Acta Neurochir (Wien) (1999) 141: 315±319
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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
The co-existence of multiple cerebral arteriovenous malformations (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 performed 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 . 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  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 neurological examination, right homonymous hemianopsia was noted. A
computed tomography (CT) scan showed a left occipital intracerebral 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 hereditary 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 catheterization 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 occipital 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 postoperative course to date.
Discussion The incidence of multiple cerebral AVMs (MCAVM) 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 spinal AVM is one-tenth that of cerebral AVMs . Multiple cerebral AVMs with a spinal AVM (MCSAVM) are extremely rare; only one other case has been reported in the literature . Single cerebral AVM
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), medium (3 to 6 cm), or large (b 6 cm) and the pattern of venous drainage was classi®ed super®cial or deep, according to the grading system proposed by Spetzler and Martin . The spinal AVMs were classi®ed as single coiled, glomus and juvenile types . 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 supratentorial regions: 9 in the right, 5 in the left hemisphere, 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 multiple AVMs. There are some characteristic features in patients with MCS-AVM and CS-AVM. Willinsky, et al.  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 cerebral aneurysm formation . 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 patients from this group (71%) there was AVM haemorrhage 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 patients 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 . The glomus type was most frequent (3 of 5 clearly de®ned spinal AVMs), although it has been reported the the juvenile type is most frequent in spinal AVM patients . 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¨erentiation of arteries, capillaries and veins . Tamaki, et al.  suggested multiple developmental defects or multiple failures in the persistence of primitive capillary beds as the pathogenesis of multiple AVMs. Recently, some insights have been gained into the embryological programme determining the development of normal arteriovenous anatomy and interventing capillary network formation . These ephrin/ephrin receptor interactions are likely to regulate human vascular development as well, and multiple AVMs may represent a widespread disturbance in these early embryological functions. Interestingly, we found no other
Fig. 4. Pathological examination of the resected AVM showed a dilated vein consisting of the arterial structure (arrows) and crowds of small arteries (arrowheads). (Elastic van Gieson. Â20. Original magni®cation)
Table 1. Co-Existence of Cerebral and Spinal AVMs Authors Hash, et al. Ho¨man, et al. Parkinson, et al. Moss, et al. (autopsy case) Mizutani, et al. Age/sex 24/M 1.3/M 47/M 50/F Symptoms ± back pain (SAH) headache (SAH) leg weakness headache (SAH) neck pain (SAH) ± ± ± leg pain (SAH) cons. dis. (ICH) ± cons. dis. (IVH) paraparesis (SAH) ± ± headache (ICH) ± Site of AVMs (no.) Rt.tent. (1) T9-10 (1) Rt.temp. (1) T2-10 (1) Lt.temp. (1) T11-L1 (1) Rt.cau. (1) Lt.front. (1) P.-M. junction (1) T6-7 (1) Cerebellum (1) C1-2 (1) Lt.temp. (1) L2 (1) Rt.front. (4) Rt.temp. (2) Lt.occip. (2) L1 (1) Venous drainage of cerebral AVM super®cial or deep (no.) super®cial super®cial super®cial N.A. N.A. N.A. super®cial deep super®cial (4) super®cial (2) super®cial (2)
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Size of cerebral AVMs or type of spinal AVMs (no.) smallÃa glomusÃb small glomus small single coiledÃb small small small N.A. mediumÃa N.A. small glomus small (4) small (2) small (2) juvenile
Tsurushima, et al. 3/F Our case 22/M
SAH Subarachnoid haemorrhage; ICH intracerebral haemorrhage; IVH intraventricular haemorrhage; Cons. dis. disturbane of consciousness 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. ; *b Ref. .
congenital vascular anomalies in the group we reviewed, except for one case . However, multiple AVMs may be attributable to some other yet unidenti®ed pathogenesis or to some strong embryogenetic 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 reported to be 2 to 3% [6, 8, 12], and Itoyama, et al. , 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 strategy 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 remained untreated because the patient refused further treatment. References
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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 cerebral 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 combined 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 Neurosurgery, Kumamoto University Medical School, 1-1-1 Honjo, Kumamoto 860-0811, Japan.