Acta Neurochir (Wien) (1999) 141: 315±319
Acta Neurochirurgica
Multiple Cerebral Arteriovenous Malformations (AVMs) Associated with
Spinal AVM
S. Hasegawa1, J.-I. Hamada1, M. Morioka1, Y. Kai1, S. Takaki2, and Y. Ushio1
1 Department of Neurosurgery, Kumamoto University Medical School, Kumamoto, Japan
2 Kumamoto City Hospital, Kumamoto, Japan
Summary
The co-existence of multiple cerebral arteriovenous malforma-
tions (AVMs) and a spinal AVM is extremely rare. A 22-year-old
man suddenly developed severe headache. Computed tomography
(CT) scan showed intracerebral haemorrhage in the left occipital
lobe. Cerebral angiography revealed eight AVMs; four were in the
right frontal lobe and two each were in the right temporal and left
occipital lobe, respectively. A huge high-¯ow spinal AVM was found
incidentally. He had no other vascular lesions such as hereditary
haemorrhagic telangiectasia. A left occipital craniotomy was per-
formed and the ruptured left occipital AVMs were removed. Further
therapeutic treatment was refused. To our knowledge, except for one
autopsy case, this is the ®rst reported patient with multiple cerebral
AVMs with a spinal AVM. We discuss the characteristics of this case
and review reported cases with cerebral and spinal AVMs.
Keywords: Multiple; cerebral arteriovenous malformations; spinal
arteriovenous malformations.
Introduction
Multiple cerebral arteriovenous malformations
(AVMs) are rare; their incidence ranges from 0.3 to
4.9% in all AVM patients [1, 5, 16, 18, 19, 26]. Spinal
AVMs are also fairly rare; their incidence is one tenth
that of cerebral AVMs [21]. To date, 5 cases with single
cerebral AVMs with a single spinal AVM [7, 9, 14, 17,
24] and only one autopsy case of multiple cerebral
AVMs with a spinal AVM [15] have been reported. We
now report an extremely rare case of multiple cerebral
AVMs with a spinal AVM.
Case Report
A 22-year-old man was admitted to our hospital on September 22,
1995 because of sudden severe headache. He had been healthy and
his past history and family history were unremarkable. On neuro-
logical examination, right homonymous hemianopsia was noted. A
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computed tomography (CT) scan showed a left occipital intra-
cerebral haematoma. Left vertebral angiography demonstrated two
separate AVMs, one fed by the left calcarine artery and drained into
the superior sagittal sinus, the other fed by the left posterior temporal
artery and drained into the left transverse sinus (Fig. 1). A right
carotid angiogram revealed an additional six distinct AVMs. Four of
these were in the right frontal lobe and two were in the right temporal
lobe (Fig. 2). The left carotid angiogram was normal. A general
physical examination revealed no abnormality and neither heredi-
tary haemorrhagic telangiectasia nor other vascular anomalies were
found. On general examination, the abdominal contrast-enhanced
CT scan showed a curious enhancing lesion in the spinal canal.
Magnetic resonance angiography (MRA) revealed a huge spinal
vascular malformation. Spinal angiography with selective catheter-
ization of the segmental arteries disclosed a juvenile type spinal
AVM at the L-1 level. It was supplied by the anterior spinal arteries
from the right ninth intercostal artery and the posterior spinal
arteries from the bilateral seventh intercostal arteries and drained
into the inferior vena cava (Fig. 3). On October 9, 1995, a left occi-
pital craniotomy was performed and the haematoma was removed to
prevent rebleeding and to obtain a pathological diagnosis of the left
occipital AVMs. Histopathological examination showed that the
dilated vein consisted of an arterial component surrounded by
crowds of small arteries (Fig. 4). A diagnosis of AVM was made.
The patient's postoperative course was uneventful and he refused
further treatment for the other vascular lesions. He was discharged in
good condition on November 2, 1995, with an uneventful postoper-
ative course to date.
Discussion
The incidence of multiple cerebral AVMs (MC-
AVM) is rare, ranging from 0.3 to 4.9% of all cerebral
AVMs and we calculate that among 1850 AVM
patients reported in the literature [1, 5, 16, 18, 19, 26],
34 (1.84%) had multiple AVMs. The incidence of spi-
nal AVM is one-tenth that of cerebral AVMs [21].
Multiple cerebral AVMs with a spinal AVM (MCS-
AVM) are extremely rare; only one other case has been
reported in the literature [15]. Single cerebral AVM
316 S. Hasegawa et al.

