Now the emphasis has shifted so much that carotid artery Address reprint requests to: James F. Toole, M.D., Department of Neurology, Bowman Gray School of Medicine, Winston-Salem, North Carolina 27103.
© 1987 by Elsevier Science Publishing Co., Inc.
occlusion or thromboembolism from bifurcation disease to the distal arterial bed is considered to be the usual cause of MCA territory transient ischemic attack (TIA) and infarction--a logical but not necessarily correct conclusion if angiography demonstrates carotid bifurcation disease. Autopsy of Caucasians from different cultures and ethnic groups reveals a low prevalence of isolated stenosis or occlusion of the MCA. Most are the result of embolism from the heart or its valves, or are tandem lesions occurring in association with carotid bifurcation atherosclerosis. Lhermitte et al [ 13], in postmortem examinations of 47 patients with MCA territory infarction found ICA occlusion in 20 (40%); in 10 patients (20%) both the MCA and ICA were normal suggesting embolism from the heart; solitary MCA atherosclerosis was present in only two (4%) of the total number of patients. Reliable information regarding how frequently MCAS (not occlusion) results in symptoms or signs in Caucasians does not exist. There are several important reasons for this deficiency: 1. Homolateral visual phenomena need not occur in ICA disease--with the result that ICA and MCA syndromes can be identical. 2. Customary angiography of MCA is inexact because it does not include magnification and multiple projections. 3. Pathoanatomic studies to determine the degree of stenosis in distinction to occlusion are not performed in the usual autopsy. In considering atherosclerosis, it is essential to keep in mind the distinction between morphologic alteration in the arterial wall and clinical symptoms resulting therefrom. Pathologically, the early stages of atherosclerosis in the carotid artery or the MCA are much the same. Even though they may differ metabolically, both evolve into a fibrous plaque which begins to intrude upon the arterial lumen resulting in progressive disturbance of laminar flow. Moossy [16], whose work on the subject is definitive, pointed out that calcification of intracranial arterial lesions is rare except at the carotid siphon. Most importantly, complicated lesions such as ulceration, subintimal hemorrhage, or atherothrombosis are rare in intracranial arterial plaques. Ulceration with distal em0090-3019/87/$3.50
Middle Cerebral Artery Stenosis
bolization, as occurs from lesions of the carotid bifurcation, was seen only once in his series and that was in a plaque in the extracranial vertebral artery, the fatty contents of which had occluded the lumen of the artery a few millimeters distally. This rarity stands in sharp contrast to the frequency of distal atherothrombotic emboli from carotid plaques and the occurrence of ulceration, thrombosis, and subintimal hemorrhage at the carotid sinus. Baker and Iannone [3] found in 173 dissections of the circle of Willis that, regardless of age or sex, atherosclerotic plaques most frequently involved the internal carotid bifurcation, the upper basilar at the origins of the posterior cerebral arteries, and, next in frequency, the middle and lower parts of the basilar artery and the MCAs followed by the vertebral, posterior cerebral, and cerebeUar arteries. Sadoshima et al [ 19], in their reports from Hisayama, Japan, noted the frequency of lacunar infarcts and the relative rarity of MCA and ICA lesions. This contrasts with the proportions found in Caucasians as typified by the Harvard Stroke registry [15]. Why does this apparent racial predisposition exist and why does atherosclerotic plaque repeatedly locate in certain positions along the course of these arteries? Some suggested reasons are hypertension, flow dynamics, or tethering of the artery which anchors certain segments. In youth, the artery changes caliber as much as 20% during the cardiac cycle, reducing to 8% during adult life and usually becoming a rigid pipe during senescence. There is no evidence to suggest that hypertension, per se, results in MCAS but it stands to reason that in patients with MCAS, hypertension will result in better perfusion of the distal vascular bed. The correlative is that reduction of arterial hypertension to normotension in such groups may result in cerebrovascular insufficiency, a point which in the future will undoubtedly be addressed using transcranial Doppler interrogation of MCA