:Acta . N urochlrurgica Acta Nenrochir (Wien) (1993) 124:71-78 9 Springer-Verlag 1993 Printed in Austria Unruptured Aneurysms Associated with Ischaemic Cerebrovascular Diseases. Surgical Indication M. Nagashima, M. Nemoto, H. Hadeishi, A. Suzuki, and N. Yasui Department of Surgical Neurology, Research Institute for Brain and Blood Vessels-Akita,Akita, Japan Summary CT. Therefore, new guidelines for operative interven- Out of 3435 patients with ischaemiccerebrovascular disease 2540 cases were investigated using cerebral angiography. In 127 of them (5%) aneurysms were found, but without clinical evidence of subarachnoid haemorrhage (SAH). 45 cases were operated upon and 82 were treated conservatively. Five of these 82 cases (6%) suffered from SAH 3 months to 10 years (mean interval 5,6 years) after the angiographic diagnosis. Four of these 5 patients with SAH died. Among the 45 surgical cases follow-up was uneventful in 29 (64%). The other 16 cases postoperatively showed neurological deterioration (36%), which was transient in 6 but with only minor improvement in 10. Of these 10 cases 2 died from cerebral infarction. related to intra-operative temporary vascular occlusion respectively myocardial infarction. Thus surgical mortality was 4% and permanent morbidity 18%. Causes of postoperative neurological deterioration were partly related to general arteriosclerotic changes and special fragility of the ischaemic brain, and partly to operative technique (excessive brain retraction, damage to cortical veins, occlusion of major vessels or damage to perforators, temporary artery occlusion). Apparently in cases with ischaemic cerebrovascular diseases operative procedures, which in other cases as a rule are well tolerated, may produce harmful effects. Therefore, in these cases, the indication for operative treatment of so far silent aneurysms should be restricted to patients who are in good general condition with longer life expectancy as far as the vascular disease is concerned, and without major neurological deficit. Furthermore, the operative technique should be especiallygentle and atraumatic. tion a n d surgical technique of so-called silent aneurysms, which have been detected only coincidentally Keywords." Ischaemic cerebrovascular disease; unruptured intracranial aneurysm; surgical indications; results; subarachnoid haemorrhage. Introduction U n r u p t u r e d a n e u r y s m s can be diagnosed m o r e freq u e n t l y t h a n k s to the availability o f m o d e r n n o n - i n vasive e x a m i n a t i o n s of cerebral vessels, for instance digital s u b t r a c t i o n a n g i o g r a p h y a n d high r e s o l u t i o n d u r i n g diagnostic investigation of other diseases, are needed. I n our d e p a r t m e n t in the past such u n r u p t u r e d aneurysms mostly were only detected by a n g i o g r a p h y in patients with clinically manifest ischaemic cerebrovascular disease, m o r e seldom in patients with hypertensive intracerebral h a e m o r r h a g e or after S A H in patients with multiple aneurysms. A l t h o u g h , according to some reports, surgery of u n r u p t u r e d a n e u r y s m s generally seems to have a good prognosis, this does n o t necessarily hold true for patients with clinically manifest ischaemic cerebrovascular disease. The analysis of our material of such cases, which is presented in this paper, tries to elucidate the influence of cerebrovascular disease o n the o u t c o m e of conservative as well as of operative t r e a t m e n t of u n r u p t u r e d aneurysms, a n d to draw conclusions regarding indications for surgery a n d its technique. Clinical Material and Methods Between 1969 and 1986 3435 patients with the clinical diagnosis of ischaemic cerebrovascular diseases had been diagnosed at the Research Institute for Brain and Blood Vessels-Akita. In 2540 of them cerebral angiography had been done. In 127 of them (5%) cerebral aneurysms were found without clinical evidence of SAH. Age ranged from 40 to 77 years (mean 60 years). There were 48 female and 79 male patients. According to the neurological symptoms and signs 32 cases (25%) had a major completed stroke, 62 (49%) a minor completed stroke, 20 (16%) a reversibleischaemicneurological deficit (RIND), and 13 (10%) transient ischaemic attack (TIA). On angiography no vascular stenosis or occlusion could be de- 72 M. Nagashima et al.: Unruptured Aneurysms Associated with Ischaemic Cerebrovascular Diseases tected in 72 cases (56%). The other 56 (44%) showed a total of 82 stenotic or occlusive lesions. 