J Neurosarg 77:853-859, 1992
The treatment of associated intracranial aneurysms and arteriovenous malformations MANUEL J. CUNHA E SA, M.D., BENNETT M. STEIN, M.D., RouEn'r A. SOLOMON, M.D., AND PAUL C. McCOnMICK, M.D.
Hospital Ega2 Moniz, Lisbon, Portugal, and Department of Neurosurgery, The Neurological Institute of New York, Columbia University, New York, New York ~" Cerebral arterial aneurysm associated with arteriovenous malformation (AVM) has been described with a variable incidence, averaging 10% of AVM cases. The present series includes 39 patients with this association, derived from a total of 400 patients with AVM's evaluated and treated since 1970. The aneurysms are classified into four major groups, each carrying particular therapeutic implications. Optimum treatment of these lesions is based in part on a knowledge of the hemodynamic alterations associated with the AVM's. In most of these cases, the symptomatic lesion was treated first; occasionally, when feasible, both lesions were treated during the same operation. All patients had some form of treatment, either surgical or endovascular, directed to at least one of the two types of lesions. All symptomatic lesions were treated and all ruptured aneurysms were obliterated. There were no deaths in this series. KE'/ WORDS
aneurism
embolization
craniotomy
9 arteriovenous malformation . cerebral blood flow
HE association of intracranial arterial aneurysm and arteriovenous malformation (AVM) has been reported with an incidence of approximately 10% of AVM eases. 1-4'7-9"11'13-15"21-25"2829'34'36-40' 45.51,53 Most authors have analyzed this coexistence from the aspect of pathophysiology and epidemiology. Less emphasis has been given to the therapy of these c o m b i n e d l e s i o n s . 4"7'19"21-25'28'34"4~ The consensus of opinion now favors early clipping of symptomatic intracranial aneurysms. With an increasing understanding of the natural history and hemodynamic changes associated with AVM's, a tendency is developing to treat these lesions whether they are symptomatic or not. 5"6.183~176 When feasible, as in most of our cases, it has been our policy to recommend surgical resection of a n A V M . 49"5~
T
Clinical Material and Methods
Incidence and Classification of Lesions Our experience is based on 39 patients with both intracranial arterial aneurysms and AVM's, representing 9.75% of 400 patients with cerebral AVM's treated between 1970 and 1990. There were 13 (33%) males and 26 (67%) females. The patients' age at the time of presentation ranged between 12 and 69 years (average J. Neurosurg. / Volume 77/December, 1992
9 subarachnoid hemorrhage
9
38.4 years). Excluding infundibular dilatations (< 3 mm), 64 aneurysms were identified by angiography. Twelve patients (30.8%) harbored multiple aneurysms, ranging from two to five. The fact that there was a high incidence of posterior circulation aneurysms (25 cases (39%)) as well as distal and "bizarre" (see below) aneurysms (18 cases (28 %)) indicated that the location of these aneurysms was different from those not associated with AVM's. 26 Furthermore, the number of aneurysms arising from the anterior cerebral arteries (nine cases (14%)) was lower than expected. We have expanded the traditional scheme of classifying aneurysms associated with AVM's to five types, including one subcategory (Fig. 1, Table 1). 19'z~'25 Among the group of aneurysms arising from arteries related to the AVM, four categories were distinguished: Type I aneurysms were seen in 39 cases (61%) and occurred proximally on major ipsilateral arteries contributing to the AVM (Fig. 2). The six cases (9.4%) of aneurysms occurring contralateral to the malformation but bearing an important indirect relationship via the circle of Willis were included in Type IA. There were 10 cases (15.6%) of Type II aneurysms, occurring distally on superficial feeders to the AVM. Type III aneurysms (eight cases (12.5%)) occurred proximally or distally involving deep arteries feeding the AVM (Fig. 853
M. J. Cunha e
Sa, et
al.
TABLE 1
Categories of aneurvsms associated with A VM's* Type I IA
Location of Aneurysm proximalon ipsilateralmajor artery feedingthe AVM proximalon major artery related but contralateralto the AVM 11 distal on superficialartery feedingthe AVM III proximalor distal on deep artery feedingthe AVM ("bizarre") IV on artery unrelated to the AVM * AVM = arteriovenousmalformation,
FIG. 1. Artist's drawing of Type I to III aneurysms associated with arteriovenous malformations. For a description of the categories see Table 1.
3). This latter group included aneurysms that we have designated as "atypical" or "bizarre" because they involved deep arteries such as the posterior or anterior choroidal, lenticulostriate, and thalamoperforating arteries (unusual locations for aneurysms). One Type IV aneurysm (1.6%) occurred on an artery anatomically and hemodynamically unrelated to the AVM. There was excellent correlation between the location of the AVM and that of the aneurysms, as can be
concluded by the almost exclusive distribution of cases in Types I, IA, II, and Ill. Giant aneurysms, rarely described in association with AVM's, ',8 were found in three of our cases, two of Type I and one of Type IV. The AVM's were separated into three categories according to size: large (> 5 cm, 20 cases), medium (2.5 to 5 cm, 11 cases), and small (< 2.5 cm, eight cases). No significant correlation was found between the size of the AVM's and the type, number, or size of the aneurysms with which they were associated.