flow before and after treatment. Epidemiology Heyman et al [9] reported an analysis of 5593 white and 911 black patients in which blacks were found to have greater prevalence of intracranial arterial disease and cerebral infarction than the whites, but a lower incidence of TIAs, thus suggesting that intracranial arterial disease seldom causes TIAs. Gorelick et al [8] observed no significant difference in prevalence of hypertension, diabetes mellitus, hypercholesterolemia, or ischemic heart disease in their report of MCA occlusion in these two racial groups. Therefore, these authors hypothesize that as yet unknown factors must account for the observed difference in the rate of occurrence of MCA occlusion between the two groups. In another publication, Caplan and associates [5] again pointed out that patients with
Surg Neurol 1987;27:44-6
45
MCA disease are more often black, female, and young and have fewer TIAs than those with ICA disease. Surprisingly, in some of their cases, the MCA syndrome did not always express itself completely from the beginning but evolved slowly over days or even weeks. Furthermore, in their experience all MCA occlusions develop infarction, but 40% of the patients with ICA disease do not. Nishimaru et al [ 18] describe a comparative study of cerebral angiographic findings in 32 Japanese patients with carotid system TIAs compared with age- and sexmatched Caucasians from North Carolina. Although atherosclerotic changes were present in equal numbers of both races, with mild lesions being similar in topography and frequency of occurrence both extracranially and intracranially, there was a striking disproportion in those with severe lesions-- 10 of 12 were located intracranially in the Japanese patients, whereas 17 of 20 were located extracranially in the carotid bifurcation in the Caucasians. This apparent racial difference in the distribution of disease is commonly attributed to hypertension and dietary factors, particularly intake of animal fats, but in truth, the reasons are not known. Other disorders that are associated with MCAS are moyamoya disease, spontaneous or posttraumatic MCA dissection, fibromuscular dysplasia, postradiation angiopathy, and the poorly understood arteritis caused by oral contraceptives and amphetamines. Each must be considered in the differential diagnosis of patients with isolated intracranial arterial disease. Ultrasound Transcranial Doppler ultrasonography, utilizing a 2-mHz pulsed focused transducer, and B-mode ultrasound are being utilized for intracranial interrogation of arteries [10-12] through the temporal bone orbit and foramen magnum. These techniques have exciting possibilities for gathering further information relevant to normal function and disease of all the large caliber intracranial arteries. Prognosis Hinton et al [10], in their consideration of 16 medically managed patients with angiographically demonstrated MCAS found that with anticoagulants the prognosis was remarkably good. Furthermore, they suggested that carotid artery stenosis "protects" the intracranial vessels from the effects of hypertension, and concluded that MCAS is "benign" when treated medically. This viewpoint is confirmed by Feldmeyer et al [7], who hypothesized that anticoagulants and platelet antiaggregants prevent distal microemboli. However, Corston et al [6] report an opposite experience among their 21 patients
46
Surg Neurol 1987;27:44-6
with angiographically demonstrated MCAS, 14 of whom presented with cerebral infarction and 7 with transient ischemic attacks. O f the former, four patients had further infarction (three fatal); of the latter, one had a fatal infarction. Only 2 of the 21 had TIAs during the followup period. Their study indicates that the prognosis for patients with MCAS is worse than the literature suggests. Moulin et al [17] have reported that of 24 patients with MCA syndrome and occlusion, eight died or were severely disabled during the acute phase. Nineteen were followed-up for a mean of 54 months with five deaths, two from cerebral infarction. O f the survivors 63% remained completely functional. Lascelles and Burrows [12] found that 2 0 % of patients die during the acute phase and that an occasional patient will recover completely. This contrasts with the report of Kaste and Waltimo [11], who found a mortality of 5%. However, angiographic demonstration of occlusion of the MCA has been shown by Sindermann et al [20] to be followed by spontaneous recanalization of the artery in