:Acta . . N6u?ochlrurgxca
Acta Neurochir (Wien) (1991) 112:92-95
9 Springer-Verlag 1991 Printed in Austria
Do Intracranial Arteriovenous Malformations Cause Subarachnoid Haemorrhage? Review of Computed Tomography Features of Ruptured Arteriovenous Malformations in the Acute Stage N. Aoki Department of Neurosurgery, Tokyo Metropolitan Fuchu Hospital Tokyo, Japan
Summary Computed tomography features of ruptured arteriovenous malformations in the acute stage were reviewed. Intracerebral or intraventricular haemorrhage was the major finding, and primary subarachnoid haemorrhage was disclosed to be rare. This observation supports the concept that arteriovenous malformations should not be included in the main pathological conditions causing subarachnoid haemorrhage. This information is of value in identifying the source of intracranial haemorrhage in patients with the coexistence of an arteriovenous malformation and an aneurysm, and provides a significant guideline for treatm~'ent. Keywords: Arteriovenous malformation; subarachnoid haemorrhage; intracerebral haemorrhage; intraventricular haemorrhage.
Introduction An intracranial arteriovenous malformation ( A V M ) , a l o n g with an i n t r a c r a n i a l a n e u r y s m , has been d e s c r i b e d as one o f the r e p r e s e n t a t i v e diseases causing s u b a r a c h n o i d h a e m o r r h a g e ( S A H ) 19. This classic concept still r e m a i n s in the recent l i t e r a t u r e a n d n e u r o surgical t e x t b o o k s 3' 4, 6, s, 10-13, 20, 22, I n the m a j o r i t y o f p a t i e n t s with A V M r u p t u r e , however, c o m p u t e d t o m o g r a p h y (CT) has s h o w n t h a t the bleeding is intracere b r a l o r i n t r a v e n t r i c u l a r ; therefore, it has b e c o m e d o u b t f u l if the A V M does really cause p r i m a r y h a e m o r r h a g e in the s u b a r a c h n o i d space. I n d e e d , in the early experience with CT, L e b l a n c etal. a l r e a d y described t h a t the presence o f s u b a r a c h n o i d b l o o d was s e l d o m detected in p a t i e n t s with r u p t u r e d A V M s 14. Similarly, recent investigators r e p o r t e d t h a t A V M s d i d n o t cause p r i m a r y S A H 15' 25. A t present, however, a m o n g neur o s u r g e o n s there m a y be no firm consensus as to w h e t h e r a n A V M is a p a t h o l o g i c a l c o n d i t i o n c o m m o n l y
causing p r i m a r y S A H , such as a n e u r y s m r u p t u r e . T o elucidate the features o f h a e m o r r h a g e due to A V M r u p t u r e A V M p a t i e n t s with i n t r a c r a n i a l h a e m o r r h a g e c o n f i r m e d by C T in the acute stage, b e l o n g i n g b o t h to the a u t h o r ' s m a t e r i a l as well as to literature r e p o r t s , are reviewed.
Material and Methods Included in the present study were patients seen at the author's institute and the literature, who had been diagnosed as having intracranial AVMs by cerebral angiography, and in whom intracranial haemorrhage had been confirmed by CT in the acute stage. Patients with a dural AVM or an associated intracranial aneurysm were excluded. Fifty patients presented at the Department of Neurosurgery, Tokyo Metropolitan Fuehu Hospital, between 1978 and 1989, after the introduction of CT. There were 30 males and 20 females, ranging in age from 5 to 78 years, with an average of 30 years (Table 1). The bleeding was classified as intracerebral haemorrhage (ICH), intraventricular haemorrhage (IVH), SAH, and subdural haematoma.
