Accessory Middle Cerebral Artery and Duplication of Middle Cerebral Artery —

Terminology, Incidence, Vascular Etiology, and Developmental Significance—

Haruaki

YAMAMOTO, Shigeaki

Tohru

MARUBAYASHI*,

MATSUOKA**, and

Yasuhiko

Yukitaka

Tohru

SOEJIMA**,

MATSUKADO***

USHIO***

Department of Neurosurgery, Shimonoseki Kousei Hospital, Shimonoseki, Yamaguchi; *Department of Neurosurgery , Kumamoto Red Cross Hospital, Kumamoto; **Department of Neurosurgery , University of Occupational and Environmental Health School of Medicine, Kitakyushu, Fukuoka,

***Department of Neurosurgery , Kumamoto University Medical School, Kumamoto

Abstract A series of 455 bilateral carotid angiographies included 14 accessory middle cerebral arteries (Acc MCAs) and seven duplication of middle cerebral arteries (Dup-MCAs). The branching patterns of Dup-MCA could be classified as “direct bifurcation” from the internal carotid artery, since most lack ed the essential bifurcation or trifurcation at the distal end of the M, portion. On the other hand, Acc-MCAs are probably residual congenital arteries. These anomalous MCAs were apparently associated with epilepsy. Five Acc-MCAs were associated with anterior communicating artery aneurysm at the origin. In addition, a rare case of Dup-MCA with arteriovenous malformation at its origin was found. Key words:

accessory

middle

cerebral

artery,

duplication

Introduction

Received

March

present

14, 1986;

addresses:

Accepted

cerebral

Materials

Anomalous middle cerebral artery (MCA) arises from the internal carotid artery (ICA) or anterior communicating artery (AComA) and follows the MCA into the Sylvian fissure where it supplies part of the cortex usually fed by the MCA.'8 Many cases have been reported of this anomalous MCA, but the terminology and clinical and neuroradiological significance remain controversial. We reviewed cerebral angiography in cases of anomalous MCA to clarify the terminology and in vestigate the etiology of these arteries.

Authors'

of middle

November

artery

and

Methods

Our series included 455 patients demonstrating clear bilateral carotid angiographic evidence of disease. 110 cases of acquired diseases such as brain tumor, hypertensive hemorrhage, and trauma were classified into the control group. There were 300 aneurysm, 31 cerebral arteriovenous malformation (AVM), and 14 idiopathic epilepsy patients. These groups were com pared with the control group. We classified arteries arising from the ICA as duplication of the MCA (Dup-MCA) and arteries from the anterior cerebral artery (ACA) as accessory

6, 1987

H. Yamamoto, M.D., Department of Neurological Surgery, Health Sciences Center , University of Virginia, Charlottesville, Virginia, U.S.A.; T. Soejima, M.D., Department of Neurosurgery, Moji Rousai Hospital, Kitakyushu, Fukuoka, Japan; Y. Matsukado, M .D., Kumamoto Chuou Hospital, Kumamoto, Japan.

MCA (Acc-MCA).28) Both ultimately ritory usually fed by the MCA.

feed the ter

Results Table 1 shows the incidence arteries in the various groups.

Table

1

Number

Table

2

Summary

of these anomalous Tables 2 and 3 give

and frequency

of 14 cases

of anomalous

of Acc-MCA

MCA

clinical data about the patients. There were 14 Acc MCA and seven Dup-MCA cases in total. Of eight Acc-MCA cases with aneurysm, saccular aneurysms occurred in five at the AComA which is the origin of the anomalous artery (Cases 1-5, Figs. 1-3). This incidence was 35.7% of 14 Acc-MCA cases and 8.9% of 56 AComA aneurysm cases. However, there was no significant difference between this (8.9%) and the incidence of Acc-MCA from AComA in the control group (2.7%, 3/110 cases). Dup-MCA occurred in two (0.7%) of 300 aneurysm cases (Cases 15 and 16, Fig. 4). The in cidence was not significantly different to that in the control group (1.8%). Four cases (28.6%) of Acc-MCA and Dup-MCA occurred in 14 cases of the epilepsy group. This in cidence was significantly different (p < 0.005) to that in the control group (5.5%). One Dup-MCA had an AVM at its origin (Case 17, Fig. 5). One rare case of juvenile ruptured AComA aneurysm with right Acc-MCA arising from the AComA and left Acc-MCA arising from left A, por tion occurred (Case 5, Fig. 6). Discussion