33 of them involved the middle cerebral arteries, 27 the internal carotid arteries, 5 the anterior cerebral arteries and 7 other sites. The aneurysms were located as follows: 65 (45%) on the internal carotid artery, 45 (31%) on the middle cerebral artery, 28 (19%) on the anterior communicating artery, and 9 (6%) on other arteries. 45 cases with aneurysms were operated upon; 82 cases were followed clinically under conservative management. 2 "~ Jo .9 5 "10 '- O brain Arteriosclerotic change 7 o I Results Five out of the 82 conserative cases (6%) suffered from SAH during follow-up and 4 of them died. The interval between angiographic diagnosis of the aneurysm and the onset of SAH ranged between 3 months and 10 years (mean 5,6 years) (Table 1). In 29 out of the 45 surgically treated cases the postoperative clinical course was uneventful (64%). But 16 cases (36%) showed neurological deterioration after the aneurysm operation. In 6 of them the neurological deterioration was transient (Table2), but 10 of them improved only a little (Table 3). Two out of these 10 cases died and 8 had permanent deficits. Cause of death in one case was cerebral infarction due to temporary intra-operative vascular occlusion, and in the other one a myocardial infarction after an episode of hypertensive intracerebral haemorrhage. Thus, the surgical mortality was 4% (2 out of 45 cases), and in 8 out of 45 cases permanent morbidity supervened (18%). The reasons for postoperative neurological deterioration are listed in Table2 (transient neurological worsening) and Table 3 (permanent neurological deficit). There have been technical factors such as excessive Fragility of ischaemic 2 Excessive brain retraction 2 Damage of cortical veins r t- S t e n o s i s of major vessels O L.. Occlusion of major vessels 2 O 3 Damage of perforators 3 Temporary obstruction --7 transientcases N permanentcases Fig. 1. Causes of neurological deterioration after surgery. They were divided into two categories. One was related to the condition of patients's brain and vessels. The other was regarded as technical failure during operation TabIe 1. S A H in the Conservatively Treated Cases Case Age/Sex Ischaemic side Ruptured aneurysms Unruptured aneurysm Timing interval to the rupture Result 1 2 3 62/M 64/M 67/F rt rt rt rt MC rt MC Aco? 6M 5Y 2Y dead dead dead 4 48/F It BA 10 Y dead 5 57/F It Aco BA It MC rt MC (2) rt AC rt IC It VA rt MC 3M fair Incidence of SAH attack 5/82 (6.1%). Incidence of fatal SAH 4/82 (4.9%). M C middle cerebral artery, 1C internal carotid artery, A C anterior cerebral artery, Aco anterior communicating artery, BA basilar artery, VA vertebral artery, M month, Y year. 73 M. Nagashima et al.: Unruptured Aneurysms Associated with Ischaemic Cerebrovascular Diseases Table 2. List of Cases with Transient Neurological Worsening After Aneurysmal Surgery Case Age/Sex Type of ischaemia Site of aneurysm (maximal diameter) Treatment Main causes of worsening ! 48/M minor stroke rt MC (5 mm) brain retraction 2 63/M minor stroke It MC (6 mm) ligation clipping clipping 3 64/M T[A it MC (3 ram) coating, wrapping 4 49/F minor stroke It IC (6 ram) rt MC (8 mm) clipping clipping subdural haemorrhage subdural effusion 5 61/M minor stroke rt AC (2 mm) rt AC (3 ram) Aco (3 mm) rt IC (5 ram) clipping clipping clipping clipping cerebellar haemorrhage 6 59/M minor stroke it MC (5 mm) BA (5 mm) It VA (3 mm) coating, wrapping coating, wrapping coating, wrapping damage to perforators subdural effusion hydrocephalus damage to perforators subdural effusion temporary obstruction (bypass) TIA transient ischaemic attack, M C middle cerebral artery, IC internal carotid artery, AC anterior cerebral artery, Aco anterior communicating artery, BA basilar artery, VA vertebral artery. Table 3. List of Cases with Permanent Neurological Worsening After