more than 24%. Summary Middle cerebral artery stenosis has been an enigmatic disorder overshadowed by diagnostic and therapeutic interest in carotid artery syndrome from which it can be indistinguishable. Recently, the advent of transcranial Doppler ultrasound has made it possible to measure flow through the MCA both in health and disease. For example, it is suspected but not known that plaques intruding into the lumen causing stenosis can regress as well as progress so that a hemodynamic lesion with proper management may become nonhemodynamic. This will be elucidated now that we have a tool for longitudinal study of the artery. Furthermore, whether stenosis with reduction of distal perfusion pressure, i.e., a hemodynamic lesion will result in diminished reserve such that changes in the contents of the blood stream as might occur with hypoxia, hyperglycemia, or hypoglycemia might render the distal brain tissue more vulnerable than the remainder, can be approached [20]. This concept is worthy of reconsideration in the light of new technology which permits more precision in its delineation. It is apparent that we do not know the significance of MCAS because we do not know its prevalence, we cannot clearly separate its clinical characteristics from that of carotid syndromes, and we have not, until recently, had proper diagnostic methods for detecting its presence or tracking its course. Now that we have methodology, answers should be forthcoming. Finally, there is the exciting area of clot lysis, which is so far advanced for coronary artery disease but still almost unexplored in cerebrovascular disease.
Toole
References 1. Aaslid R, Huber P, Nornes H. Evaluation of cerebrovascular spasm with transcranial Doppler ultrasound. J Neurosurg 1984;60:37-41. 2. Aaslid R, Markwalder T, Nornes H. Noninvasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries. J Neurosurg 1982;57:769-74. 3. Baker AB, Iannone A. Cerebrovascular disease. I. The large arteries of the circle of Willis. Neurology 1959;9:321-32. 4. Bishop C, Insall M, Powell S, Rutt D, Browse N. Effect of internal carotid artery occlusion on middle cerebral artery blood flow at rest and in response to hypercapnia. Lancet 1986;i:710-2. 5. Caplan L, Babikian V, Helgason C, Hier DB, DeWitt D, Patel D, Stein R. Occlusive disease of the middle cerebral artery. Neurology 1985;35:975-82. 6. Corston R, Kendall B, Marshall J. Prognosis in middle cerebral artery stenosis. Stroke 1984;15:237-41. 7. Feldmeyer J, Merendez C, Regli F. Stenoses symptomatiques de l'artere cerebrale moyenne. Rev Neurol (Paris) 1983;139:725-36. 8. Gorelick PB, Caplan LR, Hier DB, Parker SL, Patel D. Racial differences in the distribution of anterior circulation occlusive disease. Neurology 1984;34:54-9. 9. Heyman A, Fields WS, Keating RD. Joint study of extracranial arterial occlusion. Vl. Racial differences in hospitalized patients with ischemic stroke. JAMA 1972;222:285-9. 10. Hinton RC, Mohr JP, Ackerman RH, Adair LB, Fisher CM. Symptomatic middle cerebral artery stenosis. Ann Neurol 1979;5:152-7. l l. Kaste M, Waltimo O. Prognosis of patients with middle cerebral artery occlusion. Stroke 1976;7:482-5. 12. Lascelles RG, Burrows EH. Occlusion of the middle cerebral artery. Brain 1965;88:85-96. 13. Lhermitte F, Gautier JC, Derouesne C. Nature of occlusions of the middle cerebral artery. Neurology 1970;20:82-6. 14. Lindegaerd K, Bakke S, Grolimund P, Aaslid R, et al. Assessment of intracranial hemodynamics in carotid artery disease by transcranial Doppler ultrasound. J Neurosurg 1985;63:890-8. 15. Mohr J, Caplan L, MelskiJ, Duncan G, et al. The Harvard Stroke Registry: a prospective registry of cases hospitalized with stroke. Neurology 1978;28:754-63. 16. Moossy J. Cerebral atherosclerosis: intracranial and extracranial lesions. In: MincklerJ, ed. Pathology of the nervous system. New York: McGraw Hill, 1968:1423-32. 17. Moulin D, Lo R, Chiang J, Barnett H. Prognosis in middle cerebral artery occlusion. Stroke 1985;16:282-4. 18. Nishimaru K, McFIenry L, Toole J. Cerebral angiographic and clinical differences in carotid system transient ischemic attacks between American Caucasians and Japanese patients. Stroke 1984;15:56-9. 19. Sadoshima S, Kurozumi T, Tanaka K, Ueda K, et al. Cerebral and aortic atherosclerosis in Hisayama, Japan. Atherosclerosis 1980;36:117-26. 20. Sindermann F, Dichgans J, Bergleiter R. Occlusion of the middle cerebral artery and its branches: angiographic and clinical correlates. Brain 1969;92:607-20.
