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 Table of Contents  
Year : 2019  |  Volume : 7  |  Issue : 2  |  Page : 224-232

Moyamoya disease

Department of Neurosurgery, Kasturba Medical College, Manipal University, Manipal, Karnataka, India

Date of Submission18-Nov-2019
Date of Decision02-Dec-2019
Date of Acceptance06-Dec-2019
Date of Web Publication16-Dec-2019

Correspondence Address:
Girish Menon
Department of Neurosurgery, Kasturba Medical College, Manipal University, Manipal - 576 104, Karnataka
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/amhs.amhs_156_19

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Moyamoya disease (MMD) is a unique cerebrovascular disease characterized initially by an obliterative vasculopathy followed by a compensatory proliferative vasculopathy. Coined by Suzuki and Takaku in 1969, the term moyamoya (MM) refers to a “puff of smoke” like appearance of small collaterals seen traversing the basal ganglia and thalamus, in response to progressive stenosis and occlusion of supraclinoid internal carotid artery. The natural history is unclear but is generally one of the gradual progressions. The etiopathogenesis of MMD is unknown, but the syndromic form may be associated with certain genetic conditions, such as Down's syndrome and neurofibromatosis, and may occur following cranial radiation. The clinical manifestations are predominantly ischemic and usually confined to the anterior circulation. Hemorrhagic presentation is less common and occurs more often in adults. Similarly, posterior circulation may get involved in later stages. Treatment is essentially surgical, and a combined revascularization strategy involving a direct superficial temporal artery to middle cerebral artery anastomosis along with a pial synangiosis provides a reasonable stroke-free survival. Considerable controversy exists on the etiopathogensis, diagnostic guidelines, management protocols, ideal surgical approach, and the role of surgery in hemorrhagic MMD. This review attempts to summarize the current advances of MMD on the aspects of epidemiology, etiology, clinical features, imaging diagnosis, and treatment.

Keywords: Cerebral anastomosis, moyamoya, revascularization, stroke, synangiosis

How to cite this article:
Menon G, Hegde A. Moyamoya disease. Arch Med Health Sci 2019;7:224-32

How to cite this URL:
Menon G, Hegde A. Moyamoya disease. Arch Med Health Sci [serial online] 2019 [cited 2023 Mar 31];7:224-32. Available from: https://www.amhsjournal.org/text.asp?2019/7/2/224/273061

  Introduction Top

Moyamoya disease (MMD) is an uncommon, progressive cerebrovascular occlusive disorder of unknown etiology, which results in considerable morbidity if left untreated. More commonly seen in children where it accounts for ≥6% of strokes, it is a well-recognized cause of stroke in adult patients too.[1],[2] Earlier considered to be a disease of the oriental countries, it is increasingly reported from India and the Western world also. MMD is a unique form of vasculopathy characterized by both an occlusive and a proliferative pathology. Progressive stenosis of the terminal internal carotid artery (ICA) and proximal middle and anterior cerebral arteries (ACAs) is followed by compensatory proliferation of basal perforator vessels. These arteries, called the moyamoya (MM) vessels, traverse the thalamus and basal ganglia, providing collateral blood flow to regions of hypoperfused brain distal to the narrowed vessels. The compensatory mechanism often fails, resulting in recurrent strokes, either hemorrhagic or ischemic. The exact pathogenesis and natural history are still unclear but generally are one of the gradual progressions. The current evidence suggests that surgical management provides significant symptomatic benefit.

  History Top

MM was first described in Japanese literature by Takeuchi and Shimizu in 1957 as a case of “hypoplasia of the bilateral internal carotid arteries.”[2] It was first published in English literature by Kudo, who described it as a “spontaneous occlusion of the circle of Willis” in 1968.[3] The popular terminology “MM” was suggested soon after in 1969 by Suzuki and Takaku. “MM” is a Japanese expression that refers to “something hazy, like a puff of cigarette smoke drifting in the air.” Suzuki and Takaku coined the term MM to describe the characteristic angiographic appearance of the dilated collateral arteries that develop at the base of the brain.[4]