Table

3

Summary

of seven

cases

of Dup-MCA

Crompton2) reported 10 cases of anomalous MCA among 347 autopsy cases and termed them Acc MCA. These arteries arose from the ICA between the origin of the anterior choroidal artery and the ter minal bifurcation of the ICA into the MCA and ACA. These arteries passed into the Sylvian fissure with the MCA and apparently supplied cortex in the MCA territory. Jain12) named such arteries Acc MCA whether the origin was the ICA or the AComA. However, Baptista') called the artery origi nating from the ICA the double MCA. Krayenbuhl and Yasargil15) were the first to distinguish arteries originating from the ICA, or MCA duplication, and those from the ACA, or Acc-MCA. Teal et al. 21)felt that Acc-MCA should refer to a branch of the ACA, and an anomalous MCA, regardless of size, arising from the ICA should be termed Dup MCA. Since then, this terminology has been widely accepted. However, Munakata et al.2" reported an anomalous MCA difficult to classify as Acc-MCA or Dup-MCA. This vascular anomaly had two MCAs. Krayenbuhl's angiographic study of 1000 cases") showed that MCA branching patterns could be classified into five types. The incidence of trifurca tion was 25%, pseudotrifurcation 18.5%, lateral bifurcation 48%, lateral pseudotrifurcation 6%, and medial bifurcation branching in the lateral cerebral

Fig

1

Fig 2 Fig 3

Fig 4

Case 1 Left carotid angiogram using right carotid artery compression technique The Acc-MCA (arrowheads) originates from the AComA with an aneurysm (arrow) at the origin Case 2 Left carotid angiogram, showing the Acc-MCA (arrowheads) originating from the AComA with an aneurysm (arrow) at the origin Case 3 Left carotid angiogram, showing the Acc-MCA (arrowheads) originating from the AComA with an aneurysm (arrow) at the origin

Case 15 Left carotid angiogram, showing the left Dup-MCA and an aneurysm (arrow) at the junction of the ICA and posterior com municating artery

fissure 2 5% In our 14 Acc-MCA cases, one showed trifurcation (7 1%), and 13 lateral bifurcation (92.9%). No other branching patterns were ob

Fig

5

Case 17 Left carotid angiogram, demon strating the left Dup-MCA associated with AVM

at the origin

served. No Dup-MCA cases in our series (7 cases) had remarkable lateral bifurcation or trifurcation after branching from the ICA, and therefore belong

Fig. 6

Case 5. upper: Right carotid angiogram, demonstrating the Acc-MCA (arrowheads) originating from the AComA with an aneu rysm (arrow) at the origin. lower: Left carot id angiogram, showing the Acc-MCA (arrow heads) originating from the A, portion. The right Acc-MCA (arrows) is also visualized.

ed to the medial bifurcation group. The absence of trifurcation or bifurcation in the distal part of Dup-MCA suggests that the branching pattern of Dup-MCA is different from Acc-MCA. Each branch of Dup-MCA has large calibers and feed a wide ter ritory, suggesting they are important in blood sup ply. We therefore consider that this branching pattern is more exceptional than the anomaly of these two MCAs. Teal et a1.28) called a MCA with a major branching 0.5 cm or less from the origin an early branching MCA. Kitami et al.") defined this as ear ly bifurcation originating more proximally from the middle point of the MCA horizontal portion. The Dup-MCA branching pattern is then early bifurca tion. We define this pattern as "direct bifurcation" because this anomalous artery branches directly from the ICA. We encountered two cases (1.8%) of Dup-MCA in the control group and a total of seven cases (1.5%). These incidences do not differ significantly from that of medial bifurcation (2.5%)

