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The term moyamoya disease should be reserved for an idiopathic, sometimes familial, condition, which leads to characteristic intracranial vascular changes.
Numerous entities have been described that mimic the appearance, in which case the term moyamoya syndrome (or phenomenon or pattern) is used, which then can be further broadly divided into atherosclerotic causes and vasculitic/inflammatory causes 11.
This article concerns itself with moyamoya disease. For a list of conditions that can mimic moyamoya disease please refer to the article on moyamoya syndrome or the differential diagnosis list at the end of the article.
Moyamoya is a disease of children and young people, with a bimodal age distribution 6:
early childhood: peak ~4 years of age (two-thirds)
middle age: 30-40 years of age (one-third)
The condition was initially described in Japanese patients 14, where it is still most common, in which ~12.5% (range 10-15.4%) of cases are familial.
Presentation is to some degree age dependent. In children, hemispheric ischemic strokes are most pronounced, whereas in adults hemorrhage from the abnormal vessels is more common 6. Watershed infarcts are also very commonly identified.
The underlying pathological and genetic basis for moyamoya disease is not well understood 10. Fibrocellular proliferation and thickening of the intima is the main process responsible for vascular stenosis and occlusion. The associated neo-vascularization may be a compensatory mechanism or part of the disease process itself, with the moyamoya vessels demonstrating various histopathological abnormalities including fibrin deposition, microaneurysm formation, among other abnormalities 10.
RNF213 has been identified as a susceptibility gene 15.
Moyamoya disease affects the bilateral distal ICA and circle of Willis. Up to 18% of patients with moyamoya may present with unilateral angiography-documented disease 8.
Small abnormal net-like vessels proliferate giving the characteristic "puff of smoke" appearance on direct angiography. CTA and MRA are not always able to demonstrate this appearance on account of lower flow and spatial resolution.
Although classically described affecting the ICA, over 50% of patients also have involvement of the posterior cerebral arteries.
Generalized cerebral atrophy is a common finding. Watershed infarcts are also commonly seen.
Cerebral hemorrhage is more likely to occur in adult patients, patients with collateral circulation where perfusion has normalized such as long-term post bypass surgery or patients with extensive choroidal collaterals, advanced Suzuki stage, fetal-type PCA, patients with previous hemorrhage or microbleeds, and patients with ACA occlusion 13.
Collateral circulation forms from a number of sources:
via the abnormal moyamoya vessels: lenticulostriate, thalamoperforating, leptomeningeal, and dural arteries appear as multiple tortuous flow voids on T1 and T2 weighted sequences
pial collaterals from less affected vessels (especially PCA): forming the so-called ivy sign (high serpentine sulcal FLAIR signal intensity due to slow flow and also a high signal on T1 postcontrast-enhanced MRI) 3
multiple foci of microbleeds and also prominent deep medullary veins "brush sign" on susceptibility sequences 7
transdural branches of the middle meningeal and other dural branches
In addition to demonstrating the aforementioned arterial stenoses (best seen on MRA) or enlarged perforators (best seen on T2 weighted images), vessel wall imaging can also be helpful, particularly in distinguishing moyamoya disease from moyamoya syndrome from atherosclerotic or vasculitic/inflammatory causes 11.
Vessel wall imaging in moyamoya disease typically demonstrates 11:
concentric luminal narrowing
none or only minimal enhancement
homogeneous T2 signal
no outward remodeling (outer wall area of the stenotic segment greater than proximal normal segment; seen in atherosclerosis)
See article: Suzuki staging system for moyamoya disease.
Treatment and prognosis
Bypassing the occlusive segments is the aim of most surgical therapy and this can be accomplished by direct (i.e. direct artery-to-artery anastomosis) or indirect revascularization.
In adults, external carotid artery to middle cerebral artery (ECA-MCA) anastomoses can be performed as the vessels are larger. One of the surgical options is the superficial temporal artery to middle cerebral artery (STA-MCA) bypass.
A variety of indirect revascularization techniques have been developed, and are generally preferred in pediatric patients as their vessels are too small to allow direct anastomosis 12:
An alternative is to create multiple burr holes to allow formations of local collaterals 9.
History and etymology
The term "moyamoya" comes from a Japanese expression for something "hazy just like a puff of cigarette smoke drifting in the air" was first used in the English literature by Jiro Suzuki and Akira Takaku, Japanese neurosurgeons, in 1969 1,14,15, however, the first reported case was by K Takeuchi and K Shimizu in 1957 with many cases and case series published in the Japanese literature in the late 1950s and through the 1960s 14,15.