Fig. 1. Left vertebral angiogram showing two separate ruptured AVMs (arrows 1, 2) in the left occipital lobe. (a arterial phase; b venous
phase)

Fig. 2. Right carotid angiogram demonstrating six AVMs; four lesions (arrows 3, 4, 5, 6) are in the right frontal lobe, two (arrows 7, 8) are in
the right temporal lobe. (a arterial phases; b venous phase)

with a spinal AVM (CS-AVM) is also rare; to our
knowledge, only ®ve such cases have been reported
[7, 9, 14, 17, 24].
Table 1 summarizes the 6 cases found in our search
of the literature and the patient presented here. The
cerebral AVMs were graded as small (< 3 cm), me-
dium (3 to 6 cm), or large (> 6 cm) and the pattern of
venous drainage was classi®ed super®cial or deep, ac-
cording to the grading system proposed by Spetzler
and Martin [20]. The spinal AVMs were classi®ed as
single coiled, glomus and juvenile types [4]. Age at
presentation ranged from 1.3 years to 50 years (mean
22 years); there were 4 male and 3 female patients.
Among the 16 cerebral AVMs, 14 were in supra-
tentorial regions: 9 in the right, 5 in the left hemi-
sphere, 2 of the remaining cerebral AVMs were in the
posterior fossa. Thus, the distribution of age, sex and
lesion site in patients with MCS-AVM and CS-AVM
was essentially the same as that in patients with multi-
ple AVMs.
There are some characteristic features in patients
with MCS-AVM and CS-AVM. Willinsky, et al. [26]
reported a high incidence of small AVMs (30%) in
patients with multiple cerebral AVMs, however, of
the 16 patients with cerebral AVMs, 15 (94%) had
small AVMs. Furthermore, in the latter group of pa-
Multiple Cerebral and Spinal AVMs
Fig. 3. Spinal MRA showing a huge high-¯ow juvenile-type AVM
which is mainly fed by the anterior spinal artery and drained into a
varicose vein (arrow). (arrow drainer of the spinal AVM, arrowheads
kidney)
tients, there were no cerebral aneurysm. Among the
cerebral AVM patients, 2.7±23% demonstrated cere-
bral aneurysm formation [13]. This di¨erence may be
attributable to the size of the AVMs, that is, in cases
with small AVMs, the haemodynamic stress on the
317
feeding artery is lower than is the case in patients with
larger AVMs. Most of the cerebral AVMs drained into
a super®cial vein (12 of 13 available AVMs, 3 were
unavailable for drainage determination). In 5 of 7 pa-
tients from this group (71%) there was AVM haemor-
rhage resulting in subarachnoid haemorrhage (SAH),
intracerebral haemorrhage (ICH) or intraventricular
haemorrhage (IVH). Also, most patients from this
group (71%) had spinal symptoms; SAH was most
common. SAH was an uncommon symptom in pa-
tients with spinal AVM. Many of the spinal AVMs
were located in the lower thoracic or lumbar spinal
cord (5 of 7 AVMs); this was common for all spinal
AVMs [2]. The glomus type was most frequent (3 of 5
clearly de®ned spinal AVMs), although it has been re-
ported the the juvenile type is most frequent in spinal
AVM patients [3].
There were some distinctive features in patients with
MCS-AVM and those with CS-AVM. AVMs are
congenital lesions arising at an early embryonic stage
(at about 3 weeks of gestation) before the di¨erentia-
tion of arteries, capillaries and veins [22]. Tamaki,
et al. [23] suggested multiple developmental defects or
multiple failures in the persistence of primitive capil-
lary beds as the pathogenesis of multiple AVMs. Re-
cently, some insights have been gained into the em-
bryological programme determining the development
of normal arteriovenous anatomy and interventing
capillary network formation [25]. These ephrin/ephrin
receptor interactions are likely to regulate human vas-
cular development as well, and multiple AVMs may
represent a widespread disturbance in these early em-
bryological functions. Interestingly, we found no other
Fig. 4. Pathological examination of the
resected AVM showed a dilated vein con-
sisting of the arterial structure (arrows)
and crowds of small arteries (arrowheads).
(Elastic van Gieson. 20. Original mag-
ni®cation)
318 S. Hasegawa et al.