Table 1. Age in 50 Patients with Ruptured Arteriovenous Malformations Age (years)
Number of patients (%)
0-I0
8 (16)
11-20
11 (22)
21-30 31-40 41 50 51-60 61-70 71-80
14 (28) 3 (6) 10 (20) 2 (4) I (2) 1 (2)
N. Aoki: Ruptured Arteriovenous Malformations
93
Results
Table 2 shows the sites of the AVM in the author's series. The locations of haemorrhage are shown in Fig. 1: ICH in 30 patients (60%), ICH with IVH in 13 patients (26%), IVH in 4 patients (8%), SAH in 2 patients (4%), and subdural haematoma in one patient (2%). One patient each with SAH had the AVM in the left posterior temporal region (a 40-year-old female) and the cerebellar vallecula (a 44-year-old female). Isolated SAH on CT was revealed on the left temporal region and in the basal cistern, respectively. Table 3 reveals CT findings of patients in the literature available for review 9' 15, 17, 25. The majority of haemorrhage were ICH or IVH. In contrast, isolated SAH was shown to be very rare: it was noted in only three (4%) of 70 patients in the series of Miyasaka and his colleagues i7. Mitsugi et al. reported that two of 21 patients had ICH with SAH, in whom SAH was described to be secondary to ICH 15. Other series in the
Table 2. Site of Ruptured Arteriovenous Malformations in 50 Patients Site
Number of patients (%)
Cerebral hemisphere Corpus callosum/Ventricle Basal ganglia/Thalamus Cerebellum/Brain stem
35 3 8 4
Number of patients 30
m
(70) (6) (16) (8)
m
60%
20
13
26% 10 I
I I
4
I
I ICH
I
ICtI with IVtI
IVH
[Tqrm SAIl
SDH
Fig. 1. Site of haemorrhage caused by rupture of arteriovenous malformations confirmed by computed tomography in 50 patients. ICH Intracerebral haemorrhage, IVH intraventricular haemorrhage, SAH subarachnoid haemorrhage, SDH subdural haematoma
CT-era (not listed in Table 3) demonstrated that only two of 28 patients with various stages haemorrhage developed SAH 14. Forty-two patients with AVM rupture confirmed by CT or surgery were observed exclusively to have ICH or IVHS: Discussion
Despite the advent of CT, by which accurate pathological features can be delineated, some concepts in the pre-CT era remain without critical re-evaluation. SAH seems to be one of these conditions; i.e., a diagnosis of SAH may be made after obtaining bloody cerebrospinal fluid by lumbar puncture, despite the CT findings showing primary haemorrhage in the cerebral parenchyma or the ventricular system. It is not valid to diagnose a SAH in patients in whom subarachnoid blood was only secondarily drained from ICH or IVH. Moyamoya disease, which had been considered as one of the common diseases in Japan causing SAH in the pre-CT ear, has already been re-evaluted as being a condition developing ICH or IVH 1. On the other hand, ruptured AVMs are thought to escape from critical assessment by CT in terms of the pathological features of' the haemorrhage. The results obtained here indicate that primary SAH due to AVM rupture is rare. This observation has already been documented 14' 15,25, but it has not yet become a consensus among neurosurgeons. In patients with an AVM in the brain stem, extrapial location of the nidus is not exceptional ~9, probably presenting with primary SAH. As clearly demonstrated by recent advances of magnetic resonance imaging, however, the majority of AVMs have most parts of their nidus in the cerebral parenchyma. Consequently, rupture of AVMs commonly causes ICH or subsequent ventricular rupture. It is known that AVMs are not uncommonly associated with intracranial aneurysms, accounting for 3% 18, 7% 2I, 9% 23, and 17% 16in patients with AVMs. This high incidence of association is to be expectedbecause aneurysm formation is partly caused by haemodynamic stress 18. In the setting of the coexistence of an AVM and an aneurysm, it is important to identify the source of rupture when deciding the approach to treatment. There is an opinion that the safest approach to patients with this combination of lesions is to treat the aneurysm first, because haemodynamic changes after AVM removal may place the associated aneurysm at immediate risk 2. This approach is acceptable for patients with an undetermined source of rupture. However, it is reasonable to make the initial approach to