Clinical Features Regarding initial presentation, hemorrhage occurred in 62% of eases, seizures in 21%, headaches in 5%, and mass effect in 8%. When identified, the hemorrhage was due to the aneurysm in 46% of cases and to the AVM in 33%. Eleven patients presented with aneurysmal rupture into the subarachnoid space. Seven of these patients had Type I and four had Type II aneurysms. The single Type IV aneurysm had not bled. In 21% of patients, imaging data and surgical observation did not pinpoint the cause of the hemorrhage. These were patients with parenchymal hemorrhage who harbored
FIG. 2. Left: Left carotid angiogram, lateral view, in a 60-year-old woman with intraparenchymal ventricular hemorrhage related to an arteriovenous malformation (AVM). A posterior temporal AVM (arrowheads) and a proximal Type I large posterior communicating artery aneurysm (arrow) are evident. Right: Intraoperative photograph of the second operation following previous complete removal of the AVM showing partial thrombosis of the aneurysm sac with flow visible only through a small portion of the neck (arrow). 854
J. Neurosurg. / Volume 77/December, 1992
Management of associated aneurysms and AV M's TABLE 2 Outcome in the 39 treated patients in this series
Our policy, when feasible, is to treat the symptomatic lesion first. All symptomatic lesions were treated. In 13 patients (33%), both lesions were treated at the same time. These included Type II aneurysms in five cases and Type IlI in seven cases (Fig. 4). All patients underwent surgery or endovascular procedures for at least one of the two types of lesions. Twenty-seven patients (69%) had both lesions totally eradicated by surgery, and all ruptured aneurysms were obliterated. Eleven patients (28%) underwent embolization of their malformation, either as the only form of treatment (four cases) or as an adjuvant for surgery (seven cases). Six
patients had aneurysm obliteration as the result of embolization of their AVM's (Fig. 5). Fourteen patients (36%) had both types of lesions treated in staged operations, one operation for resection of the AVM and the other for clipping of the aneurysm. Nine patients had no treatment for their AVM's. These decisions were related to our criteria for operability of AVM's and in most cases were based on the fact that the AVM was too large and strategically located to be resected safely. There were nine unruptured aneurysms that were not obliterated. Six of these aneurysms regressed with treatment of the AVM and three remained unchanged. Unfortunately, the expectation that hemodynamically related aneurysms will regress following removal of the associated AVM was not always realized; however, none of the residual aneurysms increased in size or ruptured during the followup periods after removal of the AVM. There were no deaths in this series. Follow-up study lasted from 1 to 192 months (mean 55 months). Twelve patients had mild deficits; of these patients, seven displayed partial visual field cuts, two mild dysphasia, one transient Type III nerve palsy, one slight hemiparesis, and one a mild memory problem and unilateral blindness. One patient had a major stroke related to angiography prior to the institution of treatment and has expressive aphasia and fight hemiparesis, not worsened by surgery. One patient made a slow partial recovery from an acute postoperative hyponatremic state causing prolonged coma from brain swelling; she is now ambulatory and able to care for herself but with marked cognitive deficits. One patient developed a hemorrhage in the AVM bed in the immediate postoperative period; as a result, she was in prolonged coma and now has seizures and a left arm paresis but is otherwise normal. Outcome is summarized in Table 2.
FIG. 3. Vertebral angiogram, anteroposterior view, in a 17-year-old girl with intraparenchymal ventricular hemorrhage and coma. A Type III "bizarre" aneurysm (arrow) is seen arising from a posterior choroidal branch feeding an arteriovenous malformation (AVM, arrowheads). The AVM and aneurysm were successfully resected during the same operation.
FIG. 4. Right carotid angiogram, lateral view, in a 21-yearold woman with left hemiparesis. An arteriovenous malformation (AVM, small arrowheads) is seen, with a Type Ill "bizarre" aneurysm (large arrowhead) arising from one of the thalamoperforators feeding the AVM. The AVM and associated aneurysm were successfully resected during the same operation.
Outcome
No. of
Cases normal 24 mild neurologicaldeficit, independent 12 moderate to marked neurologicaldeficit, dependent on others 3 death 0
Type 11 or 111 aneurysms, which arose in the vicinity of, adjacent to, or even within the nidus of the AVM, making the etiology of the hemorrhage difficult to determine. The eight patients with Type lII aneurysms had deep AVM's: four thalamic, one cingulate, one temporal, one sylvian, and one fronto-parietal. No other correlation between the location of the AVM's and the number or type of the aneurysms was established. No difference in age was found between groups with aneurysmal rupture as opposed to those with AVM-related hemorrhage. Results
J. Neurosurg. / Volume 77 / December, 1992
855
M. J. Cunha e Sm e/a/.
FJ(;. 5. Right carotid angiograms, anteroposterior view, in a 21-year-old woman who presented with an episode of confusion and minimal speech disturbance. A: Preoperative angiogram showing a parietal arteriovenous malformation (AVM), with a Type Ill "bizarre" aneurysm on the deep lenliculostriate artery (arrow). B: Supraselective angiogram showing the feeder with the deep aneurysm. C: Angiogram obtained during embolization showing decreased filling of the AVM. Note the coil (arrow) placed for obliteration of the aneurysm. D: Final poslembolization angiogram showing both lesions successfully obliterated. Illustrative Case The following case illustrates the complex problems presented by tandem lesions and the various treatment options that are available. This 20-year-old man suffered a deep periventricular hemorrhage. Angiography showed a large dominanthemisphere AVM (inoperable) and a small deep Type III aneurysm on a lenticulostriate artery adjacent to the apex of the AVM. Because of an intervening septicemia, we were unable to institute therapy. Follow-up angiography showed that the aneurysm (presumed to be the site of the hemorrhage) had markedly enlarged. Treatment was immediately undertaken in the form of embolization with occlusion of the artery containing the aneurysm. The AVM was subsequently reduced but not obliterated by staged embolization (Fig. 6). The follow-up period of 8 years was without incident, and the patient's neurological status is normal. Discussion We consider the sequencing of treatment for patients presenting with an aneurysm and an AVM to be of paramount importance. Two major considerations are the hemodynamic issues and the identification and priority given to treatment of the symptomatic lesion. H e m o d y n a m i c Considerations
It has been hypothesized that aneurysms arise from a congenital defect of the artery wall. 23 This theory, is still accepted as valid for some aneurysms. 3~~ Similarly, AVM's are thought to be congenital. Boyd-Wilson ~ regarded the association as coincidental, except when 856
aneurysms occurred on direct feeders to the AVM (hemodynamic stress might be a contributing factor). Paterson and McKissock w linked the occurrence of aneury'sms to increased blood flow in nutrient arteries to the AVM. This theory has gained extensive support from m ore recent series. 47' ~~3-.~ 19,24.36Besides contributing to the development of aneurysms by flow-related factors, the presence of the AVM also causes enlargement of the feeding arteries and probable pathological changes in the arterial wall, which may represent important anatomical factors. ~'27"43"475~ The assumption is that the etiology for this association is multifactorial, involving one or more of the mechanisms discussed above. J5.34.18,53 The reported incidence of aneurysms in association with AVM's has varied significantly, from 2.7% to 17 %.7-~,~9.~8.37-4o,49.51.53This discrepancy may be attributed to a sampling error in relation to the small size of most series and the different criteria used for distinguishing aneurysm from infundibular dilatation? T M Our series has an incidence approximating 10% of AVM cases, which is higher than that of aneurysms found at autopsy in an unselected patient population. ~"-~JAll but one of the aneurysms have been located on major arterial trunks supplying the AVM. Perret and Nishioka 4~ described 34 patients harboring this association, of whom 57% had aneurysms that were hemodynamically related to the AVM. Okamoto, el al., ~' studied the difference in the distribution of aneurysms alone or with AVM's. They showed that the presence of the AVM altered the normal distribution of aneurysms, a higher number occurring on direct feeders to the malformation. Nonetheless, for aneuJ. Neurost~r,r / f~)lume 77/December, 1992
Management of associated aneurysms and AV M's
FI(;. 6. Left carotid arte~' angiograms, anteroposterior view, in a 20-year-old man presenting with coma, intracerebral hemorrhage, and subsequent sepsis. A and B: Serial angiograms obtained on different days prior to the institution of treatment showing marked enlargement of a Type III "bizarre" aneurysm (arrowhead) on a lenticulostriale branch feeding a large parietal arteriovenous malformation. C: Postembolization anglogram demonstrating proximal oblileration of lhe lenticulostriate artery. (arrow) and obliteration of the aneurysm.
