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Thrombotic Occlusion of the Middle Cerebral Artery Shinsuke Ueda, MD; Kazuhiko Fujitsu, MD; Shigeo Inomori, MD; and Takeo Kuwabara, MD Background and Purpose: Epidemiological study of middle cerebral artery occlusion is important because the indication for extracranial-intracranial arterial bypass remains in dispute. To help clarify this issue, we investigated the prognosis of thrombotic middle cerebral artery occlusion in Japanese patients. Methods: We studied 40 patients with thrombotic middle cerebral artery occlusion who were selected on the basis of clinical features, computed tomographic findings, and angiographic findings. Patients with causes of embolism (i.e., cardiomyopathy, valvular heart disease, cardiac arrhythmia, and carotid ulceration) were excluded. The 40 patients were classified into three groups according to the site of middle cerebral artery occlusion: there were 13 patients with occlusion of the proximal portion of the Ml segment, 13 with distal Ml segment occlusion, and 14 with occlusion of the M2 segment. Results: Good collateral circulation was associated with improved outcomes both clinically and by computed tomography in patients with occlusion of the proximal and distal portions of the Ml segment but not in those with M2 occlusion. Conclusions: It is reasonable to assume that not only collateral circulation but also the site of occlusion plays an important role in the outcome of middle cerebral artery occlusion. Our finding that good collateral circulation improves the outcome for thrombotic occlusion of the proximal and distal Ml segments supports the possible benefits of such surgery. (Stroke 1992;23:1761-1766) KEY WORDS • arterial occlusive diseases • cerebral infarction • collateral circulation • thrombosis
E
pidemiological study of middle cerebral artery (MCA) occlusion has become increasingly important because review of the literature suggests that the indication for extracranial-intracranial arterial bypass surgery remains in dispute.1-3 Strict differentiation of thrombosis from embolus is especially important because the clinical course, neuroradiological findings, treatment, and prognosis may be different.4 Thrombosis is usually thought to have a less-sudden onset, to be less severe clinically, and to have a computed tomographic (CT) image of an irregular low density area (LDA) without midline shift.5 Embolic cerebral infarction as reported by the Harvard Cooperative Stroke Registry,6 Blackwood et al,7 and Jorgensen and Torvik8 had an incidence of 37%, 48%, and 47%, respectively. Although many authors 9 " 13 have emphasized atherosclerotic thrombosis as the most common cause of cerebral infarction, accounting for 80-95%, some1415 have found thrombotic etiology of MCA occlusion to be less frequent. In the Japanese population, MCA occlusion is 1.8 times more common than internal carotid artery (ICA) occlusion.16 In the American Joint Study of Extracranial Arterial Occlusion,17 MCA occlusion had one fourth the incidence of ICA occlusion. The reason for the etiologiFrom the Department of Neurosurgery, Yokohama City University, School of Medicine, Yokohama, Japan. Address for correspondence: Shinsuke Ueda, MD, Department of Neurosurgery, Yokohama Red Cross Hospital, 2-85, Negishicho, Naka-ku, Yokohama 231, Japan. Received October 29, 1990; final revision received July 6, 1992; accepted July 28, 1992.
cal dominance of embolus or thrombosis is controversial, but among the Japanese population thrombotic MCA occlusion appears to have a higher incidence. In this study we investigated the prognosis of thrombotic MCA occlusion in Japanese patients in relation to clinical features, CT findings, and angiographic findings. To assess collateral circulation, we determined the presence or absence of retrograde filling, that is, the presence or absence of contrast media in MCA branches through leptomeningeal anastomosis on angiography (within 6 seconds after injection). Subjects and Methods We studied 40 patients with MCA occlusion (mean age, 66.4 years [range, 42-84 years]; 27 men, 13 women) retrospectively. With diagnosis made by CT, angiographic, and clinical findings, patients who had atrial fibrillation on electrocardiogram or angiographic findings of atherosclerotic ICA ulceration regardless of the presence of ICA stenosis were excluded from this study. All patients were admitted within 48 hours of the ictus, and the initial CT scans were undertaken within 36 hours of admission. Angiography was performed within 4 days of admission. Angiograms were divided into the following three groups according to the site of occlusion: group A, occlusion of the proximal portion of the Ml segment; group B, occlusion of the distal portion of the Ml segment; and group C, occlusion of the M2 segment (Figure 1). We determined the presence or absence of retrograde filling, that is, the presence or absence of
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Proximal Ml occlusion
Distal Ml occlusion
M2 occlusion
FIGURE 1. Angiographic findings of middle cerebral artery occlusion were classified into three groups. Left panel: Occlusion of the proximal portion of the Ml segment (group A). Center panel: Occlusion of the distal portion of the Ml segment (group B). Right panel: Occlusion of the M2 segment (group C).
