Neuro-radiology

Neuroradiology (1994) 36:15%159

9 Springer-Verlag 1994

Multiple intracranial arteriovenous malformations: a case report
K. Ericson 1, M. S/Jderman 1, B. Karlsson 2, W. Y. Guo 1, C. Lindquist 2
1Department of Neuroradiology, Karolinska Hospital, S-104 01 Stockholm, Sweden
2 Department of Neurosurgery, Karolinska Hospital, S-104 01 Stockholm, Sweden
Received: 11 November 1992/Accepted: 14 February 1993

Abstract. Multiple intracranial arteriovenous malformations are rare. T h e r e are a few cases in the literature with
up to three malformations in one patient. A child with
seven separate cerebral malformations is now described.
There was no history of haemorrhage, but only of febrile
seizures. The malformations were discovered at CT and
verified at angiography. Six were selected for stereotaxic
irradiation with the multicobalt unit. The seventh was
considered too big for irradiation and suitable for surgery.

treatment by stereotaxic irradiation. It was noted that one AVM in
the right temporal lobe was rather large, but could probably be
treated with an acceptable risk of undue radiation effects. The other
AVMs were small. The quality of the images did not, however, permit more detailed analysis of the actual size and shape of the niduses.
Angiography with a stereotaxic frame prior to treatment showed
seven separate intracranial AVMs (Figs. 1,2) in the cerebral hemispheres. The one in the right temporal lobe was large, its diameter
exceeding 3 cm. It was superficially located, and was judged unsuitable for irradiation but suitable for open surgery. The remaining
six malformations were considerably smaller and ideal targets for
stereotaxic irradiation.

Key words: A V M - Stereotaxic irradiation - Angiography

Discussion
Intracranial arteriovenous malformation (AVM) is a congenital lesion that is usually single. Although true AVMs
are often supplied from different arterial territories, each
feeding artery supplying its own part of the malformation,
the malformation usually forms a continuous nidus.
AVMs are rare, with a reported incidence of 0.1-0.2 % [1];
multiple intracranial AVMs are extremely rare, their incidence, estimated by Stone et al. [2] being 0.002 %.
Cavernous h a e m a n g i o m a s are often multiple. They are
now found m o r e commonly, because of increased use of
magnetic resonance imaging [3, 4]. Patients with different
kinds of vascular malformation have b e e n described [5, 6];
cavernous h a e m a n g i o m a s are sometimes seen in combination with AVMs or venous anomalies [5].

Case report
A girl aged 7 years had fits during periods of fever. There were no
symptoms or signs, in particular none suggesting generalised vascular disorder. Such disease could not be found in the family either.
Contrast-enhanced CT (8 mm slice thickness) disclosed two
AVMs, but angiography performed revealed six separate AVMs. A
second contrast-enhanced CT (4 mm slice thickness) 18 months
later showed five AVMs, three of which then showed evidence of
previous haemorrhage. The patient was subsequently referred for

Correspondence to: K. Ericson

Karolinska Hospital has m o r e than 20 years experience
with irradiation of AVMs by the multicobalt unit ( g a m m a
knife radiosurgery) [7-12]. F r o m over 3000 AVMs reviewed at our institution m o r e than 1000 have b e e n
treated with g a m m a knife surgery. A m o n g these
3000 cases were ten with m o r e than one intracranial nidus.
Seven patients with two or m o r e separate nidi have b e e n
treated by stereotaxic irradiation, including the present
patient. Two patients are lost to angiographic follow-up,
one has recently b e e n treated and one is awaiting treatment. O f two patients treated m o r e than two years ago the
lesions have been totally obliterated in one and partially in
the other. The remaining three patients, all of w h o m had
two nidi, were not accepted for treatment.
The combination of multiple intracranial, spinal and
pulmonary AVMs is recognised [13-15], as is an association with hereditary haemorrhagic telangiectasia
(Rendu-Osler-Weber disease). It was stated by M a r y a m a
et al. [15] that in this disease pulmonary arteriovenous fistulae are m o r e frequent than other vascular lesions in liver
or brain. Multiple cerebral AVMs and soft-tissue vascular
malformations, possibly representing Rendu-OslerWeber disease, were also described by H a n i e h et al. [16].
Occasional patients with multiple AVMs have b e e n reported by others [17-22]. Voigt et al. [23] described
multiple AVMs in a patient who also had multiple arterial
aneurysms and general arterial ectasia.