rysms arising in vessels proximal to the AVM or at several branching points away from the AVM, the incidence and distribution of aneurysms was similar to that of aneurysms alone. Our findings were similar, with the exception of a higher incidence of posterior circulation and Type III ("bizarre") aneurysms. Unpredictably, some aneurysms that are hemodynamically related to an AVM may decrease in size or disappear following obliteration of the AVM: ~'23--~'45 conversely, the growth of aneurysms when both lesions are left untreated has been documented, 4~42~52 as well as the case of aneurysmal rupture following resection of the AVM, raising the issue of perfusion overload factors.: In our series, an incidence of multiple aneurysms higher than in the normal population and a concentration of Type I~ II, and III (AVM flow-related) aneurysms support the role of the hemodynamic factors in their development. On the other hand, the fact that the Type IIl aneurysms were found in younger age groups, along with their unusual location (beyond the bifurcations of parent arteries), might indicate in some cases that congenital factors were involved. 2"3'~3"-~4455 Our Type IV aneurysm was thought to be coincidental. There is ample information from intraoperative, postoperative, and postembolization observations to suggest that an increase in intraluminal pressure, ~~832334~ as well as dilatation of the feeding arteries, ~2,~,.17.31.41.42.5().57 occurs following obliteration of the AVM. It is theoretically possible that these changes, which are abrupt but slow to normalize, could have an adverse effect on unruptured aneurysms proximal to the AVM, even J. Neurosurg. / Volume 77/December, 1 992
causing aneurysmal rupture following the AVM resection or reduction by embolization. In our experience, this has not occurred and is of theoretical interest only. After the elimination of the malformation, flow velocity is reduced and redirected to the high-resistance capillary bed, temporarily raising intraluminal arterial pressure which returns to normal as autoregulation reappears. 63~ This phenomenon has been offered as an explanation for the gradual reduction in size of some aneurysms following AVM removal. 4"23 In some eases, it may be important in altering the natural history of these aneurysms, thereby justifying exclusion of the malformation alone when the aneurysm is asymptomatic. A more radical option is the obliteration of both lesions during the same operation. 4'2234~ This strategy has been pursued in those cases of aneurysms located adjacent to the AVM. In our series, these aneurysms were all Type II or III. In a few of these cases, the embolic obliteration of both lesions can also be achieved. Treatment Strategy
Although our policy has been to treat the symptomatic lesion first, an exception in our series was a patient presenting with an intracerebral hemorrhage from an AVM whose associated aneurysms were clipped first. This was an early case, and clipping was thought necessary to permit safe embolization of the AVM for which the catheters had to be passed through the lumen of the arteries harboring the aneurysms. Based on our experience since then, caution is unjusti857
M. J. C u n h a e Sa, et al. fled and we have used embolization techniques via the arteries that contain untreated aneurysms without incident. Also to be considered is the morbidity and mortality from bleeding associated with aneurysmal rupture, which is significantly higher than that for an AVM. z~''4~Furthermore, the risk of repeated hemorrhage from an AVM is significantly lower than that for aneurysms. This has been used as the strongest argument in recommending treatment of the aneurysm first regardless of the circumstances. In our series, we found these considerations pertinent only when the cause of the hemorrhage is indefinite. In identifying the cause of intracranial hemorrhage, computerized tomography scans are most helpful. Intraparenchymal clots are generally due to AVM's, whereas subarachnoid hemorrhage is more consistently associated with aneurysmal rupture. The five patients in our series who had hemorrhage of uncertain origin all had Type II (one case) or Type III (four cases) aneurysms. By virtue of the proximity of these aneurysms to the nidus of the malformation, which itself was deep, the hemorrhage resulting from the rupture of either of these lesions would be parenchymal. The close anatomical relationship to the AVM in these cases enabled both lesions to be treated simultaneously. Conclusions A five-tiered scheme of classification for the aneurysms was developed to consider hemodynamic relationships between the AVM's and the aneurysms and the implications for treatment. The criteria used for the treatment of the malformations in this group of patients were identical to those that we apply to AVM's in general. 4~'5~ These criteria prescribe that the symptomatic lesion, when determined, is treated first. Whenever it was possible to safely exclude both the aneurysm and the malformation during the same operation without unreasonably increasing the risks of the procedure, this option was undertaken. References 1. Aarabi B, Chambers J: Giant thrombosed aneurysm associated with an arteriovenous malformation. Case report. J Neurosurg 49:278-282, 1978 2. Anderson RM, Blackwood W: The association of arteriovenous angioma and saccular aneurysm of the arteries of the brain. J Pathol Bacterial 77:101-110, 1959 3. Arieti S, Gray EW: Progressive multiform angiosis. Association of a cerebral angioma, aneurysms and other vascular changes in lhe brain. Arch Neural Psychiatry 51: 182-189, 1944 4. Azzam CJ: Growth of multiple peripheral high flow aneurysms of the posterior inferior eerebellar artery associated with a cerebellar arteriovenous malformation. Neurosurgery 21:934-939, 1987 5. Barnett GH, Little JR, Ebrahim ZY, et al: Cerebral circulation during arteriovenous malformation operation. Neurosurgery 20:836-842, 1987 6. Batjer HH, Devous MD Sr, Meyer YJ, et al: Cerebrovascular hemodynamics in arteriovenous malformation complicated by normal perfusion pressure breakthrough. 858
