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Diffusion-weighted imaging and angiographic findings in the patients with unilateral multiple small infarcts. A, View of a normal middle cerebral artery (MCA) and no embolic source. MRA indicates magnetic resonance angiography. B, View of an embolic source but no MCA occlusive lesion. TFCA indicates transfemoral conventional angiography. C, View of a lesser degree of MCA stenosis. D, View of a higher degree of MCA stenosis.

Diffusion-weighted imaging and angiographic findings in the patients with unilateral multiple small infarcts. A, View of a normal middle cerebral artery (MCA) and no embolic source. MRA indicates magnetic resonance angiography. B, View of an embolic source but no MCA occlusive lesion. TFCA indicates transfemoral conventional angiography. C, View of a lesser degree of MCA stenosis. D, View of a higher degree of MCA stenosis.

Table 1. 
Angiographic Classification of 102 Patients With Striatocapsular Small, Deep Infarctions*
Angiographic Classification of 102 Patients With Striatocapsular Small, Deep Infarctions*
Table 2. 
Clinical and Radiological Features in Each Group of Patients*
Clinical and Radiological Features in Each Group of Patients*
1.
Kappelle  LJKoudstaal  PJvan Gijn  JRamos  LMKeunen  JE Carotid angiopathy in patients with lacunar infarction: a prospective study. Stroke.1988;19:1093-1096.
2.
Horowitz  DRTuhrim  SWeinberger  JMRudolph  SH Mechanisms in lacunar infarction. Stroke.1992;23:325-327.
3.
Bogousslavsky  JBarnett  HJFox  AJHachinski  VCTaylor  W Atherosclerotic disease of the middle cerebral artery. Stroke.1986;17:1112-1120.
4.
Fisher  CM Lacunar infarcts: a review. Cerebrovasc Dis.1991;1:311-320.
5.
Thajeb  P Large vessel disease in Chinese patients with capsular infarcts and prior ipsilateral transient ischaemia. Neuroradiology.1993;35:190-195.
6.
Sweeny  RCheng  EMKidwell  CSSaver  JL Incidence of intracranial large vessel disease in patients with radiologic lacunar stroke. Neurology.1999;52(suppl 2):A557-A558.
7.
Lyden  PBrott  TTilley  B  et alfor the NINDS TPA Stroke Study Group Improved reliability of the NIH Stroke Scale using video training. Stroke.1994;25:2220-2226.
8.
Tatu  LMoulin  TBogousslavsky  JDuvernoy  H Arterial territories of the human brain: cerebral hemispheres. Neurology.1998;50:1699-1708.
9.
Nelson  RFPullicino  PKendall  BEMarshall  J Computed tomography in patients presenting with lacunar syndromes. Stroke.1980;11:256-261.
10.
Wong  KSLam  WWLiang  EHuang  YNChan  YLKay  R Variability of magnetic resonance angiography and computed tomography angiography in grading middle cerebral artery stenosis. Stroke.1996;27:1084-1087.
11.
Rorick  MBNichols  FTAdams  RJ Transcranial Doppler correlation with angiography in detection of intracranial stenosis. Stroke.1994;25:1931-1934.
12.
North American Symptomatic Carotid Endarterectomy Trial Collaborators Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med.1991;325:445-453.
13.
Lyrer  PAEngelter  SRadu  EWSteck  AJ Cerebral infarcts related to isolated middle cerebral artery stenosis. Stroke.1997;28:1022-1027.
14.
Wong  KSHuang  YNGao  SLam  WWChan  YLKay  R Intracranial stenosis in Chinese patients with acute stroke. Neurology.1998;50:812-813.
15.
Ghika  JBogousslavsky  JRegli  F Infarcts in the territory of the deep perforators from the carotid system. Neurology.1989;39:507-512.
16.
Fisher  CM Bilateral occlusion of basilar artery branches. J Neurol Neurosurg Psychiatry.1977;40:1182-1189.
17.
Ay  HOliveira-Filho  JBuonanno  FS  et al Diffusion-weighted imaging identifies a subset of lacunar infarction associated with embolic source. Stroke.1999;30:2644-2650.
Original Contribution
February 2002