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Fig.1. a Left carotid angiogram
(lateral view) showing three small
arteriovenous malformations (outlined).
b Right vertebral angiogram showing large temporal and small parieto-occipital malformations.
c Right carotid angiogram showing
four AVMs, one of which is partly
shown in b
Fig.2. a Right and
h left carotid angiogram (AP-view)
showing the malformations
The incidence of multiple AVMs is extremely low.
Cerebral angiography carries a risk, albeit low, of serious
complications. It is therefore not mandatory to perform
complete cerebral angiography as a screening procedure
to rule out multiple lesions in patients with a known AVM
but without any clinical or radiological evidence of additional lesions. However, all possible feeders, including the
external cerebral arteries, should of course be injected for
complete angiographic mapping of an AVM, so that four
vessel cerebral angiography may be necessary. MRI and
MR angiography (MRA) are becoming more and more
important in the complete mapping of an AVM, and M R A
will probably replace conventional angiography in many
of these patients.
Due to the extremely low incidence of multiple AVMs
no material large enough for statistical analysis exists. We
have, however, no reason to suppose that multiple AVMs

behave differently from a single AVM when irradiated. A
large series of single AVMs irradiated at Karolinska Hospital [10] showed complete obliteration in 87 % at 3 year
follow up. Therefore, the changes of complete obliteration of all six AVMs irradiated in this patient within a
three year period could be estimated at approximately
43 %. Undue radiation effects are a function of the size of
the irradiated volume, the dose delivered and the patient's
individual sensitivity to radiation. The very steep dose
gradient of the gamma knife makes the cumulative dose to
the brain very small [24, 25], and the risk of undue radiation effects should, for each AVM, be unaltered compared
to the risk incurred when irradiating single AVMs.
The risk of haemorrhage from intracranial arteriovenous malformations has been estimated to 2-4 per cent per
year per lesion [1,26, 27]. Since the second CT showed evidence of previous bleeding the patient must be considered

159
l u c k y n o t to h a v e s u f f e r e d significant i n t r a c r a n i a l h a e m o r r h a g e p r i o r to t r e a t m e n t . S t e r e o t a x i c i r r a d i a t i o n usually
causes o b l i t e r a t i o n o f t h e A V M a f t e r 2 - 3 y e a r s [10], a n d
t h e b l e e d i n g risk is b e l i e v e d t o b e s u b s t a n t i a l l y u n c h a n g e d
until c o m p l e t e o b l i t e r a t i o n is a c h i e v e d . T h e p a t i e n t is
t h e r e f o r e still at risk. S e v e r a l o f the A V M s c o u l d b e o p e r a t e d u p o n or t r e a t e d b y i n t e r v e n t i o n a l n e u r o r a d i o l o g y .
T h e risk w o u l d t h e n b e h i g h l y d e p e n d e n t o n i n d i v i d u a l
skills b u t t h e risk o f b l e e d i n g w o u l d b e e l i m i n a t e d i m m e diately by total extirpation.