Editor's N o t e : After reading some of the author's comments on the subject of middle cerebral artery stenosis, I asked him to prepare this special articlefor SURGICAL NEUROLOGY. Dr. Toole's long-time involvement in this field and his unique ability to synthesize a vast wealth of material into a short article make this contribution of considerable value to neurosurgeons. EBEN A L E X A N D E R , Jr., Editor
Surg Neurol 1987;27:44-6
Middle Cerebral Artery Stenosisma Neglected Problem? James F. Toole, M.D. Bowman Gray School of Medicine, Winston-Salem, North Carolina
Toole JF. Middle cerebral artery stenosis--a neglected problem? Surg Neurol 1987;27:44-6.
Transcranial Doppler ultrasonography has great potential for clinical investigations that evaluate flow through the middle cerebral artery in health and disease. This technique will help to elucidate the syndromes of middle cerebral artery stenosis and occlusion, which have been overshadowed by the syndromes of internal carotid artery disease in the past. Middle cerebral artery stenosis; Transcranial Doppler ultrasonography KEY WORDS:
Recent efforts in the prevention of stroke have emphasized diagnosis and management of extracranial arterial atherosclerosis, particularly at the carotid bifurcation. This has overshadowed a less common, but nevertheless important entity--middle cerebral artery stenosis (MCAS), which may occur separately or in conjunction with carotid artery disease. Revived interest in MCAS and the desire to ascertain its presence arise from new diagnostic techniques, particularly transcranial Doppler ultrasound, which can assess disease in the preclinical stage after which risk factor reduction or prophylactic intervention can be undertaken. The advent of transcranial Doppler evaluations of the middle cerebral artery (MCA), along with the prospect of using plasminogen activator for lysis of clot in the MCA, raises the exciting possibility that an emergency approach to diagnosis and aggressive management may lead to salvage of some patients who may be devastated by this catastrophe. However, the prerequisite for identification of symptomatic MCAS is its differentiation from the syndrome of the carotid artery itself. Prior to the introduction of arteriography, it was fashionable to attribute infarction in the distribution of the MCA to occlusion of that artery rather than to internal carotid artery (ICA) disease. Now the emphasis has shifted so much that carotid artery Address reprint requests to: James F. Toole, M.D., Department of Neurology, Bowman Gray School of Medicine, Winston-Salem, North Carolina 27103.
© 1987 by Elsevier Science Publishing Co., Inc.