N. Aoki: Ruptured Arteriovenous Malformations
94
Table 3. Site of Haemorrhage in Patients with Ruptured Arteriovenous Malformations Confirmed by Computed Tomography in the Literature
Authors (year)
Total number of patients with intracranial haemorrhage
Number of patients by site of haemorrhage
Takahashi etal. TM (1982) Mitsugi etal, 13 (1985) Miyasaka etal. 15 (1989) Fu etaL 16 (1989)
10
7
3
21
7
12
70
25
42**
7
3
4
ICH
IVH
ICH with IVH
ICH with SAH
SAH
2*
ICH Intracerebral haemorrhage, IVH intraventricular haemorrhage, SAH subarachnoid haemorrhage. * SAH secondary to ICH. ** Including isolated IVH. the r u p t u r e d lesion in patients with the identified source of h a e m o r r h a g e . This c o n s i d e r a t i o n is particularly valuable in m a k i n g decision o n emergency surgery, or in p l a n n i n g the a p p r o a c h to the lesion in a critical area. T h e present study i n c l u d i n g the a a u t h o r ' s a n d rep o r t e d series revealed that only five of 158 patients (less then 4 % ) with r u p t u r e d A V M developed p r i m a r y SAH. F u r t h e r m o r e , in a large series which included 814 patients with p r i m a r y S A H in the CT-era, only 5 patients ( 0 . 6 % ) were caused by r u p t u r e o f A V M s 24. Thus, int r a c r a n i a l A V M s should n o t be classified as a m a i n disease causing SAH, b u t should be considered as a p a t h o l o g i c a l c o n d i t i o n c o m m o n l y p r o d u c i n g I C H or IVH.
Conclusion P r i m a r y S A H is rarely caused by r u p t u r e of A V M s . A r u p t u r e d A V M can be recognized as a pathological c o n d i t i o n c o m m o n l y p r e s e n t i n g with I C H or IVH. This i n f o r m a t i o n is o f value in identifying the source o f i n t r a c r a n i a l h a e m o r r h a g e in patients with the co-existence of a n A V M a n d a n a n e u r y s m , a n d provides a significant guideline for the treatment.
Acknowledgement The author wishes to express his appreciation to Dr. Yoshiaki Shiokawa for valuable discussions and co-operation.
Referenees 1. Aoki N, Mizutani H (1984) Does moyamoya disease cause subarachnoid haemorrhage? Review of 54 cases with intracranial
hemorrhage confirmed by computerized tomography. J Neurosurg 60:348-353 2. BatjerH, Suss RA, Samson D (1986) Intracranial arteriovenous malformations associated with aneurysms. Neurosurgery 18: 2935 3. Brown RD Jr, Wiebers DO, Forbes G, O'Fallon WM, Piepgras DG, Marsh WR, Maciunas RJ (1988) The natural history of unruptured intracranial arteriovenous malformations. J Neurosurg 68:352-357 4. Celli P, Ferrante L, Palma L, Cavedon G (1984) Cerebral arteriovenous malformations in children. Clinical features and outcome of treatment in children and in adults. Surg Neurol 22:43-49 5. Date H, Yamaura A, Namba H, Saeki N, Makino H, Watanabe Y, Isobe K, Sato M (1989) Arteriovenous malformations in children and adolescents.Treatment and outcome in 51 patients. Shoni No Noshinkei 14:223-229 (in Japanese) 6. Drake CG (1979) Cerebral arteriovenous malformations. Considerations for and experience with surgical treatment in 166 cases. Clin Neurosurg 26:145-208 7. Drake CG, Friedman AH, Peerless SJ (1986) Posterior fossa arteriovenous malformations. J Neurosurg 64:1-10 8. EirasJ0 Gom6z-Perfn J, Carcavilla LI, Alberdi J (1987) Surgical experience with arteriovenous malformations in children. Child's Nerv Syst 3:156-169 9. Fu Y, Hakuba A, Yasui T, Suzuki T, Baba M, Nishimura S (1989) Cerebral arteriovenous malformations with intracranial hematoma in children. Report of seven cases. Shoni No Noshinkei 14:45-50 (in Japanese) 10. Gerosa MA, Cappellotta P, Licata C, Iraci G, Pardatscher K, Fiore DI (1981) Cerebral arteriovenous malformations in children (56 cases). Child's Brain 8:356-371 11. Giombini S, Bruzzone MG, Pluchino F, (1988) Subarachnoid hemorrhage of unexplained cause. Neurosurgery 22:313-316 12. Graf CJ, Perret GE, Torner JC (1983) Bleeding from cerebral arteriovenous malformations as part of their natural history. J Neurosurg 58:331-337