  Incidence and Prevalence Top

MMD occurs around the globe but is more common in East Asian countries such as China, Japan, and Korea.[5] Epidemiological studies have shown an increasing trend in the incidence and prevalence of MM disease globally. In Japan, the prevalence of MMD rose from 3.16 per 100,000 in 1994 to 10.5 per 100,000 people in 2006. The annual incidence increased from 0.35 per 100,000 in 1994 to 0.94 per 100,000 in 2006.[6] The incidence of MMD in the United States and Europe is about one-tenth of that in Japan.[2] MMD tends to run in families, and the incidence of familial MMD is nearly 15%. Familial MMD in Eastern Asia is almost 10 times higher than that in Western countries.[6] The exact incidence and prevalence of MMD in India are not known. However, MMD is increasingly reported as a cause for stroke in the last few decades from many centers across India.[5],[6],[7],[8]

MMD affects females twice as often as males.[2] MMD also has a bimodal age distribution, with patients typically presenting either in the first (5–10 years) or fourth decade of life (25–49 years).[7] Younger patients within the first decade present with ischemic events, whereas adult patients more commonly present with hemorrhage.[2]

  Etiopathogenesis Top

MMD starts with stenotic changes in the distal intracranial ICA at the bifurcation. It then progresses to involve the proximal ACAs and middle cerebral arteries (MCAs). Posterior circulation vessels may get involved in later stages. As a compensatory mechanism to the ischemia resulting from stenosis, a proliferative network of perforators develops within the brain. This compensatory recruitment of new vessels provides collateral blood flow to areas of the hypoperfused brain by forming a network of anastomosis at different sites. Broadly, these networks include the following: (i) anastomotic network formed near the lateral ventricle by the basal perforators and cortical vessels which traverse the brain (ii) basal collateral network formed by the union of carotid and basilar perforators (iii) anastomotic network formed on the surface of the brain by the end to end anastomosis of cortical leptomeningeal vessels and dural vessels.[9] In later stages, the anterior and middle cerebral circulations are reinforced by the dural and extracranial arterial networks (vault MM vessels).[2]

Histological examination of stenotic segments reveals endothelial hyperplasia, intimal thickening, duplication of the internal elastic lamina, and attenuation of tunica media.[9],[10] Histologically, MM vessels exhibit thin walls with fibrin deposits, fragmentation of the elastic lamina, and microaneurysm formation.[2],[11],[12] Saccular aneurysms and pseudoaneurysms may also develop along peripheral portions of perforating MM vessels, anterior and posterior choroidal arteries, and basilar top.[11]

The exact etiopathogenesis of MMD remains unknown. Possible mechanisms include genetic, acquired/environmental factors, angiogenesis, and immune/inflammatory factors. The high incidence of MMD among East Asians, familial occurrence, and its association with other genetically transmitted diseases such as neurofibromatosis suggest a probable genetic link.[3],[13] Besides hereditary factors, acquired or environmental factors such as irradiation and infection may play a role in the pathogenesis of MMD. In familial MMD from East Asian countries, the role of RNF213 p.R4810K is critical.[14] These genes are also linked to the ischemic type of MMD, while the non-RNF213 p.R4810K variants were more likely to be associated with the hemorrhagic type of MMD. Angiogenesis-related factors, such as endothelial colony-forming cells, and various cytokines, such as vascular endothelial growth factor, hepatocyte growth factor, basic fibroblast growth factor, and transforming growth factor-beta 1, are also thought to influence the development of MMD.[2],[10],[14] In the last decade, the role of inflammatory/immunological mediators in the pathogenesis of MMD-related vascular stenosis is gaining interest based on the observation of T-cell and macrophage infiltration in the intima of affected vessels on immunohistochemical staining. Further research is required to provide accurate insights into the etiopathogenesis of MMD.

Moyamoya disease and moyamoya syndrome

MMD can be idiopathic or seen in association with other disorders. The idiopathic form is known as MMD, and MM syndrome refers to cases that occur in association or secondary to other conditions, such as neurofibromatosis, sickle cell anemia, Down's syndrome, and prior cranial irradiation.[9],[10],[11] The symptomatology, angiographic findings, and clinical course of both the variants are nearly similar and so are the management strategy.