Neurosurgery 22:503-509, 1988 7. Batjer HH, Suss RA, Samson D: Intracranial arteriovenous malformations associated with aneurysms. Neurosurgery 18:29-35, 1986 8. Boyd-Wilson JS: The association of cerebral angiomas with intracranial aneurysms. J Neural Neurosurg Psychiatry 22:218-223, 1959 9. Brown RD Jr, Wiebers DO, Forbes GS: Unruptured intracranial aneurysms and arteriovenous malformations: frequency of intracranial hemorrhage and relationship of lesions. 3 Neurosurg 73:859-863, 1990 10. Chason JL, Hindman WM: Berry aneurysms of the circle of Willis. Results of a planned autopsy study. Neurology 8:41-44, 1958 11. Cronqvist S, Troupp H: Intracranial arteriovenous malformation and arterial aneurysm in the same patient. Aeta Neural Scand 42:307-316, 1966 12. Day AL, Friedman WA, Sypert GW, et al: Successful treatment of the normal perfusion pressure breakthrough syndrome. Neurosurgery 11:625-630, 1982 13. Deruty R, Mottolese C, Soustiel J, et al: Association of cerebral arteriovenous malformation and cerebral aneurysm. Diagnosis and management. Aeta Neurochir 107: 133-139, 1990 14. Fuwa I, Matsukado Y, Kaku M, et al: Enlargement of a cerebral aneurysm associated with raptured arteriovenous malformation. Aeta Neurochir 80:65-68, 1986 15. G&s G, Vifiuela F, Fox AJ, et al: Peripheral aneurysms of the cerebellar arteries. Review of 16 cases. J Neurosnrg 58:63-68, 1983 16. Garretson HD: Postoperative pressure and flow changes in the feeding arteries of cerebral arteriovenous malformations. Neurosurgery 4:544-545, 1979 (Abstract) 17. Hassler W, Gilsbach J, Gaitzsch J: Results and values of immediate postoperative angiography after operations for arteriovenous malformations. Neurochirurgia 26: 146-148, 1983 18. Hassler W, Steinmetz H: Cerebral hemodynamics in angioma patients: an intraoperative study. J Neurosnrg 67: 822-831, 1987 19. Hayashi S, Afimoto T, ltakura T, et al: The association of intmcranial aneurysms and arteriovenous malformation of the brain. Case report. J Neurosurg 55:971-975, 1981 20. Housepian EM, Pool JL: A systematic analysis of intracranial aneurysms from the autopsy files of the Presbyterian Hospital, 1914 to 1956. J Neuropathol Exp Neural 17:409-423, 1958 21. Kagawa J, Fukuda T, Azuma S, et al: [Treatment of the association of arteriovenous malformation and cerebral aneurysms.] No Shiakei Geka 17:615-623, 1989 (Jpn) 22. Kikuchi K, Kowada M, Yoneya M: Association of arteriovenous malformation and intracranial aneurysm in the posterior fossa. Surg Neural 22:499-502, 1984 23. Kondziolka D, Nixon BJ, Lasjaunias P, et al: Cerebral arteriovenous malformations with associated arterial aneurysms: hemodynamie and therapeutic considerations. Can J Neural Sci 15:130-134, 1988 24. Koulouris S, Rizzoli HV: Coexisting intracranial aneurysm and arteriovenous malformation: case report. Neurosurgery 8:219-225, 1981 25. Lasjaunias P, Piske R, Terbrugge K, et al: Cerebral arteriovenous malformations (C. AVM) and associated arterial aneurysms (AA). Analysis of 101 C. AVM cases, with 37 AA in 23 patients. Acta Nenrochir 91:29-36, 1988 26. Locksley HB: Report on the Cooperative Study of Intracranial Aneurysms and Subarachnoid Hemorrhage. Section V, Part II. Natural history of subarachnoid hemorJ. Neurosurg. / Volume 77/December, 1992
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27. 28. 29.
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rhage, intracranial aneurysms and arteriovenous malformations. Based on 6368 cases in the cooperative study. J Neurosurg 25:321-368, 1966 McCormick WF: The pathology of vascular ("arteriovenous") malformations. 3 Neurosurg 24:807-816, 1966 Miyasaka K, Wolperl SM, Prager RJ: The association of cerebral aneurysms, infundibula, and intracranial arteriovenous malformations. Stroke 13:196-203, 1982 Moniz E, Guerra M (eds): Report of the Fifth International Neurology Congress. Vol I: Reports - Vascular Diseases of the Brain. Lisbon: Fifth International Neurology Congress, 1953, pp 79-143 Mullan S, Brown FD, Patronas NJ: Hyperemic and ischemic problems of surgical treatment of arteriovenous malformations. J Neurosurg 51:757-764, 1979 Muraszko K, Wang HH, Pelton G, et al: A study of the reactivity of feeding vessels to arteriovenous malformations: correlation with clinical outcome. Neurosurgery 26: 190-200, 1990 Nornes H: Quantitation of altered hemodynamics, in Wilson CB, Stein BM (eds): lntraeranial Arteriovenous Malformations. Baltimore: Williams & Wilkins, 1984, pp 32-43 Nornes H, Grip A: Hemodynamic aspects of cerebral arteriovenous malformations. J Neurosurg 53:456-464, 1980 Noterman J, Georges P, Brotchi J: Arteriovenous malformation associated with multiple aneurysms in the posterior fossa: a case report with a review of the literature. Neurosurgery 21:387-391, 1987 Okabe T, Meyer JS, Okayasu H, et al: Xenon-enhanced CT CBF measurements in cerebral AVM's before and after excision. Contribution to pathogenesis and treatment. J Neurosurg 59:21-31, 1983 Okamoto S, Handa H, Hashimoto N: Location of intracranial aneurysms associated with cerebral arteriovenous malformation: statistical analysis. Surg Neurol 22: 335-340, 1984 Onuma T, Hori S, Suzuki J: [Intracranial aneurysm associated with arteriovenous malformation.] No Shinkei Geka 5:1157-1164, 1977 (Jpn) Ostergaard JR: Association of intmcranial aneurysm and arteriovenous malformation in childhood. Neurosurgery 14:358-362, 1984 Paterson JH, McKissock W: A clinical survey of intracranial angiomas with special reference to their mode of progression and surgical treatment: a report of 110 cases. Brain 79:233-266, 1956 Perret G, Nishioka H: Report on the Cooperative Study of lntracranial Aneurysms and Subarachnoid Hemorrhage. Section VI. Arteriovenous malformations. An analysis of 545 cases of cranio-cerebral arteriovenous malformations and fistulae reported to the cooperative study. J Neurosurg 25:467-490, 1966 Pertuiset B, Ancri D, Clergue F: Preoperative evaluation of hemodynamic factors in cerebral arteriovenous malformations or selection of a radical surgical tactic with special reference to vascular autoregulation disorders. Neuroi Res 4:209-233, 1982 Pertuiset B, Ancri D, Sichez JP, et al: Radical surgery, in cerebral AVM. Tactical procedures based upon hemody-