N. Aoki: Ruptured Arteriovenous Malformations 13. Hourihan MD, Gates PC, McAllister VL (1984) Subarachnoid hemorrhage in childhood and adolescence. J Neurosurg 60: 1163-1166 14. Leblanc R, Ethier R, Little JR (1979) Computed tomography findings in arteriovenous malformations of the brain. J Neurosurg 51:765-772 15. Mitsugi T, Ohta T, Shiguma M, Hirota N (1985) Computerized tomography features of ruptured cerebral arteriovenous malformation. Neurol Med Chir (Tokyo) 25:753-757 (in Japanese) 16. Miyasaka K, Wolpert SM, Prager R (1982) The association of cerebral aneurysms, infundibula, and intracranial arteriovenous malformations. Stroke 13:196-203 17. Miyasaka Y, Tanaka R, Tokiwa K, Ichikawa H, Suwa T, Takano S, Ohtaka H, Kurata A, Endo M, Saito M, Yada K, Kitahara T, Ohwada T (1989) Clinical significance of intracranial hemorrhage caused by cerebral arteriovenous malformations: With special reference to intraventricular hemorrhage. No Shinkei Geka 17:133-138 (in Japanese) 18. Okamoto S, Handa H, Hashimoto N (1984) Location of intracranial aneurysms associated with arteriovenous malformation: statistical analysis. Surg Neurol 22:335-340 19. Perret G, Nishioka H (1966) Arteriovenous malformations. An analysis of 545 cases of craniocerebral malformations and fistulae reported to the cooperative study. J Neurosurg 25: 467490
95 20. Sano K, Ueda Y, Saito I (1978) Subarachnoid hemorrhage in children. Child's Brain 4:38~46 21. Shiokawa Y, Aoki N, Kubota M, Mizutani H, Saito I, Takakura K (1988) Treatment of cases with coexisting intracranial aneurysms and arteriovenous malformations. Surgery for Cerebral Stroke 16:118-122 (in Japanese) 22. Smith RR (1982) Pathophysiology and clinical evaluation of subarachnoid hemorrhage. In: Youmans JR (ed) Neurological surgery, ed 2. WB Saunders, Philadelphia, pp 1627-1644 23. Suzuki M, Mizoi K, Yoshimoto T, Suzuki J (1988) Ciinical analysis of 24 cases with AVM associated with cerebral aneurysms. Surgery for Cerebral Stroke 16:107-112 (in Japanese) 24. Suzuki S, Kayama T, Sakurai Y, Ogawa A, Suzuki J (1987) Subarachnoid hemorrhage of unknown cause. Neurosurgery 21: 310-313 25. Takahashi M, Sonobe M, Shirane R, Kubota Y, Kawakami H (1982) Computer tomography of ruptured intracranial arteriovenous malformations in the acute stage. Acta Neurochir (Wien) 66:87-94
Correspondence and Reprints: Nobuhiko Aoki, M. D., Department of Neurosurgery, Tokyo Metropolitan Fuchu Hospital, 29-2 Musashidai, Fuchu-Shi, Tokyo 183, Japan.
Acta Neurochir (Wien) (1991) 112:92-95
9 Springer-Verlag 1991 Printed in Austria
Do Intracranial Arteriovenous Malformations Cause Subarachnoid Haemorrhage? Review of Computed Tomography Features of Ruptured Arteriovenous Malformations in the Acute Stage N. Aoki Department of Neurosurgery, Tokyo Metropolitan Fuchu Hospital Tokyo, Japan
Summary Computed tomography features of ruptured arteriovenous malformations in the acute stage were reviewed. Intracerebral or intraventricular haemorrhage was the major finding, and primary subarachnoid haemorrhage was disclosed to be rare. This observation supports the concept that arteriovenous malformations should not be included in the main pathological conditions causing subarachnoid haemorrhage. This information is of value in identifying the source of intracranial haemorrhage in patients with the coexistence of an arteriovenous malformation and an aneurysm, and provides a significant guideline for treatm~'ent. Keywords: Arteriovenous malformation; subarachnoid haemorrhage; intracerebral haemorrhage; intraventricular haemorrhage.
