British Journal of Radiology (2006) 79, e12-e15
© 2006 British Institute of Radiology
doi: 10.1259/bjr/40183814
Unilateral moyamoya disease with co-existing arteriovenous malformation
O Nawawi, MBBS, MRad, FRCR1,
M Sinnasamy, MBBS, MRad2 and
N Ramli, MBBS, FRCR1
1 Department of Radiology, University Malaya Medical Centre, Kuala Lumpur 59100, 2 Department of Medicine, Unit of Radiology, Universiti Putra Malaysia, Kuala Lumpur, Malaysia
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Abstract
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A case of an intracerebral bleed in a young man with a rare combination of arteriovenous malformation (AVM) and unilateral moyamoya disease is presented. The location of the bleed in the left basal ganglia corresponded to the area supplied by the basal moyamoya vessels. The AVM which received supply from collateral moyamoya vessels as well as normal cerebral arteries was located in the ipsilateral parieto-occipital region posterior to the basal ganglia bleed. This is the first reported cerebral AVM co-existing with a unilateral moyamoya disease in the English literature. Unusual features of the case such as the unilaterality of the angiographic abnormalities, their coexistence and hypotheses as to their development are discussed.
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Introduction
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The term moyamoya is a Japanese word which means "a puff of smoke". It was coined by Suzuki and Takaku in 1969 to describe the angiographic appearance of the fine, telangiectatic collateral vessels at the base of the brain in a group of 21 patients with internal carotid arterial occlusion [1]. The disease was typically seen involving both internal carotid arteries at their clinoid portion. Moyamoya disease has been associated with other vascular diseases such as aneurysm and AVM. The aneurysms which may either be true saccular aneurysms or microaneurysms arise in the telangiectatic net of collaterals, and are a frequent cause of haemorrhage in moyamoya disease [2].
The coexistence of moyamoya disease and AVM, however, is thought to be very unusual. Currently there are 14 reported cases in the literature, 13 of which have bilateral moyamoya disease involvement. There is one case of unilateral moyamoya disease associated with a dural AVM reported in the Japanese literature [3–14].
The association between these two vascular abnormalities is still unexplained. Previous authors have offered several hypotheses, but the possibility of chance still cannot be excluded.
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Case report
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A previously healthy 35-year-old gentleman presented to the emergency department with a sudden episode of generalized tonic clonic seizure 2 h earlier. The seizure, which lasted for 15 min, occurred while he was having a bath. Another similar episode was observed in the emergency department. There was no history of previous tuberculosis or substance abuse. The patient was not on any medication.
On clinical examination, the patient was noted to be drowsy, aphasic and had right hemiplegia. He was afebrile, and clinical examination of the cardiovascular/respiratory systems and abdomen were normal. Laboratory studies, which included electrolytes, coagulation profile and urinalysis, were normal.
An urgent non-contrasted CT examination of the brain revealed a left basal ganglia bleed measuring 4 cmx2.5 cm in diameter. Also seen was a focus of calcification in the left posterior parietal area with no associated mass effect (Figure 1
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Figure 1. Non enhanced CT of the brain showing a left basal ganglia haematoma with associated mass effect. A focus of calcification is seen in the left posterior parietal region.
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Cerebral angiogram performed the following day showed stenosis of the supraclinoid left internal carotid artery with occlusion of the proximal left middle cerebral artery. There was also narrowing of the A1 segment of the left anterior cerebral artery. Multiple tiny collaterals were seen arising in the area of the lenticulostriate branches giving a "puff of smoke" appearance (Figure 2). The location of these collateral vessels corresponded to the region of basal ganglia bleed seen on the CT. More peripherally in the left parietal region, an arteriovenous malformation (AVM) was seen with the nidus measuring 3 cm in diameter. The feeding arteries were from the branches of the left anterior cerebral artery, collaterals of the occluded left-middle cerebral artery and branches of the left superior cerebellar artery. This vascular malformation appeared early in the arterial phase of the angiogram. There was retrograde filling of the distal cortical left middle cerebral artery from the AVM nidus. The AVM drained into the left sigmoid sinus with no deep venous drainage seen. The right sided cerebral angiogram was normal.
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Figure 2. Left internal carotid angiogram in Towne's (upper) and lateral (lower) projection, showing occluded left middle cerebral with associated small collateral lenticulostriate vessels (arrow). Posterolaterally an arteriovenous malformation (AVM) is seen, partly supplied by the moyamoya collateral vessels and draining into the left sigmoid sinus.
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The patient was managed conservatively with antiepileptic medication (Dilantin). In the ward, he gradually regained full consciousness and speech, but with residual right hemiparesis for which physiotherapy was instituted. Unfortunately, the outcome of this patient is unknown as he decided to return to his country of origin for further treatment.
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Discussion
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Moyamoya is an occlusive cerebrovascular disease characterized by cerebral angiographic features consisting of intracranial stenosis or occlusion of the internal carotid artery or its terminal branches associated with telangiectatic collateral vessels at the base of the brain [1]. In addition to the enlarged lenticulostriate and thalamoperforating arteries, multiple leptomeningeal and transdural anastomoses develop between the cortical arteries and those of dura mater, scalp, and orbit [2]. The aetiology of this vascular abnormality remains unclear. Opinion is still divided between a congenital versus acquired aetiology. It is usually a bilateral disease, however, atypical unilateral involvement has been reported [15–17]. Although a number of factors have been suggested as the cause of unilateral diseases, in the majority of cases the cause is still inapparent. The onset of symptoms in moyamoya disease has been known to occur in two peaks, the first decade and the fourth decade. Recurrent episodes of sudden hemiplegia, headache and convulsive manifestations occur more frequently in paediatric patients, while subarachnoid or intracerebral bleeding is usually the presenting finding in adults [18]. After a progressive course for many years, the disease frequently stabilizes with residual disability.