Middle Cerebral Artery Stenosis Is a Major Clinical Determinant in Striatocapsular Small, Deep Infarction

Author Affiliations

From the Departments of Neurology, College of Medicine, Ajou University, Suwon (Drs Bang and Huh); College of Medicine, Yonsei University, Seoul (Dr Heo); and the College of Medicine, InJe University, Seoul (Drs Kim and Park), South Korea.

Arch Neurol. 2002;59(2):259-263. doi:10.1001/archneur.59.2.259
Abstract

Background  The significance of the stenotic lesions of the middle cerebral artery (MCA) in Asian patients with striatocapsular small, deep infarctions (SSDIs) remains undetermined.

Objectives  To investigate the frequency of stenotic lesions of the MCA in patients with SSDIs and to evaluate clinical and radiological features in those same patients.

Setting  Acute stroke registry of a university hospital.

Patients and Methods  One hundred two Korean patients with acute symptomatic SSDIs underwent cerebral angiography or magnetic resonance angiography and echocardiography. We divided these patients into 2 groups—patients with and without MCA occlusive lesions. The clinical and magnetic resonance image features were compared between these 2 groups.

Results  Thirty-seven patients (36%) had an ipsilateral proximal MCA lesion, whereas 65 patients (64%) showed no MCA abnormality on cerebral angiography or magnetic resonance angiography. Among 65 patients without an MCA lesion, 18 had an embolic source; the remaining 37 patients had no demonstrable embolic source. There were significant differences in the temporal profile and magnetic resonance imaging findings between the groups. Although the type of lacunar syndrome and the volume of infarcts did not differ between the groups, the unstable temporal profile and magnetic resonance imaging findings of multiple small infarcts in the symptomatic hemisphere were frequently observed in patients with MCA lesions.

Conclusions  The proximal MCA lesion was a common cause of SSDIs in Korean patients. Depending on the existence of an MCA lesion, the clinical course and magnetic resonance imaging feature of the patients with SSDIs were different.

SEVERAL THEORIES explain the pathogenesis of symptomatic small, deep infarctions. Small-vessel disease resulting from hypertension is generally thought to be the most common cause and to have characteristic clinical features and a good prognosis. Extracranial sources of emboli, such as cardiac problems or the atherosclerosis of the internal carotid artery, have been found in patients with small, deep infarctions.1,2 Atherosclerosis of the middle cerebral artery (MCA) may also occlude the origin of deep perforators resulting in striatocapsular small, deep infarctions (SSDIs).35 However, the frequency of the MCA occlusive lesions, ranging from 2%1 to 21%,6 in patients with SSDIs has rarely been described. Previous studies have shown that atherosclerotic involvement of the intracranial vessels occur more frequently in Asian patients than in Westerners.3,5 Therefore, the frequency of the MCA occlusive lesions with SSDIs may be more prevalent in Asian patients. However, to our knowledge, this has not yet been reported.

It is important to define the pathogenesis of MCA stenosis, because a different treatment may be warranted. Moreover, because the high risk of stroke has been reported if associated MCA stenosis is present,3 the detection of an MCA occlusive lesion in patients with SSDIs may achieve major significance in clinical practice.

We, therefore, retrospectively reviewed the findings of cerebral angiography, magnetic resonance angiography (MRA), and magnetic resonance imaging (MRI) in patients with acute symptomatic SSDIs. The aim of this study was to compare the clinical features and MRI findings of patients who have acute symptomatic SSDIs with and without MCA occlusive lesions.