Table 1. Co-Existence of Cerebral and Spinal AVMs

Authors Age/sex Symptoms Site of AVMs (no.) Venous drainage of cerebral AVM Size of cerebral AVMs
super®cial or deep (no.) or type of spinal AVMs (no.)

Hash, et al. 24/M ± Rt.tent. (1) super®cial smalla

back pain (SAH) T9-10 (1) glomusb
Ho¨man, et al. 1.3/M headache (SAH) Rt.temp. (1) super®cial small
leg weakness T2-10 (1) glomus
Parkinson, et al. 47/M headache (SAH) Lt.temp. (1) super®cial small
neck pain (SAH) T11-L1 (1) single coiledb
Moss, et al. 50/F ± Rt.cau. (1) N.A. small
(autopsy case) ± Lt.front. (1) N.A. small
± P.-M. junction (1) N.A. small
leg pain (SAH) T6-7 (1) N.A.
Mizutani, et al. 7/F cons. dis. (ICH) Cerebellum (1) super®cial mediuma
± C1-2 (1) N.A.
Tsurushima, et al. 3/F cons. dis. (IVH) Lt.temp. (1) deep small
paraparesis (SAH) L2 (1) glomus
Our case 22/M ± Rt.front. (4) super®cial (4) small (4)
± Rt.temp. (2) super®cial (2) small (2)
headache (ICH) Lt.occip. (2) super®cial (2) small (2)
± L1 (1) juvenile

SAH Subarachnoid haemorrhage; ICH intracerebral haemorrhage; IVH intraventricular haemorrhage; Cons. dis. disturbane of conscious-
ness disturbance; tent. tentorium; front. frontal; temp. temporal; occip. occipital; cau. caudate nucleus; P.-M. ponto-medullary; C cervical;
T thoracic; L lumbar; Rt. right; Lt. left; N.A. not available; *a Ref. [20]; *b Ref. [4].

congenital vascular anomalies in the group we re-
viewed, except for one case [14]. However, multiple
AVMs may be attributable to some other yet un-
identi®ed pathogenesis or to some strong embry-
ogenetic aberration which may be di¨erent from that
found in patients with single cerebral AVM.
At present there is no consensus regarding the most
appropriate treatment for patients with multiple
AVMs and no results of large series are currently
available. The overall bleeding risk of AVM's is re-
ported to be 2 to 3% [6, 8, 12], and Itoyama, et al. [11],
reported that in the ®rst year rebleeding occured in
6.9% of patients. The natural history of multiple
AVMs remains unclear. Radiosurgery or embolization
has been suggested as a useful modality added to the
surgical treatment of patients with multiple cerebral
AVMs [5, 10, 24, 27]. However, the therapeutic strat-
egy for multiple AVMs remains di½cult, especially if
there are multiple scattered lesions. In our case, the
ruptured AVMs were resected, but the other residual
multiple cerebral AVMs and the spinal AVM re-
mained untreated because the patient refused further
treatment.
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Comments
This is an interesting case report of a patient with multiple cerebral
AVMs in association with an L1 spinal AVM. This is a rare case as
the authors note. While it was previously thought that multiple ce-
rebral AVMs could only be seen in the setting of Osler-Weber-Rendu
disease, it has since been found that multiple lesions may be seen in
the absence of this disease, as recorded in the present report.
From our reading of the literature, however, we would disagree
with the authors on a few points. First, the authors note on page 2
of the manuscript that this is the ``®rst report'' of a case of multiple
cerebral AVMs associated with a spinal AVM. In our review, this is
the third report. In fact, the authors reference the other two cases:
Moss et al. in Neuroradiology 1989 (an autopsy case), and Mitzutani
et al. in Neurosurgery 1992 (two cerebellar AVMs and a spinal cord
AVM).
Second, the authors note 5 previously reported cases of a single
cerebral AVM associated with a spinal AVM. They fall to note the
earliest reported cases by Di Chiro et al. in Brit J Radiol 45: 533±560,
1972 and in J Neurosurg 39: 1±29, 1973. Although exact details are
not described in these cases, they were the ®rst reports of this com-
bined pathology.
With these corrections, the manuscript is an interesting case report
and review of the literature worthy of publication. It presents a rare
constellation of lesions which prompts discussion on AVM actiology
and the challenges faced in treatment of multiple lesions.
M. Alexander and R. Spetzler
Correspondence: Shu Hasegawa, M.D., Department of Neuro-
surgery, Kumamoto University Medical School, 1-1-1 Honjo, Ku-
mamoto 860-0811, Japan.