Introduction

   Middle cerebral artery(MCA) aneurysms account for approximately one-fifth of all intracranial aneurysmal subarachnoid hemorrhages(SAH).^2)12)13) Although the anatomy of MCA is variable, majority of MCA aneurysms are located exclusively at the first major bifurcation or trifurcation of MCA.²⁾¹⁰⁾ The distal branches of MCA are rare locations for cerebral aneurysms. The characteristics of these aneurysms have not been the subject of much investigation, because their incidence is low and the number of cases experienced by each surgeon is small. This present article deals with distinctive features of aneurysms of the distal MCA.


Clincal Materials and Methods

   From January. 1994 to December. 2003, 9 patients haboring distal MCA aneurysms were identified and underwent surgical treatment at our institution. We have retrospectively analyzed the clinical features, case management, and clinical results of the distal MCA aneurysms in these 9 consecutive patients based on medical records, neuroradiological and intraoperative findings. We divided the arterial location of these distal MCA aneurysms into four segments according to Gibo et al.⁴⁾：M2(insular segment), M2-3 junction, M3 (opercular segment), and M4(cortical segment). The patients' outcomes were categorized according to the Glasgow Outcome Scale as good recovery, moderate disability, severe disability, vegetative state, and death.

Result

   During the 10-year period from 1994 to 2003, 842 cases of saccular aneurysms were operated on by direct surgical approach in our institution. 241 aneurysms arose from the MCA. Of those patients, nine had distal MCA aneurysms. Case details are illustrated in Table 1. Among of them, seven patients sustained an SAH caused by rupture of the distal MCA aneurysms, other two paitents were diagnosed incidentally during investigation for another aneurysmal SAH. The mean age at presentation was 55.1 years(range 42-61 years) and female dominance was observed by seven to two. Mainly, left side is affected in eight cases and event involved in right side is only one. Six lesions were arising at M2 segment, two at M2-3 junction, one at M3-4 segment. Five of seven ruptured distal MCA aneurysms patients showed ICH on the initial CT scans, especially in the temporal lobe and five of nine cases revealed multiple aneurysms. All aneurysms were occluded by clipping surgery. In five cases presenting ICH, evacuation of hematoma was carried out simultaneously. Although there were no serious complications related to surgery, three patients presented transient speech disturbance postoperatively. In eight patients, the outcome was good, but in one, it was vegetative state；in this case, the initial neurological grade was poor, though there had been no complications during surgery.

1. Case Illustrations

1) Case 1：
   This 60-year old woman was admitted having sudden deterioration of mentality. On admission brain CT scans showed SAH and ICH in the left fronto-temporal lobe, left internal carotid angiography showed an aneurysm arising from the M2-3 segment of left MCA(Fig. 1). The aneurysm was occluded with clipping technique. The patient was discharged with good condition except mild speech disturbance which was improved at follow up.

2) Case 6：
   This 53-year-old woman presented with sudden onset of severe headache. Her neurological status at admission was rated Grade 3 on Hunt-Hess scale. On admission brain CT scans was obtained and demonstrated SAH and ICH in the right fronto-temporal lobe and angiography demonstrated saccular aneurysm arising from the M2-3 segment of right MCA(Fig. 2). The aneurysm was obliterated via the pterional transsylvian approach and ICH was evacuated. Postoperatively, the patient showed transient speech disturbance, but she was discharged in good condition except intermittent seizure attack. Her speech disturbance was improved at follow up.

Discussion

1. Case presentation
   The first case of an aneurysm arising from a distal segment of the MCA was reported in 1951 by Poppen.⁹⁾ Since that time, some cases of distal MCA aneurysms have been reported in the literature as case reports with few published series.⁷⁾⁸⁾ The rarity of these distal MCA aneurysms has been confirmed by other series that their incidence has been reported to range between 2 and 4% of all MCA aneurysms.^2)9)10) The incidence of distal MCA aneurysms was 1.1% of all intracranial aneurysms and 3.7% of all MCA aneurysms in this study. The our nine patients consisted of seven women and two men ranging in age from 42 to 61 years(mean 58.3 years). Horiuchi and colleagues⁵⁾ reported a similar a sex distribution with slightly higher mean age of 58.3 years. In our study, of nine patients with distal MCA aneurysms, left side is more frequently involved than right side by eight to one. Although it is not certain, we suggest that the cause of left side predominnace is higher hemodynamic stress of left internal carotid artery(ICA) than right one like aneurysms arising from other sites. The incidence of aneurysm decresed as the site of lesion became more distal. Six of nine distal MCA aneurysms were located in the M2 segment, other three aneurysms in the more distal portion. Five of seven ruptured distal MCA aneurysms presented ICH with SAH in the initial CT scans, and those five patients showed relatively poor clinical grade at admission. But none of them showed IVH in our series. Rinne et al.¹⁰⁾ reported that the risk of ICH increased as the site of aneurysm came to more distal in the MCA aneurysm but frequency of intraventricular hemorrhage(IVH) was not high. In the three patients, transient speech disturbance was presented postoperatively. Two of them had ICH, but not in other one. All three patients improved progressively but the cause of transient speech disturbance is considerable.