Introduction An intracranial arteriovenous malformation ( A V M ) , a l o n g with an i n t r a c r a n i a l a n e u r y s m , has been d e s c r i b e d as one o f the r e p r e s e n t a t i v e diseases causing s u b a r a c h n o i d h a e m o r r h a g e ( S A H ) 19. This classic concept still r e m a i n s in the recent l i t e r a t u r e a n d n e u r o surgical t e x t b o o k s 3' 4, 6, s, 10-13, 20, 22, I n the m a j o r i t y o f p a t i e n t s with A V M r u p t u r e , however, c o m p u t e d t o m o g r a p h y (CT) has s h o w n t h a t the bleeding is intracere b r a l o r i n t r a v e n t r i c u l a r ; therefore, it has b e c o m e d o u b t f u l if the A V M does really cause p r i m a r y h a e m o r r h a g e in the s u b a r a c h n o i d space. I n d e e d , in the early experience with CT, L e b l a n c etal. a l r e a d y described t h a t the presence o f s u b a r a c h n o i d b l o o d was s e l d o m detected in p a t i e n t s with r u p t u r e d A V M s 14. Similarly, recent investigators r e p o r t e d t h a t A V M s d i d n o t cause p r i m a r y S A H 15' 25. A t present, however, a m o n g neur o s u r g e o n s there m a y be no firm consensus as to w h e t h e r a n A V M is a p a t h o l o g i c a l c o n d i t i o n c o m m o n l y
causing p r i m a r y S A H , such as a n e u r y s m r u p t u r e . T o elucidate the features o f h a e m o r r h a g e due to A V M r u p t u r e A V M p a t i e n t s with i n t r a c r a n i a l h a e m o r r h a g e c o n f i r m e d by C T in the acute stage, b e l o n g i n g b o t h to the a u t h o r ' s m a t e r i a l as well as to literature r e p o r t s , are reviewed.
Material and Methods Included in the present study were patients seen at the author's institute and the literature, who had been diagnosed as having intracranial AVMs by cerebral angiography, and in whom intracranial haemorrhage had been confirmed by CT in the acute stage. Patients with a dural AVM or an associated intracranial aneurysm were excluded. Fifty patients presented at the Department of Neurosurgery, Tokyo Metropolitan Fuehu Hospital, between 1978 and 1989, after the introduction of CT. There were 30 males and 20 females, ranging in age from 5 to 78 years, with an average of 30 years (Table 1). The bleeding was classified as intracerebral haemorrhage (ICH), intraventricular haemorrhage (IVH), SAH, and subdural haematoma.