References
1. Wilkins R (1985) Natural history of intracranial vascular malformations: a review. Neurosurgery 16:421-430
2. Stone J, Crowell R, Lisner B, Naseem M, Oldershaw J (1983) Bilateral parietal arteriovenous malformations. Report of a case.
Neurosurgery 13:58%592
3. Gomori J, Grossman R, Goldberg H, Hackney D, Zimmerman
R, Bilaniuk L (1986) Occult cerebral vascular malformations:
high field MR imaging. Radiology 158:707-713
4. Lemme-Plaghos L, Kucharczyk W, Brant-Zawadzki M, Uske A,
Edwards M, Norman D, Newton T (1986) MR imaging of angiographically occult vascular malformations. AJNR 7:217-222
5. Lee KS, Spetzler RF (1990) Spinal cord cavernous malformation
in a patient with familial intracranial cavernous malformations.
Neurosurgery 26:877-880
6. Moss JG, Sellar RJ, Hadley DM (i989) Intracerebral and spinal
vascular malformation in a patient without hereditary haemorrhagic telangiectasia. Neuroradiology 31:280-281
7. Leksell D (1987) Stereotactic radiosurgery present status and future trends. Neurol Res 9:59-68
8. Steiner L (1988) Stereotactic radiosurgery with the 6~ gamma
unit in the surgical treatment of intracranial tumors and arteriovenous malformation. In: Schmidek H, Sweet W (eds) Operative neurosurgical techniques. Grune & Stratton, Orlando,
pp 515-529
9. Steiner L (1984) Treatment of arteriovenous malformation by
radiosurgery. In: Wilson C, Stein B (eds) Intracranial arteriovenous malformations. Williams & Wilkins, Baltimore, pp 295-313
10. Lindquist C, Steiner L (1988) Stereotactic radiosurgicaI treatment of arteriovenous malformations. In: Lunsford LD (ed)
Modem stereotactic neurosurgery. Martinus Nijhoff, Dordrecht,
pp 491-505
11. Greitz T, Lax I, BergstrOm M, Arndt J, Berggren B, Blomgren H,
Boethius J, Lindqvist M, Ribbe T, Steiner L (1986) Stereotactic
radiation therapy of intracranial lesions: methodology aspects.
Acta Radiol Onco125:81-89

12. Leksell L (1951) The stereotaxic method and radiosurgery of the
brain. Acta Chir Scand 102:316-319
13. Kawaguchi T, Fujita S, Yamada H, Nishida Y, Izawa I (1990)
Multiple cerebral and pulmonary arteriovenous malformations
in association with brain and subcutaneous abscesses: a possible
variant of hereditary hemorrhagic telangiectasia - case report.
Neurol Med Chir (Tokyo) 30:272-276
14. Gold MH, Eramo L, Prendiville JS (1989) Hereditary benign
telangiectasia. Pediatr Dermatol 6:194-197
15. Maruyama J, Watanabe M, Onodera S, Hasebe N, Yamashita H,
Tobise K (1989) A case of Rendu-Osler-Weber disease with cerebral hemangioma, mukiple pulmonary arteriovenous fistulas
and hepatic arteriovenous fistula. Jpn J Med 28:651-656
16. Hanieh A, Blumbergs P, Carney P (1981) Multiple cerebral arteriovenous malformations associated with soft-tissue vascular
malformations. Case report. J Neurosurg 54:670-672
17. Berenstein A (1981) Technique of catheterization and embolization of the lenticulate arteries. J Neurosurg 54:783-789
18. H66k O, Johannson C (1958) Intracranial arteriovenous aneurysms. A follow up study with particular attention to their
growth. Arch Neurol Psychiat 80:39-54
19. Monaco RG, Alvarez H, Goulao A, Pruvost P, Lasjaunias P
(1990) Posterior fossa arteriovenous malformations. Neuroradiology 31:471-475
20. Willinsky RA, Lasjaunias P, Terbrugge K, Burrows P (1990)
Multiple cerebral arteriovenous malformations (AVMs). Review of our experience from 203 patients with cerebral vascular
lesions. Neuroradiology 32:207-210
21. Schlachter L, Fleischer A, Faria M, Tindall G (1980) Multifocal
intracranial arteriovenous malformations. Neurosurgery 7: 440444
22. Zellem R, Buchheit W (1985) Multiple intracranial arteriovenous malformations; case report. Neurosurgery 17:88-93
23. Voigt K, Beck U, Reinshagen G (1973) A complex cerebral vascular malformation studied by angiography. Neuroradiology 5:
117-123
24. Wennerstrand J, Ungerstedt U (1970) Cerebral radiosurgery.
Acta Chir Scand 133-137
25. Larsson B, Liddn K, Sarby B (1974) Irradiation of small structures through the intact skull. Acta Radiol (Ther Phys Biol) 512534
26. Brown R, Wiebers D, Forbes G, O'Fallon W, Piepgras D, Marsh
W, Maciunas R (1988) The natural history of unruptured intracranial arteriovenous malformations. J Neurosurg 68:352-357
27. Ondra S, Troupp H, George E, Schwab K (1990) The natural history of symptomatic arteriovenous malformations of the brain; a
24-year follow-up assessment. J Neurosurg 73:387-391