occlusion or thromboembolism from bifurcation disease to the distal arterial bed is considered to be the usual cause of MCA territory transient ischemic attack (TIA) and infarction--a logical but not necessarily correct conclusion if angiography demonstrates carotid bifurcation disease. Autopsy of Caucasians from different cultures and ethnic groups reveals a low prevalence of isolated stenosis or occlusion of the MCA. Most are the result of embolism from the heart or its valves, or are tandem lesions occurring in association with carotid bifurcation atherosclerosis. Lhermitte et al [ 13], in postmortem examinations of 47 patients with MCA territory infarction found ICA occlusion in 20 (40%); in 10 patients (20%) both the MCA and ICA were normal suggesting embolism from the heart; solitary MCA atherosclerosis was present in only two (4%) of the total number of patients. Reliable information regarding how frequently MCAS (not occlusion) results in symptoms or signs in Caucasians does not exist. There are several important reasons for this deficiency: 1. Homolateral visual phenomena need not occur in ICA disease--with the result that ICA and MCA syndromes can be identical. 2. Customary angiography of MCA is inexact because it does not include magnification and multiple projections. 3. Pathoanatomic studies to determine the degree of stenosis in distinction to occlusion are not performed in the usual autopsy. In considering atherosclerosis, it is essential to keep in mind the distinction between morphologic alteration in the arterial wall and clinical symptoms resulting therefrom. Pathologically, the early stages of atherosclerosis in the carotid artery or the MCA are much the same. Even though they may differ metabolically, both evolve into a fibrous plaque which begins to intrude upon the arterial lumen resulting in progressive disturbance of laminar flow. Moossy [16], whose work on the subject is definitive, pointed out that calcification of intracranial arterial lesions is rare except at the carotid siphon. Most importantly, complicated lesions such as ulceration, subintimal hemorrhage, or atherothrombosis are rare in intracranial arterial plaques. Ulceration with distal em0090-3019/87/$3.50
Middle Cerebral Artery Stenosis
bolization, as occurs from lesions of the carotid bifurcation, was seen only once in his series and that was in a plaque in the extracranial vertebral artery, the fatty contents of which had occluded the lumen of the artery a few millimeters distally. This rarity stands in sharp contrast to the frequency of distal atherothrombotic emboli from carotid plaques and the occurrence of ulceration, thrombosis, and subintimal hemorrhage at the carotid sinus. Baker and Iannone [3] found in 173 dissections of the circle of Willis that, regardless of age or sex, atherosclerotic plaques most frequently involved the internal carotid bifurcation, the upper basilar at the origins of the posterior cerebral arteries, and, next in frequency, the middle and lower parts of the basilar artery and the MCAs followed by the vertebral, posterior cerebral, and cerebeUar arteries. Sadoshima et al [ 19], in their reports from Hisayama, Japan, noted the frequency of lacunar infarcts and the relative rarity of MCA and ICA lesions. This contrasts with the proportions found in Caucasians as typified by the Harvard Stroke registry [15]. Why does this apparent racial predisposition exist and why does atherosclerotic plaque repeatedly locate in certain positions along the course of these arteries? Some suggested reasons are hypertension, flow dynamics, or tethering of the artery which anchors certain segments. In youth, the artery changes caliber as much as 20% during the cardiac cycle, reducing to 8% during adult life and usually becoming a rigid pipe during senescence. There is no evidence to suggest that hypertension, per se, results in MCAS but it stands to reason that in patients with MCAS, hypertension will result in better perfusion of the distal vascular bed. The correlative is that reduction of arterial hypertension to normotension in such groups may result in cerebrovascular insufficiency, a point which in the future will undoubtedly be addressed using transcranial Doppler interrogation of MCA flow before and after treatment. Epidemiology Heyman et al [9] reported an analysis of 5593 white and 911 black patients in which blacks were found to have greater prevalence of intracranial arterial disease and cerebral infarction than the whites, but a lower incidence of TIAs, thus suggesting that intracranial arterial disease seldom causes TIAs. Gorelick et al [8] observed no significant difference in prevalence of hypertension, diabetes mellitus, hypercholesterolemia, or ischemic heart disease in their report of MCA occlusion in these two racial groups. Therefore, these authors hypothesize that as yet unknown factors must account for the observed difference in the rate of occurrence of MCA occlusion between the two groups. In another publication, Caplan and associates [5] again pointed out that patients with
Surg Neurol 1987;27:44-6
45