contrast media in MCA branches through leptomeningeal anastomoses with serial angiography. The presence or absence of angiographic retrograde filling was also analyzed. CT scans were classified into the following five categories: basal ganglia-centrum semiovale type, in which an LDA was localized in the basal ganglia and/or centrum semiovale; localized cortex-subcortical type, in which an LDA was localized in a small area of the cortex and subcortex of the frontal, temporal, or parietal lobe; lobular cortex-subcortical type, in which an LDA involved the cortex and subcortex of the frontal, temporal, and parietal lobes; hemispheric type, in which an LDA extended to one hemisphere including the basal ganglia; and normal type, in which an LDA was not found on CT (Figure 2). For the CT classification described above, CT scans that showed the maximum extent of LDA during repeated studies were selected. Degree of hemiparesis on admission was graded as mild, moderate, or severe using DeJong's definition,18 in which mild was defined as normal or movement against gravity and resistance, moderate was movement against gravity with resistance eliminated, and severe was partial movement with gravity eliminated, with a trace of muscle contraction. Outcomes were also graded: good outcome, full work and minimal disability, fair outcome, partial disability; and poor outcome, bed rest, vegetative state, or death. The follow-up period was from 43 days to 4 months (with the exception of four patients who died of complications). Correlations were made between the angiographic site of occlusion, retrograde filling, CT findings, degree of hemiparesis on admission, and outcome.
Results Occlusion of the MCA occurred on the left side in 24 patients and on the right in 16. Eleven of the 40 patients had hypertension and had been treated by antihypertensive medications. The prevalence of diabetes mellitus was 8% in this study. Mortality was 10%. At the onset of stroke, 22 patients (55%) had a mild disturbance of consciousness, but no patients were comatose. Mild hemiparesis was found in 14 patients, moderate hemiparesis in nine, and severe hemiparesis in 17. Two patients (5%) had a transient ischemic attack (TLA), and the remaining 38 patients had a complete stroke. Four patients (10%) had had previous ischemic events in the symptomatic side. Two of these four patients had TLA, and the remaining two had complete stroke. In 13 patients the MCA was occluded at the proximal portion of the Ml segment. Another 13 patients showed the MCA occluded at the distal portion of the Ml segment, and the remaining 14 had occlusion of the M2 segment. Two patients had mild ipsilateral ICA stenosis of less than 50%. The degree of hemiparesis of each patient on admission is indicated in Figure 3, in relation to the site of occlusion, retrograde filling, and CT findings. Figure 4 shows outcomes of the patients in relation to the site of occlusion, retrograde fining, and CT findings. All 13 patients with occlusion of the proximal Ml (group A) showed basal ganglia-centrum semiovale or hemispheric type findings on CT. Of seven patients with basal ganglia-centrum semiovale type findings on CT, six patients (86%) showed retrograde filling from the anterior cerebral artery (ACA), whereas of six patients
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Ueda et al
Basal ganglia -
Localized cortex-
centrum semiovale
Lobular c o r t e x -
subcortical
type
Thrombotic MCA Occlusion
subcortical
1763
Hemispheric type
type
type
FIGURE 2. Computed tomographic findings were classified into five categories (see text): basal ganglia-centrum semiovale type; localized cortex-subcortical type; lobular cortex-subcortical type; hemispheric type; and normal type (not shown).