PATIENTS AND METHODS

From January 6, 1996, to May 25, 2001, we retrospectively studied consecutive patients with acute symptomatic SSDIs. The inclusionary criteria were as follows: patients who had suffered traditional lacunar syndrome and who had been observed within 1 week after the onset of symptoms, those who underwent cerebral angiography or MRA within 2 weeks after the onset of symptoms, and those who had MRI-confirmed relevant focal small (<15-mm), deep infarcts within the striatocapsular area. Of the patients who had multiple lesions or no abnormalities on MRI, we selected only those who underwent diffusion-weighted MRI.

Of 292 patients who suffered from lacunar syndrome and had small, deep infarcts on MRI during the study period, 102 composed the cohort. The primary reasons for exclusion were as follows: (1) small, deep infarcts located outside striatocapsular area (ie, the territory of the posterior circulation, superficial pial MCA, or anterior choroidal artery) (n = 142 patients); (2) no documentation of a relevant lesion on MRI but the patient did not undergo diffusion-weighted MRI (n = 6 patients); (3) SSDIs associated with specific disease process4 (n = 7 patients); or (4) no undergo either cerebral angiography or MRA within 2 weeks after the onset of symptoms (n = 35 patients). We divided the patients into 2 groups according to angiographic findings. The first group included patients with mural atheroma at the proximal MCA (M1), which showed an occlusive lesion at the origin of MCA penetrating arteries on cerebral angiography or MRA. The second group included those who had a normal MCA on cerebral angiography or MRA.

We reviewed the medical history, general physical and neurological examination findings, and laboratory test results. National Institutes of Health Stroke Scale (NIHSS) score7 was checked at admission to the hospital as well as on days 1, 3, and 7 after admission. Clinical course was determined after a 1-week follow-up period and defined as follows: improved, when the NIHSS score decreased more than 2 points; stable, when the score decreased less than 2 points; worsening, when the score increased after admission; and fluctuating, when the score episodically increased and then decreased or vice versa. Electrocardiography was performed in all patients, and echocardiography was performed in 77 patients, especially when the possibility of cardioembolic sources was suggested or when no other cause of stroke was found.

Brain MRI (1.5 T) was performed in all patients and diffusion-weighted MRI in 78 patients. The diagnosis of infarcts in the striatocapsular distribution was made with the use of previously published templates.8 The volume of the lesion was calculated from the MRI using the methods of Nelson et al.9 Cerebral angiography was performed in 40 patients and MRA in the remaining 62 patients. We measured M1 stenosis on MRA or conventional angiography by previously suggested methods.10,11 The M1 stenosis was calculated according to the residual luminal diameter measured at the site of maximal narrowing and the diameter of the adjacent normal vessel, from which a percentage of stenosis was calculated. The degree of stenosis was graded as follows: lower degree of stenosis (50%-69%) or higher degree of stenosis (≥70%). All patients who were classified as having a higher degree of stenosis on MRA had segmental loss of signal at the stenotic site. In the patients who underwent MRA, ultrasonography or MRA of the carotid artery was also performed. Internal carotid artery stenosis was calculated using the North American Symptomatic Carotid Endarterectomy Trial study method.12 χ2 Test and t test were used to compare clinical and radiological findings between the 2 groups.

RESULTS

Among the 102 patients, 68% were men and 32% were women, and their ages ranged from 35 to 85 years (mean age, 58 years). The angiographic and echocardiographic findings are listed in Table 1.

Thirty-seven (36%) of the 102 patients had a symptomatic MCA lesion. The lesions were disclosed in 20 patients by cerebral angiography and in 17 patients by MRA. Twenty-one patients had a high degree of stenosis; 16 patients had a lower degree of stenosis.

Embolic sources from the internal carotid artery, aorta, and heart were found in 25 patients (25%). Cardiac sources included atrial fibrillation, congestive heart failure with aortic arch atheroma (AAA), AAA with patent foramen ovale, AAA with atrial fibrillation, akinetic left ventricular segment, and aortic stenosis with cardiac thrombi. The patients who had MCA more often had embolic sources than those who had a stenotic MCA.