Table 1. Age in 50 Patients with Ruptured Arteriovenous Malformations Age (years)
Number of patients (%)
0-I0
8 (16)
11-20
11 (22)
21-30 31-40 41 50 51-60 61-70 71-80
14 (28) 3 (6) 10 (20) 2 (4) I (2) 1 (2)
N. Aoki: Ruptured Arteriovenous Malformations
93
Results
Table 2 shows the sites of the AVM in the author's series. The locations of haemorrhage are shown in Fig. 1: ICH in 30 patients (60%), ICH with IVH in 13 patients (26%), IVH in 4 patients (8%), SAH in 2 patients (4%), and subdural haematoma in one patient (2%). One patient each with SAH had the AVM in the left posterior temporal region (a 40-year-old female) and the cerebellar vallecula (a 44-year-old female). Isolated SAH on CT was revealed on the left temporal region and in the basal cistern, respectively. Table 3 reveals CT findings of patients in the literature available for review 9' 15, 17, 25. The majority of haemorrhage were ICH or IVH. In contrast, isolated SAH was shown to be very rare: it was noted in only three (4%) of 70 patients in the series of Miyasaka and his colleagues i7. Mitsugi et al. reported that two of 21 patients had ICH with SAH, in whom SAH was described to be secondary to ICH 15. Other series in the
Table 2. Site of Ruptured Arteriovenous Malformations in 50 Patients Site
Number of patients (%)
Cerebral hemisphere Corpus callosum/Ventricle Basal ganglia/Thalamus Cerebellum/Brain stem
35 3 8 4
Number of patients 30
m
(70) (6) (16) (8)
m
60%
20
13
26% 10 I
I I
4
I
I ICH
I
ICtI with IVtI
IVH
[Tqrm SAIl
SDH
Fig. 1. Site of haemorrhage caused by rupture of arteriovenous malformations confirmed by computed tomography in 50 patients. ICH Intracerebral haemorrhage, IVH intraventricular haemorrhage, SAH subarachnoid haemorrhage, SDH subdural haematoma
CT-era (not listed in Table 3) demonstrated that only two of 28 patients with various stages haemorrhage developed SAH 14. Forty-two patients with AVM rupture confirmed by CT or surgery were observed exclusively to have ICH or IVHS: Discussion
Despite the advent of CT, by which accurate pathological features can be delineated, some concepts in the pre-CT era remain without critical re-evaluation. SAH seems to be one of these conditions; i.e., a diagnosis of SAH may be made after obtaining bloody cerebrospinal fluid by lumbar puncture, despite the CT findings showing primary haemorrhage in the cerebral parenchyma or the ventricular system. It is not valid to diagnose a SAH in patients in whom subarachnoid blood was only secondarily drained from ICH or IVH. Moyamoya disease, which had been considered as one of the common diseases in Japan causing SAH in the pre-CT ear, has already been re-evaluted as being a condition developing ICH or IVH 1. On the other hand, ruptured AVMs are thought to escape from critical assessment by CT in terms of the pathological features of' the haemorrhage. The results obtained here indicate that primary SAH due to AVM rupture is rare. This observation has already been documented 14' 15,25, but it has not yet become a consensus among neurosurgeons. In patients with an AVM in the brain stem, extrapial location of the nidus is not exceptional ~9, probably presenting with primary SAH. As clearly demonstrated by recent advances of magnetic resonance imaging, however, the majority of AVMs have most parts of their nidus in the cerebral parenchyma. Consequently, rupture of AVMs commonly causes ICH or subsequent ventricular rupture. It is known that AVMs are not uncommonly associated with intracranial aneurysms, accounting for 3% 18, 7% 2I, 9% 23, and 17% 16in patients with AVMs. This high incidence of association is to be expectedbecause aneurysm formation is partly caused by haemodynamic stress 18. In the setting of the coexistence of an AVM and an aneurysm, it is important to identify the source of rupture when deciding the approach to treatment. There is an opinion that the safest approach to patients with this combination of lesions is to treat the aneurysm first, because haemodynamic changes after AVM removal may place the associated aneurysm at immediate risk 2. This approach is acceptable for patients with an undetermined source of rupture. However, it is reasonable to make the initial approach to
N. Aoki: Ruptured Arteriovenous Malformations
94
Table 3. Site of Haemorrhage in Patients with Ruptured Arteriovenous Malformations Confirmed by Computed Tomography in the Literature
Authors (year)
Total number of patients with intracranial haemorrhage
Number of patients by site of haemorrhage
Takahashi etal. TM (1982) Mitsugi etal, 13 (1985) Miyasaka etal. 15 (1989) Fu etaL 16 (1989)
10
7
3
21
7
12
70
25
42**
7
3
4
ICH
IVH
ICH with IVH
ICH with SAH
SAH
2*
ICH Intracerebral haemorrhage, IVH intraventricular haemorrhage, SAH subarachnoid haemorrhage. * SAH secondary to ICH. ** Including isolated IVH. the r u p t u r e d lesion in patients with the identified source of h a e m o r r h a g e . This c o n s i d e r a t i o n is particularly valuable in m a k i n g decision o n emergency surgery, or in p l a n n i n g the a p p r o a c h to the lesion in a critical area. T h e present study i n c l u d i n g the a a u t h o r ' s a n d rep o r t e d series revealed that only five of 158 patients (less then 4 % ) with r u p t u r e d A V M developed p r i m a r y SAH. F u r t h e r m o r e , in a large series which included 814 patients with p r i m a r y S A H in the CT-era, only 5 patients ( 0 . 6 % ) were caused by r u p t u r e o f A V M s 24. Thus, int r a c r a n i a l A V M s should n o t be classified as a m a i n disease causing SAH, b u t should be considered as a p a t h o l o g i c a l c o n d i t i o n c o m m o n l y p r o d u c i n g I C H or IVH.