Cerebral AVM is a congenital abnormality consisting of a nidus of abnormal dilated tortuous arteries and veins with a tangle of closely packed pathologic vessels, resulting in shunting of blood from arterial to venous side without intermediary capillary bed. It is known to be accompanied by a variety of dysplasias involving the feeding arteries and draining veins. Occlusions, stenoses, aneurysms and ectasias are the dysplastic changes affecting the feeding arteries and draining veins. Flow related arterial aneurysms, as well as venous occlusions or stenoses, have been shown to have an increased risk of haemorrhage [10, 19, 20].
The combined presence of AVM and moyamoya disease is extremely rare in contrast to the presence of saccular aneurysms in patients with this occlusive disease. To date, there are only 14 cases of moyamoya disease accompanied by AVM reported in the literature. 10 of the patients presented with symptoms of cerebral ischaemia, while the remaining four presented with basal ganglia bleed. In all but one case, cerebral angiography demonstrated bilateral involvement of the internal carotid arteries with moyamoya disease. One patient had two independent AVMs located in the frontal lobes, which were supplied mainly by moyamoya collateral vessels through transdural communicating arteries. 13 out of the 15 AVMs were supplied by moyamoya collateral vessels [3–14]. So far, the pathogenesis and relationship between moyamoya disease and AVM are still obscure. There has been no satisfactory explanation as to why this is such a rare phenomenon. The question to be answered is whether the moyamoya disease caused or was caused by the AVM. It is also possible that two independent vascular abnormalities occur in one patient as two AVMs have been reported not to be supplied by moyamoya collateral vessels but by normal cerebral arteries. In these cases the presence of AVMs and moyamoya disease could purely be coincidental [9, 11].
Some authors believe that progressive vascular occlusion might be induced by AVMs. They observed new or progressive occlusions and stenoses of the arteries that originally supplied the AVMs. They suggested that the stress of high and increased blood flow through an AVM induces intimal hyperplasia at the terminal internal carotid artery, eventually leading to stenosis and occlusion. This process is also thought to represent a built-in protective mechanism against cerebral haemorrhage in AVMs [9, 10]. Besides the haemodynamic stress, the authors also suggested that angiogenesis is responsible for the proliferation of new capillaries observed in the moyamoya phenomenon. The angiogenesis might be induced by the release of an angiogenic factor such as transforming growth factors associated with AVMs [10]. These factors may originate from in situ sequestration of platelets and fibrin within the AVM nidus or its feeding arteries [21].
On the other hand, few authors have implicated angiogenesis process in moyamoya disease as being the cause for AVMs. Lichtor et al [2] postulated that in moyamoya disease the perforating vessels and end capillaries become distended in response to ischaemia. However, the capillary linkage is not rich enough to reach the cortex, so instead the increased blood flow is channelled into the normal draining veins. As a result these veins become dilated, taking on the appearance of an AVM. Unlike a true AVM, these vessels filled late rather than early in the injection phase [2]. Another report supporting AVM as being secondary to moyamoya was by Schmit et al, who demonstrated the development of AVM in a patient with moyamoya by repeated angiography over a 9-year period [12]. These reports suggest that such AVMs were not congenital, but developed as a consequence of angiogenic failure [3].
Our case is unusual not only due to the coexistence of moyamoya disease and AVM, but also because of the atypical unilateral involvement of the moyamoya disease. There have been few reports on unilateral involvement of moyamoya disease in the literature in both adults and children. The progression to the typical bilateral form is infrequent. However, young children have a higher tendency to develop contralateral lesions over the years [22, 23]. To the best of our knowledge there has been no report of combined presence of AVM and unilateral moyamoya disease in the English literature. Suggested causes for atypical unilateral involvement of moyamoya disease are tuberculous meningitis, irradiation or artherosclerosis [15, 17], none of which were present in our patient. In most cases, the cause remains undetermined. We cannot do more than speculate whether the presence of AVM initiated the development of unilateral moyamoya disease in our case.
The intracerebral bleed in our patient was not from the AVM, but from the collateral vessels at the lenticulostriate region. This is not surprising as pathologic study of moyamoya collateral vessels has shown various degrees of luminal stenosis, intimal thickening, discontinuity of the internal elastic lamina and microaneurysm formation, which cause the vessels to be more fragile and susceptible to bleeding [24]. Furthermore, Mawad et al suggested that the arterial stenosis proximal to the AVM serves as a built-in mechanism against cerebral haemorrhage from the AVM by reducing the flow to the nidus [9].
The treatment of moyamoya disease involves establishing as much blood flow as possible to the brain by creating direct or indirect bypass. On the other hand, AVMs are treated by stopping the flow into the nidus. Hence, the management principles in treating the combined presence of AVM and moyamoya disease are in direct conflict. Radiosurgery (gamma knife) has been successfully used to treat cerebral AVM in moyamoya disease [4]. In our case, the treatment was primarily symptomatic and supportive as the patient intended to seek treatment elsewhere.
In conclusion, we present a rare case of combined presence of moyamoya disease and cerebral AVM in a young and otherwise healthy gentleman. Our case is also unusual as the moyamoya disease was only present on the side where the AVM was found.
Received for publication May 23, 2005.
Accepted for publication June 27, 2005.
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Abstract
Introduction
