Multiple Cerebral Arteriovenous Malformations (AVMs) Associated withSpinal AVM

S. Hasegawa1, J.-I. Hamada1, M. Morioka1, Y. Kai1, S. Takaki2, and Y. Ushio1

1Department of Neurosurgery, Kumamoto University Medical School, Kumamoto, Japan

2Kumamoto 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

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

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Acta Neurochir (Wien) (1999) 141: 315±319

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-

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)

316 S. Hasegawa et al.

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

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. 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)

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)

Multiple Cerebral and Spinal AVMs 317

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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Table 1. Co-Existence of Cerebral and Spinal AVMs

Authors Age/sex Symptoms Site of AVMs (no.) Venous drainage of cerebral AVM

super®cial or deep (no.)

Size of cerebral AVMs

or type of spinal AVMs (no.)

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

back pain (SAH) T9-10 (1) glomus�b

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 coiled�b

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 medium�a

± 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].

318 S. Hasegawa et al.

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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.

Multiple Cerebral and Spinal AVMs 319