  Natural History and Progression Top

The natural history of MMD is that of progression, with variable rates. While some patients exhibit a fairly rapid progressive course, others have a more gradual progression over many years.[15],[16] It is believed that ischemic symptoms keep recurring in the first decade until the development of sufficient leptomeningeal or transdural collaterals, and subsequently, there may be a period of stability depending on the extent of collateral formation.[9]

Unilateral and bilateral moyamoya disease

Although most patients present with bilateral involvement, up to 18% of patients have unilateral involvement confirmed by angiography.[17] The question of whether all unilateral MMD progress to bilateral MMD and whether unilateral is early bilateral MMD remains controversial. In children, unilateral disease usually progresses to involve both sides within 1–2 years.[18],[19] Children with MM syndrome associated with cranial irradiation, Down's syndrome, neurofibromatosis, sickle cell anemia, collagen vascular disorders, Graves' disease, infections, such as tuberculous meningitis, and leptospirosis are at higher risk of progression to bilateral involvement.[15],[19]

  Clinical Presentation Top

Symptomatology in MMD is related to the compromised blood flow to the cerebral hemisphere and its consequences. The most common symptom thus is an ischemic stroke, and the signs vary according to the vascular territory affected. Anterior circulation is more often affected than posterior circulation. The MM vessels which develop in response to stenosis of ICA are small in caliber and under hemodynamic stress. They are vulnerable and prone to bleed. Microaneurysms tend to develop in these vessels, and these aneurysms can rupture under stress. The incidence of aneurysms in MMD varies from 1% in children to 6.2% in adults.[2] Thus, the second common presentation in MMD is a cerebral bleed. Dilation of meningeal and leptomeningeal collateral vessels can result in headache. Chronic infarcts with resultant gliosis can also result in seizures, focal deficits, and involuntary movements [Figure 1]. Chronic global hypoperfusion can result in a progressive decline in neurocognitive function. Involvement of the posterior circulation territory may result in visual field defects, diplopia, scintillating scotomas, ataxia, and vertigo.
Figure 1: A 12-year-old female child with recurrent left hemispheric ischemic events. Magnetic resonance imaging axial T1 (a and b) and T2 (c and d) images showing extensive left hemispheric infarcts with gliosis

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Children typically present with ischemia, and bleeding is more common in adults [Figure 2].[20],[21] One characteristic feature in children is that ischemic events get precipitated by strenuous events, such as coughing, crying, hyperventilating, or blowing. Hypocapnia-induced vasoconstriction, accompanied by a transient reduction in cerebral blood flow (CBF) in an already compromised cerebral circulation, is responsible for these events.[13] Cerebral hemorrhage is more common in adults. Hemorrhage is the presentation in 40%–65% of adult patients, and the common locations are the basal ganglia (40%), thalamus (15%), or ventricular system (30%).[22],[23]
Figure 2: Computed tomography scan plain images of a 40-year-old male presenting with sudden-onset headache and altered sensorium. Scan images showing primary intraventricular hemorrhage

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  Diagnosis Top

A strong suspicion of MMD should be maintained for all childhood strokes, especially those precipitated by hyperventilation or crying. MMD should be a differential for all nonhypertensive Spontaneous intracerebral hematoma (SICH), especially primary intraventricular hemorrhage. Plain computed tomography (CT) scan is often done as an initial screening tool and may detect the presence of an infarct or hemorrhage. Magnetic resonance imaging (MRI) may reveal the absence of flow voids in the distal ICA, suggesting stenosis. Similarly, prominent flow voids in the basal ganglia and thalamus on MRI suggest the presence of MM vessels.[24]

Although the gold standard for the diagnosis of MMD remains a cerebral angiogram, magnetic resonance angiography (MRA) is increasingly used as an alternative. Studies have shown that MRA has a sensitivity of 73% and a specificity of 100% in diagnosing MMD.[25] Sensitivity increases to 92% when MRA is combined with MRI or MRA with selective maximum intensity projection.[25],[26] The drawback, however, remains the visualization of smaller MM collaterals as well as the vault MM vessels and collaterals from the external carotid supply. These are better seen on Digital subtraction angiography (DSA), which remains the gold standard for the diagnosis of MMD [Figure 3], [Figure 4], [Figure 5], [Figure 6].[25]
Figure 3: DSA left vertebral anteroposterior (a) injection showing occlusion of terminal vertebral basilar complex and presence of moyamoya vessels left external carotid artery injection (b) showing external carotid artery collaterals