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namic ihctors. Adv Teeh Stand Neurosurg 10:81-143, 1983 Pile-Spellman J, Baker KF, Liszczak TM, et al: High-flow angiopathy: cerebral blood vessel changes in experimental chronic arteriovenous fistula. AJNR 7:811-815, 1986 Salpietro F, Cipri S, Tomasello F, et al: Late onset of a large cavernous aneurysm after spontaneous disappearance of cerebral arteriovenous malformation. Case report. J Neurosurg Sci 33:211-214, 1989 Shenkin HA, Jenkins F, Kim K: Arteriovenous anomaly of the brain associated with cerebral aneurysm. Case report. J Neurosurg 34:225-228, 1971 Spetzler RF, Martin NA, Carter LP, et al: Surgical management of large AVM's by staged embolization and operative excision. J Neurosurg 67:17-28, 1987 Stehbens WE: Blood vessel changes in chronic experimental arteriovenous fistulas. Surg Gynecol Obstet 127: 327-338, 1968 Stein BM: Arteriovenous malformations of the cerebral convexities, in Wilson CB, Stein BM (eds): Intracranial Arteriovenous Malformations. Baltimore: Williams & Wilkins, 1984, pp 156-183 Stein BM, Wolpert SM: Arteriovenous malformations of the brain. I: Current concepts and treatment. Arch Neurol 37:1-5, 1980 Stein BM, Wolpert SM: Arteriovenous malformations of the brain. II: Current concepts and treatment. Arch Neurol 37:69-75, 1980 Suzuki J, Onuma T: Intracranial aneurysms associated with arteriovenous malformations. 3 Neurosurg 50: 742-746, 1979 Tognetti F, Limoni P, Testa C: Aneurysm growth and hemodynamic stress. Surg Neurol 20:74-78, 1983 Tran-Dinh H, Williams LM, Jayasinghe LS: Association of intracranial aneurysm and arteriovenous malformation. Med J Aust 1:521-523, 1983 Tyler JL, Leblanc R, Meyer E, et al: Hemodynamic and metabolic effects of cerebral arteriovenous malformations studied by positron emission tomography. Stroke 20: 890-898,1989 Voigt K, Beck U, Reinshagen G: A complex cerebral vascular malformation studied by angiography: multiple aneurysms angiomas and arterial ectasia. Neuroradiology 5:117-123, 1973 Wilson CB, Martin N: Deep supratentorial arteriovenous malformations, in Wilson CB, Stein BM (eds): Intraeranial Arteriovenous Malformations. Baltimore: Williams & Wilkins, 1984, pp 184-208 Wolpert SM, Stein BM: Catheter embolization of intracranial arteriovenous malformations as an aid to surgical excision. Neuroradiology 10:73-85, 1982 Young WL, Prohovnik I, Ornstein E, et al: Monitoring of intraoperative cerebral hemodynamics before and after aneriovenous malformation resection. Anesth Analg 67: 1011-1014, 1988
Manuscript received October 8, 1991. Accepted in final form May 14, 1992. Address reprint requests to: Bennett M. Stein, M.D., The Neurological Institute of New York, Columbia University, 710 West 168th Street, New York, New York 10032.
859
The treatment of associated intracranial aneurysms and arteriovenous malformations MANUEL J. CUNHA E SA, M.D., BENNETT M. STEIN, M.D., RouEn'r A. SOLOMON, M.D., AND PAUL C. McCOnMICK, M.D.
Hospital Ega2 Moniz, Lisbon, Portugal, and Department of Neurosurgery, The Neurological Institute of New York, Columbia University, New York, New York ~" Cerebral arterial aneurysm associated with arteriovenous malformation (AVM) has been described with a variable incidence, averaging 10% of AVM cases. The present series includes 39 patients with this association, derived from a total of 400 patients with AVM's evaluated and treated since 1970. The aneurysms are classified into four major groups, each carrying particular therapeutic implications. Optimum treatment of these lesions is based in part on a knowledge of the hemodynamic alterations associated with the AVM's. In most of these cases, the symptomatic lesion was treated first; occasionally, when feasible, both lesions were treated during the same operation. All patients had some form of treatment, either surgical or endovascular, directed to at least one of the two types of lesions. All symptomatic lesions were treated and all ruptured aneurysms were obliterated. There were no deaths in this series. KE'/ WORDS
aneurism
embolization
craniotomy
9 arteriovenous malformation . cerebral blood flow
HE association of intracranial arterial aneurysm and arteriovenous malformation (AVM) has been reported with an incidence of approximately 10% of AVM eases. 1-4'7-9"11'13-15"21-25"2829'34'36-40' 45.51,53 Most authors have analyzed this coexistence from the aspect of pathophysiology and epidemiology. Less emphasis has been given to the therapy of these c o m b i n e d l e s i o n s . 4"7'19"21-25'28'34"4~ The consensus of opinion now favors early clipping of symptomatic intracranial aneurysms. With an increasing understanding of the natural history and hemodynamic changes associated with AVM's, a tendency is developing to treat these lesions whether they are symptomatic or not. 5"6.183~176 When feasible, as in most of our cases, it has been our policy to recommend surgical resection of a n A V M . 49"5~
T
Clinical Material and Methods
Incidence and Classification of Lesions Our experience is based on 39 patients with both intracranial arterial aneurysms and AVM's, representing 9.75% of 400 patients with cerebral AVM's treated between 1970 and 1990. There were 13 (33%) males and 26 (67%) females. The patients' age at the time of presentation ranged between 12 and 69 years (average J. Neurosurg. / Volume 77/December, 1992
9 subarachnoid hemorrhage
9
38.4 years). Excluding infundibular dilatations (< 3 mm), 64 aneurysms were identified by angiography. Twelve patients (30.8%) harbored multiple aneurysms, ranging from two to five. The fact that there was a high incidence of posterior circulation aneurysms (25 cases (39%)) as well as distal and "bizarre" (see below) aneurysms (18 cases (28 %)) indicated that the location of these aneurysms was different from those not associated with AVM's. 26 Furthermore, the number of aneurysms arising from the anterior cerebral arteries (nine cases (14%)) was lower than expected. We have expanded the traditional scheme of classifying aneurysms associated with AVM's to five types, including one subcategory (Fig. 1, Table 1). 19'z~'25 Among the group of aneurysms arising from arteries related to the AVM, four categories were distinguished: Type I aneurysms were seen in 39 cases (61%) and occurred proximally on major ipsilateral arteries contributing to the AVM (Fig. 2). The six cases (9.4%) of aneurysms occurring contralateral to the malformation but bearing an important indirect relationship via the circle of Willis were included in Type IA. There were 10 cases (15.6%) of Type II aneurysms, occurring distally on superficial feeders to the AVM. Type III aneurysms (eight cases (12.5%)) occurred proximally or distally involving deep arteries feeding the AVM (Fig. 853
M. J. Cunha e
Sa, et
al.