with hemispheric type findings on CT only two (33%) showed retrograde filling. In the patients with occlusion of the distal Ml (group B), findings on CT were basal ganglia—centrum semiovale in four, localized cortexsubcortical in four, lobular cortex-subcortical in three,
hemispheric in one, and normal in one patient. The group B patients with basal ganglia-centrum semiovale type findings on CT showed an LDA in the centrum semiovale but not in the basal ganglia. In the patients with occlusion of the M2 (group C), findings on CT
N^lta of occluiion ProxiM (Sroui
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\ X l t a of occlusion
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were localized cortex-subcortical type in 10 and normal type in four patients (Figures 3 and 4). Most patients with severe hemiparesis showed lobular cortex-subcortical and hemispheric type findings on CT. Ah1 patients with normal type findings on CT showed mild hemiparesis, and most patients with basal ganglia-centrum semiovale or localized cortex-subcortical type findings on CT had moderate hemiparesis (Figure 3). The degree of hemiparesis on admission was well correlated to the CT findings. The outcome was rated good in 12 (30%), fair in eight (20%), and poor, including death, in 20 (50%) patients. Four patients (10%) died of complications at the acute stage of the disease. Outcomes of patients in group A and group B were poor. However, the outcome was better in patients in group A and group B with retrograde filling than in those without retrograde filling. Outcomes of patients in group C were generally good irrespective of the presence or absence of retrograde filling (Figure 4). Patients with occlusion of the distal MCA branches to the motor cortex, however, showed poor outcome. Discussion Most of the published studies19-24 on MCA occlusion have not excluded embolic occlusion. The differential diagnosis between thrombotic and embolic MCA occlusion may be difficult. To improve the reliability of the selection of thrombotic MCA occlusion, patients who had atrial fibrillation or carotid artery ulceration were excluded based on clinical features, CT findings, and angiographic findings.5 It has been reported frequently that embolic MCA occlusion is more common than thrombotic MCA occlusion14-23-26; Lhermitte et al15 found that only 12.5% of 40 MCA occlusions were due to local thrombosis. However, in the Japanese popula-
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tion thrombotic MCA occlusion is reported to be more common.13 In this study, the mean age of 66.4 was higher than that in other reports.15-21-22-27 The mortality rate of this series was essentially the same as that in the study of Bogousslavsky et al.27 Therefore, age did not have a significant influence on death.27 Male predominance was noted in this series, as in other reports.27-28 Allcock19 reported no laterality of the side of the lesion, although others have reported left side predominance.21 In this series we reported no laterality of the lesion. In our patients, 18 of 40 (45%) had hypertension, and three (8%) had diabetes mellitus resulting in hypertension. Hypertension is an important risk factor in thrombotic MCA occlusion. This finding agrees with other reports.27-29 TLA has been defined as a temporary, focal neurological deficit presumably related to ischemia, lasting less than 24 hours. Only two patients presented with TLA; the remaining 38 patients presented with complete stroke. Caplan et al30 and Sindermann et al24 reported that TLA, as an initial symptom, was more frequently observed in ICA occlusion than in MCA occlusion. Thrombotic MCA occlusion has a more benign effect than embolic MCA occlusion,4-20-31-32 perhaps because the development of collateral circulation is better in gradual thrombotic occlusion than in sudden embolic occlusion. Therefore, although disturbance of consciousness was found in 21 patients (53%), severe disturbance of consciousness as occurs in the case of embolic occlusion was not observed. In group A, most patients with good retrograde filling showed basal ganglia-centrum semiovale type findings on CT, whereas four of five patients without retrograde filling showed hemispheric type findings on CT (Figures 3 and 4). We offer two possible explanations for the fact that basal ganglia-centrum semiovale type findings oc-
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Thrombotic MCA Occlusion
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botic occlusion of the proximal and distal Ml segments supports the possible benefits of such surgery. Acknowledgments We thank Drs. Ilu Kim, Masaharu Oda, and Akihito Saito for referring patients into this study. FIGURE 5. Left panel: Collateral circulation from anterior cerebral artery (ACA) may not supply basal ganglia because perforators of Ml segment are most distal to collateral circulation. Center panel: Atherosclerotic changes may involve origin of perforators. Right panel: Paraventricular zone may be supplied by medullary branches (arrows) rising from distal middle cerebral artery (MCA). See text for further discussion.
