Moyamoya disease concurrent with dural arteriovenous fistula: A case report and literature review
Affiliations: Department of Neurosurgery, The First Hospital of Jilin University, Changchun, Jilin 130021, P.R. China
- Published online on: October 9, 2020 https://doi.org/10.3892/etm.2020.9290
- Article Number: 161
Copyright: © Hou et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
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Moyamoya disease (MMD) is an idiopathic chronic disease characterized by progressive steno-occlusive alteration of the internal carotid artery terminal and the beginning of the anterior cerebral artery and middle cerebral artery (1). Dural arteriovenous fistula (DAVF) is an uncommon vascular malformation that is characterized by abnormal connections between meningeal arteries and dural venous sinuses, meningeal veins or cortical veins (2).
MMD is currently considered a genetic disease (1). For DAVF, progressive stenosis or thrombosis of the dural venous sinus are thought to have a pivotal role in the genesis of DAVF (2). In general, there is no relationship between MMD and DAVF; however, in extremely rare circumstances, patients with MMD have been reported to have concurrent DAVF (3,4). In the present study, another case of MMD concurrent with DAVF was reported. In addition, a literature review of the reported cases was also performed to further expound this rare scenario.
A 47-year-old male was admitted was admitted to The First Hospital of Jilin University (Changchun, China) on Sep 27th 2015 due to sudden onset of headache. The patient was generally healthy and denied a history of hypertension, diabetes or any other chronic diseases. Physical examination was unremarkable except for mild neck stiffness. Head CT indicated hemorrhage of the right thalamus with ventricular extension (Fig. 1A and B). CT angiography (CTA) revealed that the normal vasculature in the anterior and posterior circulation disappeared and was replaced by moyamoya-like vessels (Fig. 1C and D). A diagnosis of hemorrhagic MMD was made. The patient received conservative management, including analgesic (flurbiprofen, 50 mg/bid), antemetic (tropisetron hydrochloride, 5 mg/bid) and fluid infusion (normal saline and 5% glucose solution) and was discharged 3 days later.
Head CT indicates (A) right thalamus hemorrhage with (B) ventricular extension. (C) Volume rendering and (D) maximum intensity projection of CT angiography reveals steno-occlusive alteration of the internal carotid artery terminus and posterior cerebral artery origin, and the normal vasculature in the anterior and posterior circulation is replaced by moyamoya-like vessels.
After three months, the patient was readmitted due to dizziness and gait disturbance. Diffusion-weighted MRI indicated acute infarction in the left cerebellar hemisphere (Fig. 2A) and encephalomalacia in the right thalamus (Fig. 2B). The cerebral blood volume (Fig. 2C and D) and cerebral blood flow (Fig. 2E and F) maps on perfusion-weighted MRI suggested relatively normal blood perfusion in the bilateral hemispheres.
MRI with (A) diffusion-weighted imaging and (B) T2-weighted imaging indicates acute infarction of the left cerebellar hemisphere and old malacia in the right thalamus. The (C and D) cerebral blood volume and (E and F) cerebral blood flow maps on perfusion-weighted MRI indicated relatively normal blood perfusion in the bilateral hemispheres.
Conventional angiography of the internal carotid arteries and vertebral arteries (Fig. 3) confirmed the findings from previous CTA. An angiogram of the external carotid arteries indicated that the middle meningeal artery (MMA) and occipital artery (OA) had formed efficient collaterals with the brain vasculature (Fig. 4). A DAVF was also noted. The DAVF (Cognard classification Ⅰ) was fed by the left MMA, OA and posterior meningeal artery (PMA). It drained into the transverse-sigmoid sinus and occipital sinus (Fig. 5).
Angiogram of the bilateral ICAs (A and B) in AP view indicates steno-occlusive alteration of the ICA terminus. Angiogram of the right VA in (C) anteroposterior and (D) lateral views indicates steno-occlusive alteration of the proximal posterior cerebral artery. Extensive moyamoya-like vessels developed across the anterior and posterior circulation. ICA, internal carotid artery; VA, vertebral artery; L, left; R, right.