TABLE 1
Categories of aneurvsms associated with A VM's* Type I IA
Location of Aneurysm proximalon ipsilateralmajor artery feedingthe AVM proximalon major artery related but contralateralto the AVM 11 distal on superficialartery feedingthe AVM III proximalor distal on deep artery feedingthe AVM ("bizarre") IV on artery unrelated to the AVM * AVM = arteriovenousmalformation,
FIG. 1. Artist's drawing of Type I to III aneurysms associated with arteriovenous malformations. For a description of the categories see Table 1.
3). This latter group included aneurysms that we have designated as "atypical" or "bizarre" because they involved deep arteries such as the posterior or anterior choroidal, lenticulostriate, and thalamoperforating arteries (unusual locations for aneurysms). One Type IV aneurysm (1.6%) occurred on an artery anatomically and hemodynamically unrelated to the AVM. There was excellent correlation between the location of the AVM and that of the aneurysms, as can be
concluded by the almost exclusive distribution of cases in Types I, IA, II, and Ill. Giant aneurysms, rarely described in association with AVM's, ',8 were found in three of our cases, two of Type I and one of Type IV. The AVM's were separated into three categories according to size: large (> 5 cm, 20 cases), medium (2.5 to 5 cm, 11 cases), and small (< 2.5 cm, eight cases). No significant correlation was found between the size of the AVM's and the type, number, or size of the aneurysms with which they were associated.
Clinical Features Regarding initial presentation, hemorrhage occurred in 62% of eases, seizures in 21%, headaches in 5%, and mass effect in 8%. When identified, the hemorrhage was due to the aneurysm in 46% of cases and to the AVM in 33%. Eleven patients presented with aneurysmal rupture into the subarachnoid space. Seven of these patients had Type I and four had Type II aneurysms. The single Type IV aneurysm had not bled. In 21% of patients, imaging data and surgical observation did not pinpoint the cause of the hemorrhage. These were patients with parenchymal hemorrhage who harbored
FIG. 2. Left: Left carotid angiogram, lateral view, in a 60-year-old woman with intraparenchymal ventricular hemorrhage related to an arteriovenous malformation (AVM). A posterior temporal AVM (arrowheads) and a proximal Type I large posterior communicating artery aneurysm (arrow) are evident. Right: Intraoperative photograph of the second operation following previous complete removal of the AVM showing partial thrombosis of the aneurysm sac with flow visible only through a small portion of the neck (arrow). 854
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Management of associated aneurysms and AV M's TABLE 2 Outcome in the 39 treated patients in this series
Our policy, when feasible, is to treat the symptomatic lesion first. All symptomatic lesions were treated. In 13 patients (33%), both lesions were treated at the same time. These included Type II aneurysms in five cases and Type IlI in seven cases (Fig. 4). All patients underwent surgery or endovascular procedures for at least one of the two types of lesions. Twenty-seven patients (69%) had both lesions totally eradicated by surgery, and all ruptured aneurysms were obliterated. Eleven patients (28%) underwent embolization of their malformation, either as the only form of treatment (four cases) or as an adjuvant for surgery (seven cases). Six
patients had aneurysm obliteration as the result of embolization of their AVM's (Fig. 5). Fourteen patients (36%) had both types of lesions treated in staged operations, one operation for resection of the AVM and the other for clipping of the aneurysm. Nine patients had no treatment for their AVM's. These decisions were related to our criteria for operability of AVM's and in most cases were based on the fact that the AVM was too large and strategically located to be resected safely. There were nine unruptured aneurysms that were not obliterated. Six of these aneurysms regressed with treatment of the AVM and three remained unchanged. Unfortunately, the expectation that hemodynamically related aneurysms will regress following removal of the associated AVM was not always realized; however, none of the residual aneurysms increased in size or ruptured during the followup periods after removal of the AVM. There were no deaths in this series. Follow-up study lasted from 1 to 192 months (mean 55 months). Twelve patients had mild deficits; of these patients, seven displayed partial visual field cuts, two mild dysphasia, one transient Type III nerve palsy, one slight hemiparesis, and one a mild memory problem and unilateral blindness. One patient had a major stroke related to angiography prior to the institution of treatment and has expressive aphasia and fight hemiparesis, not worsened by surgery. One patient made a slow partial recovery from an acute postoperative hyponatremic state causing prolonged coma from brain swelling; she is now ambulatory and able to care for herself but with marked cognitive deficits. One patient developed a hemorrhage in the AVM bed in the immediate postoperative period; as a result, she was in prolonged coma and now has seizures and a left arm paresis but is otherwise normal. Outcome is summarized in Table 2.
FIG. 3. Vertebral angiogram, anteroposterior view, in a 17-year-old girl with intraparenchymal ventricular hemorrhage and coma. A Type III "bizarre" aneurysm (arrow) is seen arising from a posterior choroidal branch feeding an arteriovenous malformation (AVM, arrowheads). The AVM and aneurysm were successfully resected during the same operation.
FIG. 4. Right carotid angiogram, lateral view, in a 21-yearold woman with left hemiparesis. An arteriovenous malformation (AVM, small arrowheads) is seen, with a Type Ill "bizarre" aneurysm (large arrowhead) arising from one of the thalamoperforators feeding the AVM. The AVM and associated aneurysm were successfully resected during the same operation.