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Figure 4: DSA left common carotid artery injections oblique (a) and lateral (b) images showing occlusion of the supraclinoid internal carotid artery and presence of moyamoya vessels

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Figure 5: DSA Left ICA AP (A) and Lateral (B), right ICA AP (a) and lateral (b) injection showing stenosis and occlusion of the terminal supraclinoid internal carotid artery. The posterior circulation is being supplied by a dominant posterior communicating artery seen prominently on left ICA AP (c) and lateral (d) projections (fetal circulation on both sides)

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Figure 6: DSA external carotid artery injection in the same patient showing extensive external carotid artery collaterals

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The Revised Japanese Guidelines of 2012 cerebral angiography defines the current staging and classification of MMD based on angiographic findings. Earlier MMD was classically described to progress through the following six characteristic angiographic stages named after Suzuki [Table 1][14],[45] and later modified by Mugikura et al.[27] [Table 2]. The novel guidelines added a staging based on scores of MRA and the diagnostic criteria of which are shown in [Table 3].[22],[14],[45]
Table 1: Stages and cerebral angiographic findings

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Table 2: Angiographic internal carotid artery staging system modified by Mugikura et al.

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Table 3: Classification and scoring based on the magnetic resonance angiography findings

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The abnormal vascular anastomosis at the base of the brain is distinct with a characteristic pattern in each type of MMD. The Japanese Adult MMD (JAM) trial studies show that hemorrhagic MMD patients have a higher percentage of choroidal and thalamic anastomosis in comparison to patients with ischemic MMD. Suzuki's angiographic staging was also significantly higher in hemorrhagic MMD.

Electroencephalography can be helpful as it shows a characteristic diffuse pattern of monophasic slow waves “buildup,” followed by a characteristic “re-buildup” phenomenon induced by hyperventilation.[28] This finding, characteristic of MMD, is thought to be a consequence of decreased arterial CO2 tension, which causes vasoconstriction of previously maximally dilated normal cerebral vessels and leads to cerebral ischemia.

CBF estimation also forms part of the investigation for MMD. Positron emission tomography, xenon-enhanced CT, and single-photon emission CT (SPECT) done before treatment identify regional perfusion instability and confirm the improvement of functional perfusion following surgery.[1],[19] Chronic ischemia and hypoperfusion result in reduced CBF and higher cerebral blood volume. Assessment of cerebrovascular reserve and abnormal vasoreactivity to vasodilatory stimuli through these tests and the acetazolamide challenge test helps to predict the likelihood of further disease progression and the success of a surgical procedure.[29]

  Treatment Top

The natural history of MMD is unpredictable but generally is one of the slow progressions. Although some patients stabilize without intervention, the majority of the patients are left with permanent neurological deficits.[2],[11] Thus, timely diagnosis with prompt, appropriate surgical management is a priority. In the absence of definitive medical treatment to halt the progression or stabilize the course of MMD, surgery remains the mainstay in treatment.[30],[31]

Medical management

There is no known effective medical treatment in MMD. Aspirin helps to prevent ischemic symptoms secondary to emboli from the microthrombus formation at sites of arterial stenosis.[2],[32] Calcium channel blockers help in patients with refractory transient ischemic attacks and in relieving intractable headaches. Potential newer agents under trial include angiogenic growth factors, which induce neovascularization, novel therapies that alter or block arterial wall disease, and gene therapy.