curred in group A patients. First, retrograde filling from the ACA may not supply the basal ganglionic area that is most distant to the collateral circulation (Figure 5, left panel). The other possible explanation, already discussed by some authors,29-33 is that the atherosclerotic change may extend to the origins of the perforators (Figure 5, center panel). Deep perforators from the ACA supply the basal ganglia, but they did not appear to be related to the size of the deep basal ganglionic infarcts in group A. Outcomes were worse in patients with hemispheric type findings than in patients with basal ganglia-centrum semiovale type findings. In addition to CT findings, presence or absence of retrograde filling appears to affect the outcome and degree of hemiparesis in group A patients. Krayenbuhl and Yasargil,34 Fisher et al,14 and Saito et al29 found that the amount of collateral circulation was intimately related to final outcome. In contrast, Sindermann et al24 noted no correlation between collateral circulation and outcome. In our series, collateral circulation was found to affect outcome in group A and group B patients but not in group C patients. It is reasonable to assume that not only collateral circulation but also the site of occlusion plays an important role in the outcome of MCA occlusion. Taking MCA distribution into consideration, it is understandable that most of the patients in group B showed localized cortex-subcortical or lobular cortexsubcortical type findings on CT. However, basal gangliacentrum semiovale type findings on CT were also shown in four patients in group B. LDAs in these four patients were found in the centrum semiovale but not in the basal ganglia. These findings suggest that the centrum semiovale in these patients was supplied by the medullary branches rising from the distal MCA (Figure 5, right panel). Patients in group C showed either localized cortex-subcortical or normal type findings on CT. No ischemic events recurred in this series, probably because of the short duration of the follow-up period (from 43 days to 4 months). According to Bogousslavsky et al,27 ischemic events during the follow-up period (35-72 months) recurred in only 10% of the patients with isolated MCA occlusion. Therefore, surgical indication for revascularization after thrombotic MCA occlusion should be determined carefully in the chronic stage. If surgical revascularization is regarded as the construction of an artificial collateral circulation, our finding that good collateral circulation improves the outcome for throm-
References 1. Arthur LD: Indication for surgical intervention in middle cerebral artery ocdusion. / Neuwsurg 1984;60:296-304 2. EC/IC Bypass Study Group: Cooperative Study of Extracranial/ Intracranial Arterial Anastomosis (EC/IC Bypass Study): Methodology and entry characteristics. Stroke 1985;16:397-4O6 3. EC/IC Bypass Study Group: Failure of extracranial-intracranial arterial bypass to reduce the risk of ischemic stroke: Result of an international randomized trial. N Engl J Med 1985;313:1191-1200 4. Fukada N, Kogure T, Ogawa A, Yoshimoto T, Suzuki J: Clinical course and prognosis of middle cerebral artery occlusion in the acute stage. Jpn J Stroke 1985;7:425-432 5. Tomura N, Inugami A, Kanno I, Higano S, Fijita H, Tabata K, Shishido F, Uemura K, Abe T: Differentiation between cerebral embolism and thrombosis on sequential CT scans. J Comput Assist Tomogr 1990;14:26-31 6. Mohr JP, Caplan LR, Melski JW, Goldstein RJ, Duncan GW, Kistler JP, Pessin MS, Bleich HL: The Harvard Cooperative Stroke Registry: A prospective registry. Neurology 1978^8:754-762 7. Blackwood W, Hallpike JF, Kocen RS, Mair WGP: Atheromatous disease of the carotid arterial system and embolism from the heart in cerebral infarction: A morbid anatomical study. Brain 1969;92; 897-910 8. Jorgensen L, Torvik A: Ischemic cerebrovascular disease in an autopsy series: Part 1. Prevalence, location and predisposing factors in verified thromboembolic occlusions and their significance in the pathogenesis of cerebral infarction. J Neural Set 1966^:490-510 9. Alter M, Christoferson L, Resch J, Meyers G, Ford J: Cerebrovascular disease: Frequency and population selectivity in an upper midwestem community. Stroke 1970;l:454-465 10. Eisenberg H, Morrison JT, Sullivan P, Foote FM: Cerebrovascular accidents: Incidence and survival rates in a defined population: Middlesex county, Connecticut. JAMA 1964;189:883-888 11. Gh/nn AA: Vascular diseases of the nervous system: A series of 315 cases. Br Med J 1956;2:1216-1219 12. Harman B, Leyten ACM, van Luijk JH, Frenken CWGM, Op de Coul AAW, Schulte BPM: Epidemiology of stroke in Tilburg, The Netherlands: The population-based stroke incidence register: 2. Incidence, initial clinical picture and medical care and three-week case fatality. Stroke 1982;13:629-634 13. Okada H, Horibe H, Ohno Y, Hayakawa N, Aoki N: A prospective study of cerebrovascular disease in Japanese rural communities, Akabane and Asahi: Part 1. Evaluation of risk factors in the occurrence of cerebral hemorrhage and thrombosis. Stroke 1976;7:599-6O7 14. Fisher CM, Gore I, Okabe N, White PD: Atherosclerosis of the carotid and vertebral arteries —extracranial and