Outcome
No. of
Cases normal 24 mild neurologicaldeficit, independent 12 moderate to marked neurologicaldeficit, dependent on others 3 death 0
Type 11 or 111 aneurysms, which arose in the vicinity of, adjacent to, or even within the nidus of the AVM, making the etiology of the hemorrhage difficult to determine. The eight patients with Type lII aneurysms had deep AVM's: four thalamic, one cingulate, one temporal, one sylvian, and one fronto-parietal. No other correlation between the location of the AVM's and the number or type of the aneurysms was established. No difference in age was found between groups with aneurysmal rupture as opposed to those with AVM-related hemorrhage. Results
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855
M. J. Cunha e Sm e/a/.
FJ(;. 5. Right carotid angiograms, anteroposterior view, in a 21-year-old woman who presented with an episode of confusion and minimal speech disturbance. A: Preoperative angiogram showing a parietal arteriovenous malformation (AVM), with a Type Ill "bizarre" aneurysm on the deep lenliculostriate artery (arrow). B: Supraselective angiogram showing the feeder with the deep aneurysm. C: Angiogram obtained during embolization showing decreased filling of the AVM. Note the coil (arrow) placed for obliteration of the aneurysm. D: Final poslembolization angiogram showing both lesions successfully obliterated. Illustrative Case The following case illustrates the complex problems presented by tandem lesions and the various treatment options that are available. This 20-year-old man suffered a deep periventricular hemorrhage. Angiography showed a large dominanthemisphere AVM (inoperable) and a small deep Type III aneurysm on a lenticulostriate artery adjacent to the apex of the AVM. Because of an intervening septicemia, we were unable to institute therapy. Follow-up angiography showed that the aneurysm (presumed to be the site of the hemorrhage) had markedly enlarged. Treatment was immediately undertaken in the form of embolization with occlusion of the artery containing the aneurysm. The AVM was subsequently reduced but not obliterated by staged embolization (Fig. 6). The follow-up period of 8 years was without incident, and the patient's neurological status is normal. Discussion We consider the sequencing of treatment for patients presenting with an aneurysm and an AVM to be of paramount importance. Two major considerations are the hemodynamic issues and the identification and priority given to treatment of the symptomatic lesion. H e m o d y n a m i c Considerations
It has been hypothesized that aneurysms arise from a congenital defect of the artery wall. 23 This theory, is still accepted as valid for some aneurysms. 3~~ Similarly, AVM's are thought to be congenital. Boyd-Wilson ~ regarded the association as coincidental, except when 856
aneurysms occurred on direct feeders to the AVM (hemodynamic stress might be a contributing factor). Paterson and McKissock w linked the occurrence of aneury'sms to increased blood flow in nutrient arteries to the AVM. This theory has gained extensive support from m ore recent series. 47' ~~3-.~ 19,24.36Besides contributing to the development of aneurysms by flow-related factors, the presence of the AVM also causes enlargement of the feeding arteries and probable pathological changes in the arterial wall, which may represent important anatomical factors. ~'27"43"475~ The assumption is that the etiology for this association is multifactorial, involving one or more of the mechanisms discussed above. J5.34.18,53 The reported incidence of aneurysms in association with AVM's has varied significantly, from 2.7% to 17 %.7-~,~9.~8.37-4o,49.51.53This discrepancy may be attributed to a sampling error in relation to the small size of most series and the different criteria used for distinguishing aneurysm from infundibular dilatation? T M Our series has an incidence approximating 10% of AVM cases, which is higher than that of aneurysms found at autopsy in an unselected patient population. ~"-~JAll but one of the aneurysms have been located on major arterial trunks supplying the AVM. Perret and Nishioka 4~ described 34 patients harboring this association, of whom 57% had aneurysms that were hemodynamically related to the AVM. Okamoto, el al., ~' studied the difference in the distribution of aneurysms alone or with AVM's. They showed that the presence of the AVM altered the normal distribution of aneurysms, a higher number occurring on direct feeders to the malformation. Nonetheless, for aneuJ. Neurost~r,r / f~)lume 77/December, 1992
Management of associated aneurysms and AV M's
FI(;. 6. Left carotid arte~' angiograms, anteroposterior view, in a 20-year-old man presenting with coma, intracerebral hemorrhage, and subsequent sepsis. A and B: Serial angiograms obtained on different days prior to the institution of treatment showing marked enlargement of a Type III "bizarre" aneurysm (arrowhead) on a lenticulostriale branch feeding a large parietal arteriovenous malformation. C: Postembolization anglogram demonstrating proximal oblileration of lhe lenticulostriate artery. (arrow) and obliteration of the aneurysm.
rysms arising in vessels proximal to the AVM or at several branching points away from the AVM, the incidence and distribution of aneurysms was similar to that of aneurysms alone. Our findings were similar, with the exception of a higher incidence of posterior circulation and Type III ("bizarre") aneurysms. Unpredictably, some aneurysms that are hemodynamically related to an AVM may decrease in size or disappear following obliteration of the AVM: ~'23--~'45 conversely, the growth of aneurysms when both lesions are left untreated has been documented, 4~42~52 as well as the case of aneurysmal rupture following resection of the AVM, raising the issue of perfusion overload factors.: In our series, an incidence of multiple aneurysms higher than in the normal population and a concentration of Type I~ II, and III (AVM flow-related) aneurysms support the role of the hemodynamic factors in their development. On the other hand, the fact that the Type IIl aneurysms were found in younger age groups, along with their unusual location (beyond the bifurcations of parent arteries), might indicate in some cases that congenital factors were involved. 2"3'~3"-~4455 Our Type IV aneurysm was thought to be coincidental. There is ample information from intraoperative, postoperative, and postembolization observations to suggest that an increase in intraluminal pressure, ~~832334~ as well as dilatation of the feeding arteries, ~2,~,.17.31.41.42.5().57 occurs following obliteration of the AVM. It is theoretically possible that these changes, which are abrupt but slow to normalize, could have an adverse effect on unruptured aneurysms proximal to the AVM, even J. Neurosurg. / Volume 77/December, 1 992
causing aneurysmal rupture following the AVM resection or reduction by embolization. In our experience, this has not occurred and is of theoretical interest only. After the elimination of the malformation, flow velocity is reduced and redirected to the high-resistance capillary bed, temporarily raising intraluminal arterial pressure which returns to normal as autoregulation reappears. 63~ This phenomenon has been offered as an explanation for the gradual reduction in size of some aneurysms following AVM removal. 4"23 In some eases, it may be important in altering the natural history of these aneurysms, thereby justifying exclusion of the malformation alone when the aneurysm is asymptomatic. A more radical option is the obliteration of both lesions during the same operation. 4'2234~ This strategy has been pursued in those cases of aneurysms located adjacent to the AVM. In our series, these aneurysms were all Type II or III. In a few of these cases, the embolic obliteration of both lesions can also be achieved. Treatment Strategy
