Download Thrombotic Occlusion of the Middle Cerebral Artery

1761
Thrombotic Occlusion of the
Middle Cerebral Artery
Shinsuke Ueda, MD; Kazuhiko Fujitsu, MD; Shigeo Inomori, MD; and Takeo Kuwabara, MD
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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
1762
Stroke
Vol 23, No 12 December 1992
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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
Ueda et al
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Basal ganglia -
Localized cortex-
centrum semiovale
Lobular c o r t e x -
subcortical
type
subcortical
Thrombotic MCA Occlusion
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
Tjrpa of
CT
N^
N.
Haul (anil ia cantruai laalovala
i n
A)
Ratrotrada f l l l l n f
Praaant
x x AAA
Abaant
Distal n
(Brow B)
Hatrofrada f i l l i n *
Abaant
Pratant
O
H2
(Crow> C)
btrotrada ( I l l l t *
Mntnt
Praaant
A
O
Localizad cortai subeortieal
^T^
'***
Hwlapharlc
typa
ftoraal
trp*
X
X
X X
x x x AO
AAOOO
OOO
O
1 Y 1
Lobalar cortax —
•ubeortical
/TT.
""*
x AO
[
Yl
XO
X X X X
X
X^*^
O
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.
1764
Stroke
Vol 23, No 12 December 1992
\ X l t a of occlusion
Typa of
>v
Proxlaal K
(Group A)
Distal HI
(Group B)
•atrotrada fllllnt
btrotradt f l l l l m
Abaant
Praaant
Praaant
Baul fanil la cantrua saaiovala
• ••CO
Abaant
•CO
O
K2
(trout C)
Ratrofradi ft II ins
Praaant
Abaant
*
O
LocalIzad cortai tubcortlcal >rTrx
•OO
Lobular cortax •ubcortlcal
/^^
tyoa
/ y%
c
Haalspharic
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•orsal
tirpa
* *
•
• • •
*
• • • c c eoooo
* *
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.
*
o
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-
ooo
O
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-
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.
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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
1766
Stroke
Vol 23, No 12 December 1992
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
Thrombotic occlusion of the middle cerebral artery.
S Ueda, K Fujitsu, S Inomori and T Kuwabara
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Stroke. 1992;23:1761-1766
doi: 10.1161/01.STR.23.12.1761
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