MCA disease are more often black, female, and young and have fewer TIAs than those with ICA disease. Surprisingly, in some of their cases, the MCA syndrome did not always express itself completely from the beginning but evolved slowly over days or even weeks. Furthermore, in their experience all MCA occlusions develop infarction, but 40% of the patients with ICA disease do not. Nishimaru et al [ 18] describe a comparative study of cerebral angiographic findings in 32 Japanese patients with carotid system TIAs compared with age- and sexmatched Caucasians from North Carolina. Although atherosclerotic changes were present in equal numbers of both races, with mild lesions being similar in topography and frequency of occurrence both extracranially and intracranially, there was a striking disproportion in those with severe lesions-- 10 of 12 were located intracranially in the Japanese patients, whereas 17 of 20 were located extracranially in the carotid bifurcation in the Caucasians. This apparent racial difference in the distribution of disease is commonly attributed to hypertension and dietary factors, particularly intake of animal fats, but in truth, the reasons are not known. Other disorders that are associated with MCAS are moyamoya disease, spontaneous or posttraumatic MCA dissection, fibromuscular dysplasia, postradiation angiopathy, and the poorly understood arteritis caused by oral contraceptives and amphetamines. Each must be considered in the differential diagnosis of patients with isolated intracranial arterial disease. Ultrasound Transcranial Doppler ultrasonography, utilizing a 2-mHz pulsed focused transducer, and B-mode ultrasound are being utilized for intracranial interrogation of arteries [10-12] through the temporal bone orbit and foramen magnum. These techniques have exciting possibilities for gathering further information relevant to normal function and disease of all the large caliber intracranial arteries. Prognosis Hinton et al [10], in their consideration of 16 medically managed patients with angiographically demonstrated MCAS found that with anticoagulants the prognosis was remarkably good. Furthermore, they suggested that carotid artery stenosis "protects" the intracranial vessels from the effects of hypertension, and concluded that MCAS is "benign" when treated medically. This viewpoint is confirmed by Feldmeyer et al [7], who hypothesized that anticoagulants and platelet antiaggregants prevent distal microemboli. However, Corston et al [6] report an opposite experience among their 21 patients
46
Surg Neurol 1987;27:44-6
with angiographically demonstrated MCAS, 14 of whom presented with cerebral infarction and 7 with transient ischemic attacks. O f the former, four patients had further infarction (three fatal); of the latter, one had a fatal infarction. Only 2 of the 21 had TIAs during the followup period. Their study indicates that the prognosis for patients with MCAS is worse than the literature suggests. Moulin et al [17] have reported that of 24 patients with MCA syndrome and occlusion, eight died or were severely disabled during the acute phase. Nineteen were followed-up for a mean of 54 months with five deaths, two from cerebral infarction. O f the survivors 63% remained completely functional. Lascelles and Burrows [12] found that 2 0 % of patients die during the acute phase and that an occasional patient will recover completely. This contrasts with the report of Kaste and Waltimo [11], who found a mortality of 5%. However, angiographic demonstration of occlusion of the MCA has been shown by Sindermann et al [20] to be followed by spontaneous recanalization of the artery in more than 24%. Summary Middle cerebral artery stenosis has been an enigmatic disorder overshadowed by diagnostic and therapeutic interest in carotid artery syndrome from which it can be indistinguishable. Recently, the advent of transcranial Doppler ultrasound has made it possible to measure flow through the MCA both in health and disease. For example, it is suspected but not known that plaques intruding into the lumen causing stenosis can regress as well as progress so that a hemodynamic lesion with proper management may become nonhemodynamic. This will be elucidated now that we have a tool for longitudinal study of the artery. Furthermore, whether stenosis with reduction of distal perfusion pressure, i.e., a hemodynamic lesion will result in diminished reserve such that changes in the contents of the blood stream as might occur with hypoxia, hyperglycemia, or hypoglycemia might render the distal brain tissue more vulnerable than the remainder, can be approached [20]. This concept is worthy of reconsideration in the light of new technology which permits more precision in its delineation. It is apparent that we do not know the significance of MCAS because we do not know its prevalence, we cannot clearly separate its clinical characteristics from that of carotid syndromes, and we have not, until recently, had proper diagnostic methods for detecting its presence or tracking its course. Now that we have methodology, answers should be forthcoming. Finally, there is the exciting area of clot lysis, which is so far advanced for coronary artery disease but still almost unexplored in cerebrovascular disease.