Although our policy has been to treat the symptomatic lesion first, an exception in our series was a patient presenting with an intracerebral hemorrhage from an AVM whose associated aneurysms were clipped first. This was an early case, and clipping was thought necessary to permit safe embolization of the AVM for which the catheters had to be passed through the lumen of the arteries harboring the aneurysms. Based on our experience since then, caution is unjusti857
M. J. C u n h a e Sa, et al. fled and we have used embolization techniques via the arteries that contain untreated aneurysms without incident. Also to be considered is the morbidity and mortality from bleeding associated with aneurysmal rupture, which is significantly higher than that for an AVM. z~''4~Furthermore, the risk of repeated hemorrhage from an AVM is significantly lower than that for aneurysms. This has been used as the strongest argument in recommending treatment of the aneurysm first regardless of the circumstances. In our series, we found these considerations pertinent only when the cause of the hemorrhage is indefinite. In identifying the cause of intracranial hemorrhage, computerized tomography scans are most helpful. Intraparenchymal clots are generally due to AVM's, whereas subarachnoid hemorrhage is more consistently associated with aneurysmal rupture. The five patients in our series who had hemorrhage of uncertain origin all had Type II (one case) or Type III (four cases) aneurysms. By virtue of the proximity of these aneurysms to the nidus of the malformation, which itself was deep, the hemorrhage resulting from the rupture of either of these lesions would be parenchymal. The close anatomical relationship to the AVM in these cases enabled both lesions to be treated simultaneously. Conclusions A five-tiered scheme of classification for the aneurysms was developed to consider hemodynamic relationships between the AVM's and the aneurysms and the implications for treatment. The criteria used for the treatment of the malformations in this group of patients were identical to those that we apply to AVM's in general. 4~'5~ These criteria prescribe that the symptomatic lesion, when determined, is treated first. Whenever it was possible to safely exclude both the aneurysm and the malformation during the same operation without unreasonably increasing the risks of the procedure, this option was undertaken. References 1. Aarabi B, Chambers J: Giant thrombosed aneurysm associated with an arteriovenous malformation. Case report. J Neurosurg 49:278-282, 1978 2. Anderson RM, Blackwood W: The association of arteriovenous angioma and saccular aneurysm of the arteries of the brain. J Pathol Bacterial 77:101-110, 1959 3. Arieti S, Gray EW: Progressive multiform angiosis. Association of a cerebral angioma, aneurysms and other vascular changes in lhe brain. Arch Neural Psychiatry 51: 182-189, 1944 4. Azzam CJ: Growth of multiple peripheral high flow aneurysms of the posterior inferior eerebellar artery associated with a cerebellar arteriovenous malformation. Neurosurgery 21:934-939, 1987 5. Barnett GH, Little JR, Ebrahim ZY, et al: Cerebral circulation during arteriovenous malformation operation. Neurosurgery 20:836-842, 1987 6. Batjer HH, Devous MD Sr, Meyer YJ, et al: Cerebrovascular hemodynamics in arteriovenous malformation complicated by normal perfusion pressure breakthrough. 858
Neurosurgery 22:503-509, 1988 7. Batjer HH, Suss RA, Samson D: Intracranial arteriovenous malformations associated with aneurysms. Neurosurgery 18:29-35, 1986 8. Boyd-Wilson JS: The association of cerebral angiomas with intracranial aneurysms. J Neural Neurosurg Psychiatry 22:218-223, 1959 9. Brown RD Jr, Wiebers DO, Forbes GS: Unruptured intracranial aneurysms and arteriovenous malformations: frequency of intracranial hemorrhage and relationship of lesions. 3 Neurosurg 73:859-863, 1990 10. Chason JL, Hindman WM: Berry aneurysms of the circle of Willis. Results of a planned autopsy study. Neurology 8:41-44, 1958 11. Cronqvist S, Troupp H: Intracranial arteriovenous malformation and arterial aneurysm in the same patient. Aeta Neural Scand 42:307-316, 1966 12. Day AL, Friedman WA, Sypert GW, et al: Successful treatment of the normal perfusion pressure breakthrough syndrome. Neurosurgery 11:625-630, 1982 13. Deruty R, Mottolese C, Soustiel J, et al: Association of cerebral arteriovenous malformation and cerebral aneurysm. Diagnosis and management. Aeta Neurochir 107: 133-139, 1990 14. Fuwa I, Matsukado Y, Kaku M, et al: Enlargement of a cerebral aneurysm associated with raptured arteriovenous malformation. Aeta Neurochir 80:65-68, 1986 15. G&s G, Vifiuela F, Fox AJ, et al: Peripheral aneurysms of the cerebellar arteries. Review of 16 cases. J Neurosnrg 58:63-68, 1983 16. Garretson HD: Postoperative pressure and flow changes in the feeding arteries of cerebral arteriovenous malformations. Neurosurgery 4:544-545, 1979 (Abstract) 17. Hassler W, Gilsbach J, Gaitzsch J: Results and values of immediate postoperative angiography after operations for arteriovenous malformations. Neurochirurgia 26: 146-148, 1983 18. Hassler W, Steinmetz H: Cerebral hemodynamics in angioma patients: an intraoperative study. J Neurosnrg 67: 822-831, 1987 19. Hayashi S, Afimoto T, ltakura T, et al: The association of intmcranial aneurysms and arteriovenous malformation of the brain. Case report. J Neurosurg 55:971-975, 1981 20. Housepian EM, Pool JL: A systematic analysis of intracranial aneurysms from the autopsy files of the Presbyterian Hospital, 1914 to 1956. J Neuropathol Exp Neural 17:409-423, 1958 21. Kagawa J, Fukuda T, Azuma S, et al: [Treatment of the association of arteriovenous malformation and cerebral aneurysms.] No Shiakei Geka 17:615-623, 1989 (Jpn) 22. Kikuchi K, Kowada M, Yoneya M: Association of arteriovenous malformation and intracranial aneurysm in the posterior fossa. Surg Neural 22:499-502, 1984 23. Kondziolka D, Nixon BJ, Lasjaunias P, et al: Cerebral arteriovenous malformations with associated arterial aneurysms: hemodynamie and therapeutic considerations. Can J Neural Sci 15:130-134, 1988 24. Koulouris S, Rizzoli HV: Coexisting intracranial aneurysm and arteriovenous malformation: case report. Neurosurgery 8:219-225, 1981 25. Lasjaunias P, Piske R, Terbrugge K, et al: Cerebral arteriovenous malformations (C. AVM) and associated arterial aneurysms (AA). Analysis of 101 C. AVM cases, with 37 AA in 23 patients. Acta Nenrochir 91:29-36, 1988 26. Locksley HB: Report on the Cooperative Study of Intracranial Aneurysms and Subarachnoid Hemorrhage. Section V, Part II. Natural history of subarachnoid hemorJ. Neurosurg. / Volume 77/December, 1992
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Manuscript received October 8, 1991. Accepted in final form May 14, 1992. Address reprint requests to: Bennett M. Stein, M.D., The Neurological Institute of New York, Columbia University, 710 West 168th Street, New York, New York 10032.
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