intracranial. / Neuwpathol Exp Neural 1965;24:455-476 15. Lhermitte F, Gautier JC, Derouesne C: Nature of occlusion of the middle cerebral artery. Neurology 1970-^0:82-88 16. Barnett HJM: Rationale of the international cooperative study of EC/IC bypass, in Handa H, Kikuchi H, Yonekawa Y (eds): Cerebral Ischemia: Clinical and Experimental Approach. Tokyo, Igakushoin, 1982, pp 131-134 17. Hass WK, Fields WS, North RR, Kricheff II, Chase NE, Bauer RB: Joint Study of Exlracranial Arterial Occlusion: II. Arteriography techniques: sites and complications. JAMA 1968;230361-968 18. DeJong RN: The Neurological Examination. New York/Evanston/ London, Harper & Row Publishers, Inc, 1976, pp 452-453 19. Allcock JM: Occlusion of the middle cerebral artery: Serial angiography as a guide to conservative therapy. J Neuwsurg 1967;27: 353-363 20. Burrows EH, Lascelles RG: The contribution of radiology to the diagnosis and prognosis of occlusion of the middle cerebral artery and its branches. Br J Radial 196538:481-593 21. Kaste M, Waltimo O: Prognosis of patients with middle cerebral artery occlusion. Stroke 1976;7:482-485 22. Lascelles RG, Burrows EH: Occlusion of the middle cerebral artery. Brain 1965;88:85-96
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23. Moulin DE, Lo R, Chiang J, Bamett HTM: Prognosis in middle cerebral artery occlusion. Stroke 1985;16:282-284 24. Sindermann F, Dichgans J, Bergleiter R: Occlusion of the middle cerebral artery and its branches: Angiographic and clinical correlates. Brain 1969;92:607-620 25. Lhermitte F, Gautier JC, Derouesne C, Guiraud B: Ischemic accidents in the middle cerebral artery territory. Arch Natrol 1968; 19: 248-256 26. Olsen TS: Regional cerebral blood flow after occlusion of the middle cerebral artery. Acta Nairol Scand 1986;73:321-337 27. Bogousslavsky J, Barnett HJM, Fox AJ, Hachinski VC, Taylor W: Atherosclerotic disease of the middle cerebral artery. Stroke 1986; 17:1112-1120 28. Rodda RA, Path FRC: The arterial patterns associated with internal carotid disease and cerebral infarcts. Stroke 1986;17: 69-75
29. Saito I, Segawa H, Shiokawa Y, Taniguchi M, Tsutsumi K: Middle cerebral artery: Correlation of computed tomography and angiography with clinical outcome. Stroke 1987;18:863-868 30. Caplan L, Babikan V, Helgason C, Hier DB, DeWitt D, Patel D, Stein R: Occlusive disease of the middle cerebral artery. Neurology 1985^5:975-982 31. Choki J, Yamaguchi T, Hirata Y, Tashiro M, Sawada T: Clinical features of cerebral embolism: Analysis of 48 cases in the acute stage. Jpn J Stroke 1982;4:54-62 32. Torvik A, Jorgensen L: Thrombotic and embolic occlusion of the carotid arteries in an autopsy series: Part 2. Cerebral lesions and clinical course. / Neurol Sd 1966;3:401-432 33. Iwamoto T, Katsumuna H, Araki G, Yunoki K: A study of cerebral infarction of the basal ganglia due to main trunk obstruction. Jpn J Stroke 1985;7:291-298 34. Krayenbuhl H, Yasargil G: Der cerebrate kollaterale blutkrcsilauf im angiographischen BUtLActa Neuroctur (Wien) 1958;6J0-80
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Thrombotic occlusion of the middle cerebral artery. S Ueda, K Fujitsu, S Inomori and T Kuwabara Stroke. 1992;23:1761-1766 doi: 10.1161/01.STR.23.12.1761 Stroke is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231 Copyright © 1992 American Heart Association, Inc. All rights reserved. Print ISSN: 0039-2499. Online ISSN: 1524-4628
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Thrombotic Occlusion of the Middle Cerebral Artery Shinsuke Ueda, MD; Kazuhiko Fujitsu, MD; Shigeo Inomori, MD; and Takeo Kuwabara, MD Background and Purpose: Epidemiological study of middle cerebral artery occlusion is important because the indication for extracranial-intracranial arterial bypass remains in dispute. To help clarify this issue, we investigated the prognosis of thrombotic middle cerebral artery occlusion in Japanese patients. Methods: We studied 40 patients with thrombotic middle cerebral artery occlusion who were selected on the basis of clinical features, computed tomographic findings, and angiographic findings. Patients with causes of embolism (i.e., cardiomyopathy, valvular heart disease, cardiac arrhythmia, and carotid ulceration) were excluded. The 40 patients were classified into three groups according to the site of middle cerebral artery occlusion: there were 13 patients with occlusion of the proximal portion of the Ml segment, 13 with distal Ml segment occlusion, and 14 with occlusion of the M2 segment. Results: Good collateral circulation was associated with improved outcomes both clinically and by computed tomography in patients with occlusion of the proximal and distal portions of the Ml segment but not in those with M2 occlusion. Conclusions: It is reasonable to assume that not only collateral circulation but also the site of occlusion plays an important role in the outcome of middle cerebral artery occlusion. Our finding that good collateral circulation improves the outcome for thrombotic occlusion of the proximal and distal Ml segments supports the possible benefits of such surgery. (Stroke 1992;23:1761-1766) KEY WORDS • arterial occlusive diseases • cerebral infarction • collateral circulation • thrombosis