Surgery Case Age/Sex Type of ischaemia Site of aneurysm (maximal diameter) Treatment Main causes of worsening Outcome 1 46/F major rt MC (10 mm) clipping brain retraction pneumonia partially dependent 2 47/F major rt IC (9 mm) suture coagulation temporary obstruction (premature rupture) dead 3 43/M RIND It MC (3 ram) It IC (4 ram) coating clipping embolic occlusion due to CEA fully dependent 4 63/M minor It MC (8 ram) clipping MC occlusion venous injury ICH (basal ganglia) dead 5 69/M major rt MC (2 ram) clipping temporary obstruction (CEA)partiaily dependent hydrocephalus 6 48/M RIND It IC (3 mm) coating ICH (subcortical) self managed 7 63/M major rt IC (6 ram) clipping venous injury subdural effusion fully dependent 8 65/M minor Aco (10 ram) clipping brain retraction pneumonia, GI bleeding fully dependent 9 63/F minor Aco (8 mm) rt MC (8 ram) clipping clipping damage to perforators partially dependent I0 59/F minor It MC (7 ram) clipping damage to perforator partially dependent RIND reversible ischaemic neurological deficit, CEA carotid endarterectomy, GI bleeding gastro-intestinal bleeding, M C middle cerebral artery, IC internal carotid artery, AC anterior cerebral artery, Aco anterior communicating artery, MCA middle cerebral artery, ICH intracerebral haemorrhage. 74 M. Nagashima etal.: Unruptured Aneurysms Associated with Ischaemic Cerebrovascular Diseases Fig. 2. Preoperative CT of case 1 showed small infarctions in the right frontal white matter and the left internal capsule (a, b). After surgery an additional infarction (arrow) was visible in the left basal ganglia (c, d) Fig. 3. Angiography in case 1. Aneurysm of the left middle cerebral artery before surgery (a, b) and after clipping (c, d) M. Nagashima et al.: Unruptured Aneurysms Associated with Ischaemic Cerebrovascular Diseases 75 b r a i n r e t r a c t i o n , injuries to p e r f o r a t i n g a r t e r i e s o r cereb r a l veins, a n d t e m p o r a r y v a s c u l a r o c c l u s i o n d u r i n g E C - I C b y p a s s w h i c h was p e r f o r m e d s i m u l t a n e o u s l y . A p p a r e n t l y a b r a i n w i t h p r e - e x i s t i n g i s c h a e m i c lesions is m o r e v u l n e r a b l e , a n d o p e r a t i v e p r o c e d u r e s w h i c h in o t h e r cases as a rule are well t o l e r a t e d m a y p r o d u c e h a r m f u l effects. P o s t o p e r a t i v e c o m p l i c a t i o n s h a v e b e e n s u b d u r a l effusions or bleeding, cerebellar subdural haemorrhage, hydrocephalus, pneumonia and gastro-intestinal bleeding. Illustrative Cases Case l, Female, 59 Years Hospitalization because of right hemiparesis, dysarthria and mental disturbance. CT and angiography: Multiple lacunar state and left middle cerebral artery aneurysm (Figs. 2, 3). Two months later the aneurysm was operated upon. Clipping was difficult because of marked arteriosclerotic changes near the aneurysm. Therefore, several attempts at dipping were necessary before a clip could be positioned satisfactorily. After the operation the pre-existing right hemiparesis was worse. CT revealed a small low density area in the left basal ganglia (Fig. 2). It is likely that the infarction is caused by injury to a perforating artery during operation. In cases with marked arteriosclerotic changes even temporary compression of a perforating artery by a clip blade might be sufficient to cause its permanent occlusion. Case 2, Male, 61 Years Hospitalization because of a vertigo attack. Neurological examination disclosed a horizontal, saccadic nystagmus to the right. CT was normal. Angiography showed three aneurysms, one each at the right internal carotid, anterior communicating and right anterior cerebral arteries (Fig. 4). One month after the first vertigo attack all three aneurysms were clipped at one operative session. Postoperatively the patient had a mild prolonged disturbance of consciousness and severe headache which improved gradually. CT revealed haemorrhage on the superior surface of the right cerebeIlar hemisphere (Fig. 5). This was possibly caused by a lesion of a cerebellar bridging vein as a consequence of excessive aspiration of cerebrospinal fluid. Case 3, Male, 59 Years Hospitalization