Conclusion P r i m a r y S A H is rarely caused by r u p t u r e of A V M s . A r u p t u r e d A V M can be recognized as a pathological c o n d i t i o n c o m m o n l y p r e s e n t i n g with I C H or IVH. This i n f o r m a t i o n is o f value in identifying the source o f i n t r a c r a n i a l h a e m o r r h a g e in patients with the co-existence of a n A V M a n d a n a n e u r y s m , a n d provides a significant guideline for the treatment.
Acknowledgement The author wishes to express his appreciation to Dr. Yoshiaki Shiokawa for valuable discussions and co-operation.
Referenees 1. Aoki N, Mizutani H (1984) Does moyamoya disease cause subarachnoid haemorrhage? Review of 54 cases with intracranial
hemorrhage confirmed by computerized tomography. J Neurosurg 60:348-353 2. BatjerH, Suss RA, Samson D (1986) Intracranial arteriovenous malformations associated with aneurysms. Neurosurgery 18: 2935 3. Brown RD Jr, Wiebers DO, Forbes G, O'Fallon WM, Piepgras DG, Marsh WR, Maciunas RJ (1988) The natural history of unruptured intracranial arteriovenous malformations. J Neurosurg 68:352-357 4. Celli P, Ferrante L, Palma L, Cavedon G (1984) Cerebral arteriovenous malformations in children. Clinical features and outcome of treatment in children and in adults. Surg Neurol 22:43-49 5. Date H, Yamaura A, Namba H, Saeki N, Makino H, Watanabe Y, Isobe K, Sato M (1989) Arteriovenous malformations in children and adolescents.Treatment and outcome in 51 patients. Shoni No Noshinkei 14:223-229 (in Japanese) 6. Drake CG (1979) Cerebral arteriovenous malformations. Considerations for and experience with surgical treatment in 166 cases. Clin Neurosurg 26:145-208 7. Drake CG, Friedman AH, Peerless SJ (1986) Posterior fossa arteriovenous malformations. J Neurosurg 64:1-10 8. EirasJ0 Gom6z-Perfn J, Carcavilla LI, Alberdi J (1987) Surgical experience with arteriovenous malformations in children. Child's Nerv Syst 3:156-169 9. Fu Y, Hakuba A, Yasui T, Suzuki T, Baba M, Nishimura S (1989) Cerebral arteriovenous malformations with intracranial hematoma in children. Report of seven cases. Shoni No Noshinkei 14:45-50 (in Japanese) 10. Gerosa MA, Cappellotta P, Licata C, Iraci G, Pardatscher K, Fiore DI (1981) Cerebral arteriovenous malformations in children (56 cases). Child's Brain 8:356-371 11. Giombini S, Bruzzone MG, Pluchino F, (1988) Subarachnoid hemorrhage of unexplained cause. Neurosurgery 22:313-316 12. Graf CJ, Perret GE, Torner JC (1983) Bleeding from cerebral arteriovenous malformations as part of their natural history. J Neurosurg 58:331-337
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Correspondence and Reprints: Nobuhiko Aoki, M. D., Department of Neurosurgery, Tokyo Metropolitan Fuchu Hospital, 29-2 Musashidai, Fuchu-Shi, Tokyo 183, Japan.