Angiogram of the left ECA in (A) AP and (B) lateral views indicate that the MMA has anastomosed with the pial artery at the midline. A dural arteriovenous fistula (white circle) is noted in the left occipital region. Angiogram of the right ECA in (C) AP and (D) lateral views indicates that the MMA and OA have anastomosed with the pial arteries (white circle). AP, anteroposterior; ECA, external carotid artery; MMA, middle meningeal artery; OA, occipital artery; L, left; R, right.
Angiogram of the left ECA in (A) arterial and (B) capillary phases indicates that the DAVF is supplied by the left MMA, PMA (arrowhead) and OA. It drained (white arrows) to the TS, SS and occipital sinus. Angiogram in (C) anteroposterior and (D) lateral views of the right ECA indicates that the DAVF (double asterisk and circle) is also supplied by the right ECA and drains to the left TSS. DAVF, dural arteriovenous fistula; ECA, external carotid artery; MMA, middle meningeal artery; PMA, posterior meningeal artery; SS, sigmoid sinus; TS, transverse sinus; TSS, transverse-sigmoid sinus; L, left; R, right.
As no retrograde blood flow or cortical venous drainage was noted, conservative management and follow-up were proposed for the DAVF. Oral aspirin (100 mg, QD) was prescribed. The patient was discharged 1 month later with no neurological deficit. He was stable and lived independently during a 4-year follow-up. However, the patient refused re-examination of the digital subtraction (DSA) and MR perfusion due to economic factors during the follow-up period. It was not possible to produce any further radiological evidence for the evaluation of the development of MMD and DAVF.
MMD is an idiopathic steno-occlusive disease that mainly affects the anterior circulation. In a small proportion of patients, the posterior circulation may also be involved (1). As a consequence of an insufficient blood supply across the involved brain tissue, collateral vessels may arise from the cranial base perforators, which leads to the characteristic moyamoya-like vasculature in the cranial base (5).
According to previous studies, MMD may coexist with intracranial aneurysms, brain arteriovenous malformation (BAVM) and primitive carotid-basilar anastomosis (6). In extremely rare circumstances, transdural collaterals may anastomose directly with intracranial venous structures, leading to the formation of DAVFs (3,4). In a literature review of studies published in the English language, only 6 cases of AVF concurrent with MMD or moyamoya syndrome (MMS) were identified (Table I) (3,4,7-10). Among the 7 reported cases (including the case of the present study), 6 were DAVFs and 1 was a pial AVF. A total of 5 patients had concurrent MMD and 2 patients had concurrent MMS.
As a result of its rarity and the lack of research, the mechanisms underlying DAVF formation during MMD progression have remained elusive. It requires to be further investigated whether an association exists between DAVF and MMD. The specific location of a DAVF concurrent with MMD also remains to be studied. In clinical practice, progressive stenosis or occlusion of the dural venous sinus have a pivotal role in the formation of DAVF (2). Trauma, craniotomy, infection and venous sinus thrombosis are also responsible for a small proportion of DAVFs (11).
However, none of the previous case studies have reported thrombosis or stenosis of the venous system. A total of 3 patients developed AVF (1 case of pial AVF and 2 of DAVF) after extracranial-to-intracranial vascular bypass (3,4,8). No other risk factors were identified. However, concurrent AVF is an acquired disease rather than a congenital anomaly. This deduction is based on the following evidence. First, 4 of the reported AVFs were identified in a delayed fashion during the imaging follow-up of MMD or MMS (4,8,10). Furthermore, delayed development of BAVM has also been reported in patients with MMD or MMS (12,13). As the BAVM shares a similar vasculature with AVF, it may share a similar pathogenic mechanism with AVF in patients with MMD or MMS.