A number of conditions can lead to imaging appearances that are very similar to moyamoya disease. For a full list, please refer to moyamoya syndrome:
- 1. Suzuki J & Takaku A. Cerebrovascular "Moyamoya" Disease. Disease Showing Abnormal Net-Like Vessels in Base of Brain. Arch Neurol. 1969;20(3):288-99. doi:10.1001/archneur.1969.00480090076012 - Pubmed
- 2. Mugikura S, Takahashi S, Higano S et al. The Relationship Between Cerebral Infarction and Angiographic Characteristics in Childhood Moyamoya Disease. AJNR Am J Neuroradiol. 1999;20(2):336-43. PMC7056099 - Pubmed
- 3. Yoon H, Shin H, Chang Y. "Ivy Sign" in Childhood Moyamoya Disease: Depiction on FLAIR and Contrast-Enhanced T1-Weighted MR Images. Radiology. 2002;223(2):384-9. doi:10.1148/radiol.2232011094 - Pubmed
- 4. Bruno A, Adams H, Biller J, Rezai K, Cornell S, Aschenbrener C. Cerebral Infarction Due to Moyamoya Disease in Young Adults. Stroke. 1988;19(7):826-33. doi:10.1161/01.str.19.7.826 - Pubmed
- 5. Hsu S, Chaloupka J, Fattal D. Rapidly Progressive Fatal Bihemispheric Infarction Secondary to Moyamoya Syndrome in Association with Graves Thyrotoxicosis. AJNR Am J Neuroradiol. 2006;27(3):643-7. PMC7976957 - Pubmed
- 6. Valery N. Kornienko, I.N. Pronin. Diagnostic Neuroradiology. (2008) ISBN: 9783540756521 - Google Books
- 7. Horie N, Morikawa M, Nozaki A, Hayashi K, Suyama K, Nagata I. "Brush Sign" on Susceptibility-Weighted MR Imaging Indicates the Severity of Moyamoya Disease. AJNR Am J Neuroradiol. 2011;32(9):1697-702. doi:10.3174/ajnr.A2568 - Pubmed
- 8. Smith E & Scott R. Progression of Disease in Unilateral Moyamoya Syndrome. Neurosurg Focus. 2008;24(2):E17. doi:10.3171/FOC/2008/24/2/E17 - Pubmed
- 9. Kapu R, Symss N, Cugati G, Pande A, Vasudevan C, Ramamurthi R. Multiple Burr Hole Surgery as a Treatment Modality for Pediatric Moyamoya Disease. J Pediatr Neurosci. 2010;5(2):115-20. doi:10.4103/1817-1745.76102 - Pubmed
- 10. Bang O, Fujimura M, Kim S. The Pathophysiology of Moyamoya Disease: An Update. J Stroke. 2016;18(1):12-20. doi:10.5853/jos.2015.01760 - Pubmed
- 11. Mossa-Basha M, de Havenon A, Becker K et al. Added Value of Vessel Wall Magnetic Resonance Imaging in the Differentiation of Moyamoya Vasculopathies in a Non-Asian Cohort. Stroke. 2016;47(7):1782-8. doi:10.1161/STROKEAHA.116.013320 - Pubmed
- 12. Digiusto M, Bhalla T, Grondin R, Tobias J. Perioperative Care of the Pediatric Patient for Pial Synangiosis Surgery. Int J Clin Exp Med. 2013;6(3):231-8. PMC3609701 - Pubmed
- 13. Hirano Y, Miyawaki S, Imai H et al. Differences in Clinical Features Among Different Onset Patterns in Moyamoya Disease. J Clin Med. 2021;10(13):2815. doi:10.3390/jcm10132815 - Pubmed
- 14. Oshima H & Katayama Y. Discovery of Cerebrovascular Moyamoya Disease: Research During the Late 1950s and Early 1960s. Childs Nerv Syst. 2012;28(4):497-500. doi:10.1007/s00381-012-1708-x - Pubmed
- 15. Kuribara T, Akiyama Y, Mikami T et al. Macrohistory of Moyamoya Disease Analyzed Using Artificial Intelligence. Cerebrovasc Dis. 2022;51(4):413-26. doi:10.1159/000520099 - Pubmed