E
pidemiological study of middle cerebral artery (MCA) occlusion has become increasingly important because review of the literature suggests that the indication for extracranial-intracranial arterial bypass surgery remains in dispute.1-3 Strict differentiation of thrombosis from embolus is especially important because the clinical course, neuroradiological findings, treatment, and prognosis may be different.4 Thrombosis is usually thought to have a less-sudden onset, to be less severe clinically, and to have a computed tomographic (CT) image of an irregular low density area (LDA) without midline shift.5 Embolic cerebral infarction as reported by the Harvard Cooperative Stroke Registry,6 Blackwood et al,7 and Jorgensen and Torvik8 had an incidence of 37%, 48%, and 47%, respectively. Although many authors 9 " 13 have emphasized atherosclerotic thrombosis as the most common cause of cerebral infarction, accounting for 80-95%, some1415 have found thrombotic etiology of MCA occlusion to be less frequent. In the Japanese population, MCA occlusion is 1.8 times more common than internal carotid artery (ICA) occlusion.16 In the American Joint Study of Extracranial Arterial Occlusion,17 MCA occlusion had one fourth the incidence of ICA occlusion. The reason for the etiologiFrom the Department of Neurosurgery, Yokohama City University, School of Medicine, Yokohama, Japan. Address for correspondence: Shinsuke Ueda, MD, Department of Neurosurgery, Yokohama Red Cross Hospital, 2-85, Negishicho, Naka-ku, Yokohama 231, Japan. Received October 29, 1990; final revision received July 6, 1992; accepted July 28, 1992.
cal dominance of embolus or thrombosis is controversial, but among the Japanese population thrombotic MCA occlusion appears to have a higher incidence. In this study we investigated the prognosis of thrombotic MCA occlusion in Japanese patients in relation to clinical features, CT findings, and angiographic findings. To assess collateral circulation, we determined the presence or absence of retrograde filling, that is, the presence or absence of contrast media in MCA branches through leptomeningeal anastomosis on angiography (within 6 seconds after injection). Subjects and Methods We studied 40 patients with MCA occlusion (mean age, 66.4 years [range, 42-84 years]; 27 men, 13 women) retrospectively. With diagnosis made by CT, angiographic, and clinical findings, patients who had atrial fibrillation on electrocardiogram or angiographic findings of atherosclerotic ICA ulceration regardless of the presence of ICA stenosis were excluded from this study. All patients were admitted within 48 hours of the ictus, and the initial CT scans were undertaken within 36 hours of admission. Angiography was performed within 4 days of admission. Angiograms were divided into the following three groups according to the site of occlusion: group A, occlusion of the proximal portion of the Ml segment; group B, occlusion of the distal portion of the Ml segment; and group C, occlusion of the M2 segment (Figure 1). We determined the presence or absence of retrograde filling, that is, the presence or absence of
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Proximal Ml occlusion
Distal Ml occlusion
M2 occlusion
FIGURE 1. Angiographic findings of middle cerebral artery occlusion were classified into three groups. Left panel: Occlusion of the proximal portion of the Ml segment (group A). Center panel: Occlusion of the distal portion of the Ml segment (group B). Right panel: Occlusion of the M2 segment (group C).
contrast media in MCA branches through leptomeningeal anastomoses with serial angiography. The presence or absence of angiographic retrograde filling was also analyzed. CT scans were classified into the following five categories: basal ganglia-centrum semiovale type, in which an LDA was localized in the basal ganglia and/or centrum semiovale; localized cortex-subcortical type, in which an LDA was localized in a small area of the cortex and subcortex of the frontal, temporal, or parietal lobe; lobular cortex-subcortical type, in which an LDA involved the cortex and subcortex of the frontal, temporal, and parietal lobes; hemispheric type, in which an LDA extended to one hemisphere including the basal ganglia; and normal type, in which an LDA was not found on CT (Figure 2). For the CT classification described above, CT scans that showed the maximum extent of LDA during repeated studies were selected. Degree of hemiparesis on admission was graded as mild, moderate, or severe using DeJong's definition,18 in which mild was defined as normal or movement against gravity and resistance, moderate was movement against gravity with resistance eliminated, and severe was partial movement with gravity eliminated, with a trace of muscle contraction. Outcomes were also graded: good outcome, full work and minimal disability, fair outcome, partial disability; and poor outcome, bed rest, vegetative state, or death. The follow-up period was from 43 days to 4 months (with the exception of four patients who died of complications). Correlations were made between the angiographic site of occlusion, retrograde filling, CT findings, degree of hemiparesis on admission, and outcome.