CLINICAL FEATURES

None had cortical dysfunction, such as aphasia or agnosia. Faciobrachiocrural involvement was characteristic, except for the patients with dysarthria clumsy hand syndrome or ataxic hemiparesis (Table 2). The age, sex ratio, the risk factors for stroke, and the types of the lacunar syndrome were not different between the groups.

However, unstable clinical courses (fluctuating or worsening) were significantly more common in the patients with MCA lesions (14 patients [38%]) compared with those without it (8 patients [12%]). The frequency of such an unstable temporal profile was higher in the patients with a higher degree of M1 stenosis (48%) than in those with a lower degree of stenosis (25%). A history of previous transient ischemic attack (TIA) was also more frequent in patients with MCA lesions (14 patients [38%]) than in those without them (11 patients [17%]). In the patients without an MCA lesion, the frequency of unstable clinical course or TIA was unrelated to the embolic sources.

MRI FINDINGS

Multiple small infarctions in the symptomatic hemispheric area were found in 23 patients (Figure 1 and Table 2). In 12 of 78 patients who underwent diffusion-weighted MRI, incidental small ischemic lesions were detected outside the striatocapsular area. Ten patients had proximal embolic sources (patients 2 through 4; Figure 1, B) or a high degree of MCA stenosis (patients 6 through 12; Figure 1, D). In the remaining 11 patients, multiple small, deep infarctions were found within the striatocapsular area of the symptomatic side, and 8 of them had ipsilateral MCA lesion of either degree (patients 1 through 3, Figure 1, C and patients 1 through 5, Figure 1, D). No significant difference in the size or volume of each ischemic lesion and white matter changes were found between the 2 groups.

COMMENT

In this study, about 40% of the patients with SSDIs had stenotic lesions of the MCA, which is a parent artery of the lenticulostriate arteries. Intracranial stenosis has been reported to be neglected as a cause of small, deep infarction1; however, about half of the patients who had MCA stenosis also had small, deep infarctions.13,14 Findings from our present study suggest that large-artery atherosclerosis and small arterial abnormalities may present with symptomatic SSDIs in a significant fraction of patients. Since intracranial atheroscleosis is more common in Asians than in Westerners, who are known to have extracranial stenosis more frequently,1,3,5,15 it is conceivable that intracranial stenosis may play an important role in the development of small, deep infarctions in Asians.15

Patients with stenotic MCA lesions showed clinical characteristics distinct from those with the normal MCA. A history of TIA and temporal profile of fluctuation or worsening of symptoms were frequent in the patients with stenotic MCA lesions. Fisher16 reported that vascular stenosis was associated with an unstable clinical course. Capsular lacunar syndromes with prior ipsilateral TIA were not benign and indicated large-vessel disease of either the MCA or the internal carotid artery.5 Our findings, in agreement with published data, suggest that patients with small, deep infarction associated with occlusive diseases of the parent artery may experience unstable clinical courses.

With the introduction of the diffusion-weighted imaging, silent infarctions at different sites from the symptomatic small, deep infarction could be detected. Multiple infarctions on the ipsilateral striatocapsular area or cortical and subcortical areas supplied by the MCA were other distinct features of severe MCA stenosis. Thromboembolism from the atherosclerotic plaque of the MCA might be responsible for the frequent association of multiple infarctions in the patients with severe MCA stenosis. Multiple small lesions on diffusion-weighted MRI were reported to be more likely to harbor an identifiable stroke mechanism than a single small, deep infarction.17

Several limitations of our present study deserve to be mentioned. Although proximal embolic sources were not found in most of the patients with an MCA lesion, a signal gap in the MRA or even a narrowing in the angiogram may represent only a partially recanalized clot. Also, there may be a discrepancy in the degree of stenosis between MRA and angiogram. None of our patients underwent both MRA and conventional angiogram.

CONCLUSIONS

Striatocapsular small infarctions were frequently associated with occlusive lesions of the MCA, which may require diagnostic and therapeutic approach different from the small arterial disease of good prognosis. A history of preceding TIA, fluctuating or progressive clinical courses, and ipsilateral multiple infarctions on MRI are findings that strongly suggest occlusive lesions of the MCA.