because of right hemiparesis, dysarthria and dysphagia for more than 4 months. CT showed small low density areas bilaterally in the basal ganglia and the corona radiata. At angiography three aneurysms were found located on the left middle cerebral, the basilar and the left vertebral arteries, respectively (Fig. 6). All three aneurysms were operated upon in one session using a left fronto-temporal craniotomy and trans-sylvian and subtemporal transtentorial approach. Because all aneurysms showed a broad neck, only coating and wrapping was done. Postoperatively there was prolonged disturbance of consciousness for one week and transient deterioration of the hemiparesis and aphasia. Fig. 4. Pre-operative angiography in case 2 revealed three aneurysms at the right carotid-anterior choroidal artery junction (a, arrow), the right anterior cerebral artery (a, arrow head) and the anterior communicating artery (b, arrow)~ They were clipped (c) Postoperative CT showed an additional low density area in the left basal ganglia and a small subdural effusion over the left hemisphere (Fig. 7). More than a month later the subdural effusion had increased and communicating hydrocephalus developed (Fig. 8) which, four months later, was treated by ventriculo-peritoneal shunting. 76 M. Nagashima etal,: Unruptured Aneurysms Associated with Ischaemic Cerebrovascular Diseases Fig. 5. Pre- and post-operative CT of case 2. Pre-operative (a, b) no abnormality. Post-operative (c, d) haemorrhage of the superior surface of the right cerebellar hemisphere Fig. 6. Angiography in case 3. Aneurysm of the left middle cerebral artery (a, arrow), basilar artery (b, arrow) and left vertebral artery (b, arrow head) Fig. 7. Pre- and early post-operative CT of case 3. Pre-operative only generalized brain atrophy (a, b), post-operative infarction in the left basal ganglia (arrow). Also subdural effusion (c, d) M. Nagashima et al.: Unruptured Aneurysms Associated with Ischaemic Cerebrovascular Diseases 77 Fig. 8. CT of case 3 three weeks at~ter surgery. Increased subdural effusion on the left side (a, b) is shown. Ventricular dilatation which suggested communicating hydrocephalus was revealed on CT four months after surgery (c, d) The additional infarction may be caused by kinking of a perforating artery on the occasion of the wrapping of the middle cerebral artery aneurysm. And the development of the subdural effusion may be fostered by the pre-existing vascular brain atrophy. General Condition Senility, Systemic Disorder Neurological Status Severe Deficit Discussion In cases with cerebral arteriosclerosis and especially with clinical signs of cerebral ischaemia prognosis after SAH is poor. But also the risk of aneurysm surgery in such cases might be high, in spite of recent neurosurgical advances. Therefore, regarding the treatment of unruptured aneurysms, a dilemma results between operative prevention of SAH and the risks of aneurysm surgery. Several reports deal with the natural history of unruptured aneurysms. Heiskanen 2, for a ten year period after aneurysms diagnosis, found an incidence or rupture of i l , 5 % and a mortality of 6,6%. Jane e t al. 4 report a statistical yearly rupture risk of incidental aneurysms of 1%. Several authors t' 3, 6, 9 describe a relationship between aneurysm size and rupture probability. Also in our opinion size and shape of cerebral aneurysms are important factors in evaluating the indications for surgery and the prognosis. On the other hand it is generally accepted that unruptured aneurysms have a better operative prognosis compared to cases after SAH. Heiskanen 3 reported a mortality of 2,3% and Wirhth e t a l . 