According to the limited evidence, the ischemic environment and consequent angiogenesis have been suggested to have pivotal roles in the formation of AVFs. The levels of proangiogenic factors such as basic fibroblast growth factor and vascular endothelial growth factor are both elevated in the dura of patients with MMD or DAVF (3). For these patients, progressive arterial occlusion both in the anterior and posterior circulation may create a robust ischemic environment for collateral formation from the external carotid and vertebral arteries. A DAVF may form during this angiogenic process (14).
The management of MMD-associated AVF depends on its clinical presentation and invasiveness. Among the cases retrieved in the present literature review, 3 patients underwent successful transvenous and/or transarterial embolization of the AVFs; 2 of these patients were treated for persistent tinnitus or eye symptoms and 1 patient was treated for the presence of cortical venous drainage (3,4,9). A total of 4 patients were managed conservatively (7,8,10).
For the patient of the present study, a close follow-up strategy was also adopted. This conservative strategy was selected for the following reasons. First, the DAVF was incidentally detected and the patient was asymptomatic. The patient was first admitted to our hospital for thalamus hemorrhage and re-admitted for cerebellar infarction 3 months later. The hemorrhage and infarction have nothing to do with the DAVF. It may be proposed that both the hemorrhage and infarction resulted from the MMD, based on the following reasons: i) This patient has no history of hypertension, which is the most common cause of cerebral hemorrhage in the thalamus or basal ganglion; ii) DAVF is a superficial cerebrovascular disease and cannot lead to deep parenchymal hemorrhage such as thalamus hemorrhage in this patient; iii) patients with MMD frequently develop slim and fragile vessels across the brain surface and paraventricular area and these fragile vessels and microaneurysms in the fragile vessels are prone to bleed (15); iv) catheter angiogram did not reveal any arteriovenous malformation or aneurysm around the hemorrhagic thalamus; v) the cerebellum is supplied by the three paired cerebellar arteries (superficial cerebellar artery, anterior inferior cerebellar artery and posterior inferior cerebellar artery). However, the DAVF in this patient was supplied by the MMA, OA and PMA. Hence, the DAVF was not responsible for the cerebellar infarction.
Furthermore, no cortical venous drainage was identified on angiogram. For patients with DAVF, cortical venous drainage is considered a risk factor of future hemorrhage. Those patients without cortical venous drainage would have a relatively benign natural course (2).
In addition, the perfusion-weighted MRI indicated relatively normal blood perfusion in the bilateral hemispheres, i.e. no severe blood insufficiency was noted across the bilateral hemispheres, which may have been compensated by the collaterals during the progression of the disease.
Finally, there were multiple feeders supplying the DAVF. Embolization of the feeders may pose a risk of compromising the transdural collaterals. Furthermore, evidence that bypass surgery is superior to medical therapy is not convincing in adult patients at present (16). Hence, for asymptomatic DAVFs or those without cerebral venous drainage, close follow-up is a reasonable option. However, for those patients concurrent with high-grade DAVFs, aggressive management through the endovascular route or open surgery is recommended to avoid future catastrophic intracranial hemorrhage. However, re-examination of the DSA and MR perfusion was refused by the patient of the present study during follow-up. The radiological progression of the MMD and DAVF remained undetermined for this patient, which limits the universality of the conservative treatment for this patient.
No funding was received.
Availability of data and materials
The datasets used and/or analyzed during the present study are available from the corresponding author on reasonable request.
KH and YZ designed the study and drafted the manuscript. XC, KX and JY collected and analyzed of the clinical data. JY critically revised the manuscript. All authors read and approved the final manuscript.
Ethics approval and consent to participate
Ethics approval is not required for case reports at our institution. Informed consent for participation in the study or use of the medical data was obtained from the patient.
Patient consent for publication
Written informed consent was obtained from the patient for publication of this manuscript and any accompanying images.
The authors declare that they have no competing interests.
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