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Article Information

Accepted for publication September 18, 2001.

Author contributions: Study concept and design (Drs Bang and Huh); acquisition of data (Drs Bang, Kim, and Park); analysis and interpretation of data (Drs Bang and Heo); drafting of the manuscript (Drs Bang, Kim, and Park); critical revision of the manuscript for important intellectual content (Drs Heo and Huh); statistical expertise (Dr Bang); administrative, technical, and material support (Dr Kim, Park, and Huh); and study supervision (Drs Heo and Huh).

Corresponding author and reprints: Kyoon Huh, MD, Department of Neurology, College of Medicine, Ajou University, Woncheon-dong San 5, Paldal-ku, Suwon, Kyungki-do 442-749, South Korea (e-mail: khuh@madang.ajou.ac.kr).

References
1.
Kappelle  LJKoudstaal  PJvan Gijn  JRamos  LMKeunen  JE Carotid angiopathy in patients with lacunar infarction: a prospective study. Stroke.1988;19:1093-1096.
2.
Horowitz  DRTuhrim  SWeinberger  JMRudolph  SH Mechanisms in lacunar infarction. Stroke.1992;23:325-327.
3.
Bogousslavsky  JBarnett  HJFox  AJHachinski  VCTaylor  W Atherosclerotic disease of the middle cerebral artery. Stroke.1986;17:1112-1120.
4.
Fisher  CM Lacunar infarcts: a review. Cerebrovasc Dis.1991;1:311-320.
5.
Thajeb  P Large vessel disease in Chinese patients with capsular infarcts and prior ipsilateral transient ischaemia. Neuroradiology.1993;35:190-195.
6.
Sweeny  RCheng  EMKidwell  CSSaver  JL Incidence of intracranial large vessel disease in patients with radiologic lacunar stroke. Neurology.1999;52(suppl 2):A557-A558.
7.
Lyden  PBrott  TTilley  B  et alfor the NINDS TPA Stroke Study Group Improved reliability of the NIH Stroke Scale using video training. Stroke.1994;25:2220-2226.
8.
Tatu  LMoulin  TBogousslavsky  JDuvernoy  H Arterial territories of the human brain: cerebral hemispheres. Neurology.1998;50:1699-1708.
9.
Nelson  RFPullicino  PKendall  BEMarshall  J Computed tomography in patients presenting with lacunar syndromes. Stroke.1980;11:256-261.
10.
Wong  KSLam  WWLiang  EHuang  YNChan  YLKay  R Variability of magnetic resonance angiography and computed tomography angiography in grading middle cerebral artery stenosis. Stroke.1996;27:1084-1087.
11.
Rorick  MBNichols  FTAdams  RJ Transcranial Doppler correlation with angiography in detection of intracranial stenosis. Stroke.1994;25:1931-1934.
12.
North American Symptomatic Carotid Endarterectomy Trial Collaborators Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med.1991;325:445-453.
13.
Lyrer  PAEngelter  SRadu  EWSteck  AJ Cerebral infarcts related to isolated middle cerebral artery stenosis. Stroke.1997;28:1022-1027.
14.
Wong  KSHuang  YNGao  SLam  WWChan  YLKay  R Intracranial stenosis in Chinese patients with acute stroke. Neurology.1998;50:812-813.
15.
Ghika  JBogousslavsky  JRegli  F Infarcts in the territory of the deep perforators from the carotid system. Neurology.1989;39:507-512.
16.
Fisher  CM Bilateral occlusion of basilar artery branches. J Neurol Neurosurg Psychiatry.1977;40:1182-1189.
17.
Ay  HOliveira-Filho  JBuonanno  FS  et al Diffusion-weighted imaging identifies a subset of lacunar infarction associated with embolic source. Stroke.1999;30:2644-2650.
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