2. Pathogenesis
   Because majority of MCA aneurysms arise at the first major bifurcation,²⁾¹⁰⁾ there were few reports on the characteristics of distal MCA aneurysms.⁶⁾⁸⁾ In the cases of distal intracranial aneurysms, most occur as results of bacterial or disseminated fungal infection, trauma and neoplastic emboli.¹⁾³⁾ We obtained no histological specimens of aneurysm wall in our series, but all were presumed typical saccular aneurysms in the angiographic and intraoperative findings and there were no past medical history including valvular heart disease, evidence of previous infection, trauma and neoplastic disorders. Although some hypotheses such as congenital embryological defect in the vessel wall or hemodynamic stress had been proposed, the cause of cerebral aneurysms formation is still unclear, especially in the distal MCA aneurysms. We found three peculiar features in our series. The first feature is that five of nine cases presented multiple lesions. We suggested the genetic constitutional factor might influence the formation of cerebral aneurysms. And the second one is distinctive female predominance by seven to two in sex distribution. This is same ratio of Horiuchi and colleague's report.⁵⁾ In the view of this female predominance, we thought that hormonal influences might play a important role. The last is that eight of nine aneurysms were located in the left MCA. We wonder why the majority was arising from left MCA, but if we propose a hypothesis of left side dominance, high hemodynamic stress of left ICA might be a major factor of this phenomenon.

3. Surgical treatment
   The ideal treatment of a truly saccular lesion is clipping or endovascular obliteration of the aneurysm neck. However, the angiographic anatomy of distal MCA aneurysms is less conductive to treatment with GDC embolization than that of aneurysms at other site. In addition, high incidence of accompanying ICH makes a reason for the preference of direct microsurgical repair. In our series, all distal MCA aneurysms were treated by clipping.
   The surgical treatment of distal MCA aneurysms remains a technical challenge for surgeons, who must dissect the distal sylvian fissure sufficiently and follow the MCA from its proximal portion to the distal MCA aneurysms. This procedure is generally more difficult and requires much time and effort. Nevertheless, it is difficult to find exact location of distal MCA aneurysms during procedure. In addition, there is a risk of frontal lobe injury by further dissection of distal sylvian fissure and retraction of frontal lobe. Three of our nine patients showed postoperative transient speech disturbance in type of Broca's aphasia. We thought that the cause of this speech disturbance would be excessive dissection of distal sylvian fissure and retraction of frontal lobe. Although all three patients improved progressively, surgeons must take care not to injury brain during dissection and retraction. Although we did not use special equipment, Payer and colleagues⁷⁾ reported the usefulness of intraoperative color-coded duplex sonography, and Horiuchi and colleagues⁵⁾ emphasized that intraoperative angiography is useful in targeting the aneurysms. We think that the neuronavigation system might be also useful for localization of distal MCA aneurysms. At surgery, evacuation of ICH make it easy to secure the aneurysms and lower the intracranial pressure, but surgeons must care not to bring about premature rupture of aneurysms during removal of ICH. Distal branches of MCA and their aneurysms are generally small, and miniclips are more appropriate so that the weight of the clip does not torque or kink the parent vessel.

4. Patient outcomes
   Although high incidence of ICH, clincal outcomes of our patients were favorable. Only one patient whose initial status was very poor remained vegetable state. Complication related to operation was transient speech disturbance in three cases which located more distal MCA. All of them had resolved at follow up. We thought that the cause of speech disturbance might be the excessive dissection of sylvian fissure and retraction of frontal lobe. No other complication was present in our series.

Conclusion

   The aneurysms of distal MCA are rare. They have a high tendency to accompany ICH. Nevertheless, favorable outcomes at long-term follow up review were achieved for the majority of patients in this series. The appropriate surgical approach should be chosen to reach the aneurysm without brain injuy, and it is desirable for finding the exact location of aneurysms to employ special equipment such as intraoperative angiography, sonography or neuronavigator.

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