Surgical management

The primary aim in the surgical management of MMD is to reinforce CBF using the branches of the external carotid artery. Three different revascularization procedures have been described – indirect, direct, and combined revascularization. A brief summary of treatment outcomes following various modes of surgery versus conservative management in ischemic, hemorrhagic, and asymptomatic MMD is well described in [Table 4], [Table 5], [Table 6].
Table 4: Treatment outcomes for asymptomatic moyamoya disease based on a literature review

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Table 5: Treatment outcomes for hemorrhagic moyamoya disease based on a literature review

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Table 6: Treatment outcomes for ischemic moyamoya disease based on a literature review

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Direct revascularization

The most commonly performed direct revascularization procedure for MMD is the superficial temporal artery-middle cerebral artery (STA-MCA) anastomosis, which was done for the first time in 1970.[33] Other procedures include those targeting the ACA and posterior cerebral artery (PCA) territory such as STA-ACA, STA-PCA, and occipital artery-PCA anastomosis.[33] A recent meta-analysis of various clinical studies revealed that STA-MCA bypass surgery in adults significantly decreases the risk of future strokes in comparison to conservative management with an odds ratio of 0.301 (P< 0.001) [Figure 7].[34] STA-MCA is equally effective for hemorrhagic MMD also, and the recently concluded JAM study revealed that the annual risk of secondary re-hemorrhage in adults was significantly reduced from 8% in the nonsurgical group to 3% in the STA-MCA bypass group.[35] The major limitation for the direct bypass is the demanding surgical technique, especially in children where the donor STA vessels are very small. The bypass patency rates varies from 53% in children to 94% in adults.[36]
Figure 7:Postoperative angiogram following a direct revascularization showing a patent superficial temporal artery to middle cerebral artery anastomosis

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Indirect revascularization

Indirect revascularization relies on neovascularization and ingrowth of new blood vessels on the cortical surface through angiogenic mechanisms from pedicle-based grafts (i.e., pial synangiosis). Indirect techniques are easier to perform but may take months to develop and are less predictable in hemodynamic outcomes. Indirect procedures yield better outcome in children since a high level of plasticity, and angiogenic potential of the brain tissue and vasculature are required for their success. The higher levels of circulating vascular proliferative factors seen in MMD patients probably help in this angiogenesis. The most prominent type of indirect revascularization is encephalo-myo-synangiosis (EMS). Other variations include encephalo-arterio-synangiosis, encephalo- myo-arterio-synangiosis, encephalo-duro-synangiosis, encephalo-duro-arterio-synangiosis, encephalo-duroarterio- myo-synangiosis (EDAMS), encephalo-duro-galeo (periosteal) -synangiosis, as well as various combinations of these. Other techniques include multiple burr holes or omental transplantation which stimulates transcranial angiogenesis.

Combined revascularization techniques

Of late, combined procedures that include a direct STA-MCA bypass with an indirect procedure such as EDAMS or EMS are gaining popularity. Such procedures are beneficial, especially in children where the bypass has a higher failure rate, and the indirect techniques have a superior take rate. More evidence on the superiority of combined procedures over a single technique is required before it can be recommended as the standard of care.

Comparison of the different revascularization techniques

Most studies suggest that direct and combined procedures provide a longer stroke-free outcome when compared to indirect procedures alone. However, it is also well accepted that patent grafts, angiographically proven neovascularization, and improved cerebrovascular hemodynamics do not necessarily translate into better clinical outcomes. A randomized trial comparing the hemodynamic result of indirect (EMS) versus combined (STA/MCA bypass + EMS) revascularization concluded that combined revascularization improved cerebrovascular reserve capacity, significantly compared to indirect techniques.[37] Similarly, the meta-analysis by Jeon et al. and Qian et al. suggest that direct bypass (direct and combined procedures) is superior in stroke prevention when compared with indirect bypass procedures, both for the adult and pediatric patient populations.[34],[35],[36],[37],[38] Rates of perioperative complication rates are also comparable but may be marginally higher with direct/combined techniques: A meta-analysis that focused on perioperative complications in adults suggests that the beneficial effects of direct revascularization techniques outweigh their marginally higher complication rate.[39],[40] Thus, direct anastomoses should be regarded as the mainstay of any revascularization attempt for both adults and patients with pediatric MMD.