Toole
References 1. Aaslid R, Huber P, Nornes H. Evaluation of cerebrovascular spasm with transcranial Doppler ultrasound. J Neurosurg 1984;60:37-41. 2. Aaslid R, Markwalder T, Nornes H. Noninvasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries. J Neurosurg 1982;57:769-74. 3. Baker AB, Iannone A. Cerebrovascular disease. I. The large arteries of the circle of Willis. Neurology 1959;9:321-32. 4. Bishop C, Insall M, Powell S, Rutt D, Browse N. Effect of internal carotid artery occlusion on middle cerebral artery blood flow at rest and in response to hypercapnia. Lancet 1986;i:710-2. 5. Caplan L, Babikian V, Helgason C, Hier DB, DeWitt D, Patel D, Stein R. Occlusive disease of the middle cerebral artery. Neurology 1985;35:975-82. 6. Corston R, Kendall B, Marshall J. Prognosis in middle cerebral artery stenosis. Stroke 1984;15:237-41. 7. Feldmeyer J, Merendez C, Regli F. Stenoses symptomatiques de l'artere cerebrale moyenne. Rev Neurol (Paris) 1983;139:725-36. 8. Gorelick PB, Caplan LR, Hier DB, Parker SL, Patel D. Racial differences in the distribution of anterior circulation occlusive disease. Neurology 1984;34:54-9. 9. Heyman A, Fields WS, Keating RD. Joint study of extracranial arterial occlusion. Vl. Racial differences in hospitalized patients with ischemic stroke. JAMA 1972;222:285-9. 10. Hinton RC, Mohr JP, Ackerman RH, Adair LB, Fisher CM. Symptomatic middle cerebral artery stenosis. Ann Neurol 1979;5:152-7. l l. Kaste M, Waltimo O. Prognosis of patients with middle cerebral artery occlusion. Stroke 1976;7:482-5. 12. Lascelles RG, Burrows EH. Occlusion of the middle cerebral artery. Brain 1965;88:85-96. 13. Lhermitte F, Gautier JC, Derouesne C. Nature of occlusions of the middle cerebral artery. Neurology 1970;20:82-6. 14. Lindegaerd K, Bakke S, Grolimund P, Aaslid R, et al. Assessment of intracranial hemodynamics in carotid artery disease by transcranial Doppler ultrasound. J Neurosurg 1985;63:890-8. 15. Mohr J, Caplan L, MelskiJ, Duncan G, et al. The Harvard Stroke Registry: a prospective registry of cases hospitalized with stroke. Neurology 1978;28:754-63. 16. Moossy J. Cerebral atherosclerosis: intracranial and extracranial lesions. In: MincklerJ, ed. Pathology of the nervous system. New York: McGraw Hill, 1968:1423-32. 17. Moulin D, Lo R, Chiang J, Barnett H. Prognosis in middle cerebral artery occlusion. Stroke 1985;16:282-4. 18. Nishimaru K, McFIenry L, Toole J. Cerebral angiographic and clinical differences in carotid system transient ischemic attacks between American Caucasians and Japanese patients. Stroke 1984;15:56-9. 19. Sadoshima S, Kurozumi T, Tanaka K, Ueda K, et al. Cerebral and aortic atherosclerosis in Hisayama, Japan. Atherosclerosis 1980;36:117-26. 20. Sindermann F, Dichgans J, Bergleiter R. Occlusion of the middle cerebral artery and its branches: angiographic and clinical correlates. Brain 1969;92:607-20.
Editor's N o t e : After reading some of the author's comments on the subject of middle cerebral artery stenosis, I asked him to prepare this special articlefor SURGICAL NEUROLOGY. Dr. Toole's long-time involvement in this field and his unique ability to synthesize a vast wealth of material into a short article make this contribution of considerable value to neurosurgeons. EBEN A L E X A N D E R , Jr., Editor