Results Occlusion of the MCA occurred on the left side in 24 patients and on the right in 16. Eleven of the 40 patients had hypertension and had been treated by antihypertensive medications. The prevalence of diabetes mellitus was 8% in this study. Mortality was 10%. At the onset of stroke, 22 patients (55%) had a mild disturbance of consciousness, but no patients were comatose. Mild hemiparesis was found in 14 patients, moderate hemiparesis in nine, and severe hemiparesis in 17. Two patients (5%) had a transient ischemic attack (TLA), and the remaining 38 patients had a complete stroke. Four patients (10%) had had previous ischemic events in the symptomatic side. Two of these four patients had TLA, and the remaining two had complete stroke. In 13 patients the MCA was occluded at the proximal portion of the Ml segment. Another 13 patients showed the MCA occluded at the distal portion of the Ml segment, and the remaining 14 had occlusion of the M2 segment. Two patients had mild ipsilateral ICA stenosis of less than 50%. The degree of hemiparesis of each patient on admission is indicated in Figure 3, in relation to the site of occlusion, retrograde filling, and CT findings. Figure 4 shows outcomes of the patients in relation to the site of occlusion, retrograde fining, and CT findings. All 13 patients with occlusion of the proximal Ml (group A) showed basal ganglia-centrum semiovale or hemispheric type findings on CT. Of seven patients with basal ganglia-centrum semiovale type findings on CT, six patients (86%) showed retrograde filling from the anterior cerebral artery (ACA), whereas of six patients
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Ueda et al
Basal ganglia -
Localized cortex-
centrum semiovale
Lobular c o r t e x -
subcortical
type
Thrombotic MCA Occlusion
subcortical
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Hemispheric type
type
type
FIGURE 2. Computed tomographic findings were classified into five categories (see text): basal ganglia-centrum semiovale type; localized cortex-subcortical type; lobular cortex-subcortical type; hemispheric type; and normal type (not shown).
with hemispheric type findings on CT only two (33%) showed retrograde filling. In the patients with occlusion of the distal Ml (group B), findings on CT were basal ganglia—centrum semiovale in four, localized cortexsubcortical in four, lobular cortex-subcortical in three,
hemispheric in one, and normal in one patient. The group B patients with basal ganglia-centrum semiovale type findings on CT showed an LDA in the centrum semiovale but not in the basal ganglia. In the patients with occlusion of the M2 (group C), findings on CT
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FIGURE 3. Chart showing degree of hemiparesis on admission in relation to site of occlusion, computed tomographic (CT) findings, and retrograde filling. O, Mild hemiparesis; A, moderate hemiparesis; x, severe hemiparesis.
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\ X l t a of occlusion
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FIGURE 4. Chart showing outcome in relation to site of occlusion, computed tomographic (CT) findings, and retrograde filling. O, Good outcome; €>, fair outcome; • , poor outcome.
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were localized cortex-subcortical type in 10 and normal type in four patients (Figures 3 and 4). Most patients with severe hemiparesis showed lobular cortex-subcortical and hemispheric type findings on CT. Ah1 patients with normal type findings on CT showed mild hemiparesis, and most patients with basal ganglia-centrum semiovale or localized cortex-subcortical type findings on CT had moderate hemiparesis (Figure 3). The degree of hemiparesis on admission was well correlated to the CT findings. The outcome was rated good in 12 (30%), fair in eight (20%), and poor, including death, in 20 (50%) patients. Four patients (10%) died of complications at the acute stage of the disease. Outcomes of patients in group A and group B were poor. However, the outcome was better in patients in group A and group B with retrograde filling than in those without retrograde filling. Outcomes of patients in group C were generally good irrespective of the presence or absence of retrograde filling (Figure 4). Patients with occlusion of the distal MCA branches to the motor cortex, however, showed poor outcome. Discussion Most of the published studies19-24 on MCA occlusion have not excluded embolic occlusion. The differential diagnosis between thrombotic and embolic MCA occlusion may be difficult. To improve the reliability of the selection of thrombotic MCA occlusion, patients who had atrial fibrillation or carotid artery ulceration were excluded based on clinical features, CT findings, and angiographic findings.5 It has been reported frequently that embolic MCA occlusion is more common than thrombotic MCA occlusion14-23-26; Lhermitte et al15 found that only 12.5% of 40 MCA occlusions were due to local thrombosis. However, in the Japanese popula-