Timing of surgery

Surgery needs to be recommended for all symptomatic MMD patients with proven angiographic evidence.[34] Early diagnosis and prompt surgical revascularization help in achieving an excellent long-term outcome with improved intellectual function.[35] The outcome is better if surgery is done before infarction occurs. In asymptomatic patient's CBF studies, SPECT with acetazolamide challenge should be performed. Reduced cerebral perfusion is an excellent indicator of surgical treatment in such patients. In patients with prior stroke and existing fixed neurological deficits, the decision to operate should be customized depending on the risk of stroke in new cortical territories and the patient's quality of life.[41],[42],[43],[44],[45]

Japan adult moyamoya trial and guideline recommendation

The latest guideline for MMD in Japan recommends direct revascularization surgery for patients presenting with ischemic symptoms (Recommendation Grade B).[46] However, in patients with hemorrhagic MMD, there has been a controversy about whether surgical revascularization has a potential role in reducing the risk of re-bleeding. The JAM trial was a randomized controlled trial, which examined this efficacy of direct extracranial–intracranial (EC-IC) bypass.[37] The results showed that the annual risk of re-bleeding was 2.7% in the surgical group versus 7.6% (P = 0.042) in the nonsurgical group. In a subgroup analysis of the JAM trial, patients with posterior hemorrhage demonstrated a higher re-bleeding rate (17.1% per year) compared to those with anterior hemorrhage and EC-IC bypass significantly reduced the risk of re-bleeding in patients with posterior hemorrhage (P = 0.001).[47] Incorporating these findings, the latest guideline, recommends direct revascularization surgery for hemorrhagic MMD with posterior hemorrhage (Grade B).

Targeted revascularization of anterior cerebral artery and posterior cerebral artery territories

Most of the direct and indirect revascularization procedures target the MCA territory. However, ischemic symptoms affect the ACA and PCA territory too. Selective surgery targeting ACA and PCA territory is again a matter of debate as there is a belief that revascularization of the MCA territory also takes care of the impaired ACA/PCA territories via leptomeningeal anastomoses.[40] Decision regarding surgical revascularization of the ACA and PCA territory needs to be customized based on the patient's symptoms and surgeons' expertise. Direct procedures include STA-ACA (for the ACA territory) and the occipital artery-PCA anastomosis (for the PCA territory).[44] Indirect revascularization methods such as burr-hole procedures, omentum transposition/transplantation, and enlarged encephalo-duro-myo-synangiosis have also been tried for both ACA and PCA territory. These procedures, however, are not performed routinely.[48],[49],[50]

Rescue revascularization

Rescue procedures may sometimes be needed after failed revascularization surgery with persistent or recurrent symptoms. Surgical options are few and limited. Options for direct revascularization include a radial artery bypass or a saphenous vein graft bypass surgery.[41]

Role of antiplatelet therapy after surgery

The role of perioperative aspirin is controversial although most cerebrovascular surgeons prefer to use it after bypass surgery. A recent meta-analysis on the use of aspirin after bypass surgery suggests that although aspirin did not affect perioperative stroke rate and bypass patency, it results in better clinical outcomes.[42]

  Outcome Prognosticators Top

Overall prognosis of MMD is determined by several factors. These are (1) the speed and extent of vascular occlusion; (2) the potential for development of collateral circulation; (3) the age at onset; (4) the severity of neurological deficits at presentation and degree of disability; and (5) the extent of infarcts seen on imaging studies at the time of first presentation.[2] The extent of disease at the time of diagnosis is more important than the age at onset of symptoms.[18] Surgical revascularization performed before infarction has excellent prognosis even in the presence of severe angiographic changes.[19],[30],[43],[51],[52],[53] However, when untreated, there is progression of both clinical symptoms and angiographic findings, leading to clinical deterioration and possible irreversible neurological deficits.[26]

  Conclusion Top

MMD is an uncommon cause of stroke in adults and children, which, if not treated, will inevitably progress with devastating consequences. The exact etiopathogenesis is not clearly known. Strong suspicion of MMD needs to be kept for all children presenting with stroke and in adults presenting with spontaneous intracerebral hemorrhage. Early diagnosis and appropriate surgical management prevent long-term morbidity. Future investigations are required to understand the exact etiopathogenesis and natural history of this unique disease.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

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Conflicts of interest

There are no conflicts of interest.

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7]

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]

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