in Krayenbuhl's classification. We therefore suggest that Dup-MCA is merely a MCA branching pattern, and not an anomaly. In contrast, we think that Acc MCA is an anomalous vessel and the term Acc-MCA is very appropriate because of the relatively small caliber, the limited territory, and the "accessory" function in the MCA territory. We propose that there is a definite difference between Acc-MCA and Dup-MCA in the vascular etiology. The incidence of Acc-MCA in autopsy cases is reported to be 0.32)-2.7%12) and that of Dup-MCA 0.712)-2.9%.2) The incidence of Acc-MCA in angiographic studies is lower at 0.24-0.34%.30) Our angiographic study showed that the incidence of Acc-MCA was 3.1% and that of Dup-MCA 1.5%, which are close to the reported autopsy studies. The association of anomalous MCA with cerebral aneurysms is relatively high',") but may be an inci dental finding or possibly lower than reported.s,13,1'> Our Acc-MCA group included eight of 14 aneurysm cases (57.1%), five of which were located at the origin of the Acc-MCA arising from the AComA. The incidence of this association was not significant compared to the control group. However, this high incidence of Acc-MCA with an aneurysm at the origin suggests some relationship between anoma lous MCA and aneurysms. Case 5 in particular is a 19-year-old juvenile with ruptured aneurysm demon strating two Acc-MCAs (Fig. 6). Possible etiologies for cerebral aneurysm include remnant of embryonic artery, defect in the medial membrane, 4) degeneration of arterial wall '21) and hemodynamic stress.26) AComA is a preferred loca tion for cerebral aneurysm. Therefore, an Acc-MCA arising from the AComA may promote a defect of the medial membrane or hemodynamic changes, causing the cerebral aneurysm. Nine Acc-MCA cases with cerebral aneurysm have been reported in the past. 5,7,8,16,19-21,29,31) Five had aneurysm arising from the A, portion. Fuwa et al.') indicated that the loca tion suggested both congenital and acquired etiological factors. We found no Dup-MCA with aneurysm at the origin but eight such cases have been reported including six ruptured aneu rysms.', 10,13,15,24,27) As Dup-MCA is a "direct bifurcation" from the ICA, it will demonstrate the same etiology for aneurysms as Acc-MCA. Our Case 17 had an AVM at the origin of the Dup-MCA (Fig. 5), and Noguchi et al.22) reported a case of left Dup-MCA associated with AVM fed by this anomalous artery. Case 17 is the first case of Dup-MCA combined with AVM at the origin and is very interesting in the congenital development of the venous system.

Ito et al.") reported four of six Acc-MCA cases and one of seven Dup-MCA cases with idiopathic epilepsy. Koga et al.") also pointed out that Acc MCA cases tend to have epilepsy. The frequency of Acc or Dup-MCA in our epilepsy group was higher than that in the control group. This theme requires further study. Handa and co-workers6,8,9) believed that the Acc MCA is the artery of Heubner demonstrating ex treme hypertrophy for unknown reasons, but this theory is not currently accepted. 11,12,24,28) Our study showed that these anomalous MCAs coursed into the Sylvian fissure parallel to the main trunk of MCA and fed the MCA territory. The Heubner arteries were clearly identified. The primary several branches is the primitive

cranial division of the ICA has in the 7-12 mm embryo. The largest anterior choroidal artery. Just distal

to this artery, there are several twigs representing the middle cerebral stem .21) The MCA becomes a promi nent stem with several branches spreading over the cerebral hemisphere in the 16-18 mm stage. In these developmental stages, the MCA has various patterns of division. Fisher et al.') presented an autopsy case of anomalous reduplication of the circle of Willis. They thought that this anomalous reduplication could be related to residual primitive ventral and dorsal ophthalmic arteries present at this develop mental stage or anastomotic loops appearing at a slightly later stage in the formation of the adult

aneurysms associated with the accessory middle cerebral artery and duplication of the middle cerebral artery. Report of two cases. Neurol Med Chir 6)

7)

8)

9)

10)

11)

12)

13)

ophthalmic artery. Acc or Dup-MCA may there fore be considered as persistent embryonic vessels. In conclusion, we suggest that while Acc-MCA is a true anomalous artery, Dup-MCA is a variation of the branching of the ICA. Associations between Acc-MCA and AComA aneurysm, and these anomalous MCAs and epilepsy may exist, but re

14)

quire

16)

further

investigation.

15)

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4)

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Address reprint requests to: H. Yamamoto, M.D., Depart ment of Neurosurgery, Kumamoto University Medical School, 1-1-1 Honjo, Kumamoto 860, Japan.