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tion thrombotic MCA occlusion is reported to be more common.13 In this study, the mean age of 66.4 was higher than that in other reports.15-21-22-27 The mortality rate of this series was essentially the same as that in the study of Bogousslavsky et al.27 Therefore, age did not have a significant influence on death.27 Male predominance was noted in this series, as in other reports.27-28 Allcock19 reported no laterality of the side of the lesion, although others have reported left side predominance.21 In this series we reported no laterality of the lesion. In our patients, 18 of 40 (45%) had hypertension, and three (8%) had diabetes mellitus resulting in hypertension. Hypertension is an important risk factor in thrombotic MCA occlusion. This finding agrees with other reports.27-29 TLA has been defined as a temporary, focal neurological deficit presumably related to ischemia, lasting less than 24 hours. Only two patients presented with TLA; the remaining 38 patients presented with complete stroke. Caplan et al30 and Sindermann et al24 reported that TLA, as an initial symptom, was more frequently observed in ICA occlusion than in MCA occlusion. Thrombotic MCA occlusion has a more benign effect than embolic MCA occlusion,4-20-31-32 perhaps because the development of collateral circulation is better in gradual thrombotic occlusion than in sudden embolic occlusion. Therefore, although disturbance of consciousness was found in 21 patients (53%), severe disturbance of consciousness as occurs in the case of embolic occlusion was not observed. In group A, most patients with good retrograde filling showed basal ganglia-centrum semiovale type findings on CT, whereas four of five patients without retrograde filling showed hemispheric type findings on CT (Figures 3 and 4). We offer two possible explanations for the fact that basal ganglia-centrum semiovale type findings oc-
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Veda et al
Thrombotic MCA Occlusion
1765
botic occlusion of the proximal and distal Ml segments supports the possible benefits of such surgery. Acknowledgments We thank Drs. Ilu Kim, Masaharu Oda, and Akihito Saito for referring patients into this study. FIGURE 5. Left panel: Collateral circulation from anterior cerebral artery (ACA) may not supply basal ganglia because perforators of Ml segment are most distal to collateral circulation. Center panel: Atherosclerotic changes may involve origin of perforators. Right panel: Paraventricular zone may be supplied by medullary branches (arrows) rising from distal middle cerebral artery (MCA). See text for further discussion.
curred in group A patients. First, retrograde filling from the ACA may not supply the basal ganglionic area that is most distant to the collateral circulation (Figure 5, left panel). The other possible explanation, already discussed by some authors,29-33 is that the atherosclerotic change may extend to the origins of the perforators (Figure 5, center panel). Deep perforators from the ACA supply the basal ganglia, but they did not appear to be related to the size of the deep basal ganglionic infarcts in group A. Outcomes were worse in patients with hemispheric type findings than in patients with basal ganglia-centrum semiovale type findings. In addition to CT findings, presence or absence of retrograde filling appears to affect the outcome and degree of hemiparesis in group A patients. Krayenbuhl and Yasargil,34 Fisher et al,14 and Saito et al29 found that the amount of collateral circulation was intimately related to final outcome. In contrast, Sindermann et al24 noted no correlation between collateral circulation and outcome. In our series, collateral circulation was found to affect outcome in group A and group B patients but not in group C patients. It is reasonable to assume that not only collateral circulation but also the site of occlusion plays an important role in the outcome of MCA occlusion. Taking MCA distribution into consideration, it is understandable that most of the patients in group B showed localized cortex-subcortical or lobular cortexsubcortical type findings on CT. However, basal gangliacentrum semiovale type findings on CT were also shown in four patients in group B. LDAs in these four patients were found in the centrum semiovale but not in the basal ganglia. These findings suggest that the centrum semiovale in these patients was supplied by the medullary branches rising from the distal MCA (Figure 5, right panel). Patients in group C showed either localized cortex-subcortical or normal type findings on CT. No ischemic events recurred in this series, probably because of the short duration of the follow-up period (from 43 days to 4 months). According to Bogousslavsky et al,27 ischemic events during the follow-up period (35-72 months) recurred in only 10% of the patients with isolated MCA occlusion. Therefore, surgical indication for revascularization after thrombotic MCA occlusion should be determined carefully in the chronic stage. If surgical revascularization is regarded as the construction of an artificial collateral circulation, our finding that good collateral circulation improves the outcome for throm-
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Thrombotic occlusion of the middle cerebral artery. S Ueda, K Fujitsu, S Inomori and T Kuwabara Stroke. 1992;23:1761-1766 doi: 10.1161/01.STR.23.12.1761 Stroke is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231 Copyright © 1992 American Heart Association, Inc. All rights reserved. Print ISSN: 0039-2499. Online ISSN: 1524-4628
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