9 of 6,5%. Permanent or transient morbidity were 6,3 %, respectively, 14,3% in the material of Samson e t a l . v. Wirth e t al. 9 as well as Kitahara e t al. s also discussed the risk of aneurysm operations in cases complicated by cerebral ischaemia. Morbidity in the material of Wirth was 10,8%. Kitahara experienced a postoperative deterioration in 35% (7/20) and a mortality of 10% Conservative Follow-up Conservative Follow-up Probability of SAH Very small Aneurysm Conservative Follow-up Surgical Risk Marked Arteriosclerosis Excessive Brain Ischaemia Conservative Follow-up Agreement Wish to Operate of Patient and Family No : Conservative Follow-up Yes : Surgical Treatment Fig. 9. Decision making in case of unruptured aneurysms associated with cerebral ischaemia. Surgery can only be recommended in selected cases (2/20). In our material morbidity was 18% (8/45) and mortality 5% (2/45). The causes of symptomatic complications after surgery are thought to be fragility of the ischaemic brain and arteriosclerotic changes in the vicinity of the aneurysm. As already mentioned some technical failures during operation have contributed to postoperative worsening in our material, these include excessive brain retraction, damage of veins and perforating arteries, stenosis or occlusion of major vessels. But it is likely that these surgical events would have been better tolerated in cases where cerebral ischaema was not a complication. It therefore would be advisable to give priority to the protection of parent or perforating arteries and not to persist in complete clipping s of the aneurysmal neck. Patients with advanced senility, major cerebral infarction or other severe complications are not likely to 78 M. Nagashima etal.: Unruptured Aneurysms Associated with Ischaemic Cerebrovascular Diseases experience S A H d u r i n g their r a t h e r s h o r t life expectancy. Therefore, in such cases no i n d i c a t i o n for ope r a t i o n o f u n r u p t u r e d a n e u r y s m s exists. F u r t h e r m o r e , cases with severe n e u r o l o g i c a l deficit o r a n g i o g r a p h i cally p r o v e n m a r k e d arteriosclerotic changes have no good operative prognosis. F i n a l l y , the p a t i e n t s a n d their families s h o u l d be carefully i n f o r m e d a b o u t higher o p e r a t i v e risk a n d the o t h e r a b o v e m e n t i o n e d p r o g n o s t i c factors. T h e i r inf o r m e d c o n s e n t for surgery is i n d i s p e n s a b l e (Fig. 9). Conclusion U n r u p t u r e d c e r e b r a l a n e u r y s m s a s s o c i a t e d with isc h a e m i c c e r e b r o v a s c u l a r disease s h o u l d be o p e r a t e d u p o n only in selected cases. P r e c o n d i t i o n s are the absence o f m a j o r n e u r o l o g i c a l deficit a n d o t h e r severe complications. T h e high v u l n e r a b i l i t y o f the ischaemic b r a i n requires a n especially gentle o p e r a t i v e technique. Acknowledgement We are deeply grateful to the staff of the Department of Surgical Neurology of the Research Institute for Brain and Blood VesselsAkita. In particular, we thank Mr. K. Yoshioka and Mr. Y. Tozawa for preparation of the figures, Miss T. Abe of the medical record library, and Miss T. Aburaya for preparation of the manuscript. References l. Asari S, Yamamoto Y (1986) New category of unruptured cerebral aneurysms. Neurol Med Chir (Tokyo) 26:785-791 2. Heiskanen O (1981) Risks of bleeding from unruptured aneurysms in the cases with multiple intracranial aneurysms. J Neurosurg 55:524-526 3. Heiskanen O (1986) Risk of surgery for unruptured intracranial aneurysms. J Neurosurg 65:451-453 4. Jane JA, Kassell NF, Torner JC, Winn HR (1985) The natural history of aneurysms and arteriovenous malformation. J Neurosurg 62:321-323 5. Kitahara S, Saito I, Segawa H, Nihei H, Okada T (1983) Operation on cerebral aneurysm complicated with cerebral infarction. In: Kodama N (ed) Proceeding of the 2rid Conference of Surgical Treatment of Stroke. Neuron, Tokyo, pp 165-168 6. Prezelmoski MM, Fischer M, Davidson RI, Jones HR, Marcus EM (1986) Unruptured intracranial aneurysm and transient focal cerebral ischemia: a follow-up study. Neurology 36:584-587 7. Samson DS, Hodosh RM, Kemp W (1977) Surgical management of unruptured asymptomatic aneurysms. J Neurosurg 46: 731734 8. Takahashi A, Ohta H, Suzuki A, Yasui N (1987) Rebleeding after clipping of aneurysm. Surg Cereb Stroke (Tokyo) 15:116-122 9. Wirth FP, Laws ER Jr, Piepgras D, Scott RM (1983) Surgical treatment of incidental intracranial aneurysms. Neurosurgery 12: 507-511 Correspondence: Masabumi Nagashima, M.D., Department of Anatomy, Hokkaido University School of Medicine, N-15, W-7, Kita-Ku, Sapporo, Hokkaido 060, Japan.