Moyamoya Disease: Treatment and Outcomes

Tackeun Kim, Chang Wan Oh, Jae Seung Bang, Jeong Eun Kim, Won-Sang Cho, Tackeun Kim, Chang Wan Oh, Jae Seung Bang, Jeong Eun Kim, Won-Sang Cho

Abstract

Although the pathogenesis of moyamoya disease (MMD) has not been fully elucidated, the effectiveness of surgical revascularization in preventing stroke has been addressed by many studies. The main mechanism of surgical revascularization is augmenting the intracranial blood flow using an external carotid system by either direct bypass or pial synangiosis. This can improve resting cerebral blood flow as well as vascular reserve capacity. For direct revascularization, the superficial temporal artery is used as the donor artery in most cases, although the occipital artery may be used in limited cases. Usually, the cortical branch of the middle cerebral artery is selected as the recipient of direct anastomosis. As for indirect revascularization, various techniques using different kinds of connective tissues have been introduced. In some cases, reinforcing the anterior cerebral artery and the posterior cerebral artery territories can be considered. The effectiveness of surgical revascularization for preventing ischemic stroke had been generally accepted by many studies. However, for preventing hemorrhagic stroke, new evidence has been added by a recent randomized controlled trial. The incidence of peri-operative complications such as stroke and hyperperfusion syndrome seems to be high due to the nature of the disease and technical demands for treatment. Preventing and adequately managing these complications are essential for ensuring the benefits of surgery.

Keywords: Cerebral revascularization; Moyamoya disease; Treatment outcome.

Conflict of interest statement

The authors have no financial conflicts of interest.

Figures

Figure 1.
Figure 1.
This line charts demonstrates the change in the number of revascularization surgeries from 2009 to 2013 in Korea. The number of indirect revascularization surgeries is constant over this period while the number of direct revascularization surgeries gradually increases.
Figure 2.
Figure 2.
Post-operative angiography of the external carotid artery. Black arrowheads indicate the superficial temporal artery (donor artery). The tip of the black arrow is the anastomosis site to the angular artery (recipient artery). The middle cerebral artery is supplied from the superficial temporal artery with a reverse direction (white arrowheads).
Figure 3.
Figure 3.
The quantitative magnetic resonance angiography shows intact bypass flow through the superficial temporal artery.
Figure 4.
Figure 4.
Intraoperative photos show the surgical procedure of encephalo-duro-arterio synangiosis (EDAS). (A) The formation of the arterial flap containing the parietal branch of the superficial temporal artery (STA) and surrounding galea tissue as a cuff shape. Under the flap, the cortex is exposed through the ovoid craniotomy and durotomy. (B) Completed suture with dural margin. The proximal and distal end of the STA is kept connected without cutting (white arrowheads=the parietal branch of the STA; black arrowheads=the dural margin being sutured with the cuff of flap water-tightly; asterisk=the temporalis muscle split vertically and reflected).
Figure 5.
Figure 5.
Post-operative single-photon emission computed tomography showing improved vascular reserve in the Diamox study comparing the pre-operative status.

References

    1. Suzuki J, Takaku A. Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol. 1969;20:288–299.
    1. Fujimura M, Sonobe S, Nishijima Y, Niizuma K, Sakata H, Kure S, et al. Genetics and Biomarkers of Moyamoya Disease: significance of RNF213 as a Susceptibility Gene. J Stroke. 2014;16:65–72.
    1. Kim T, Lee H, Bang JS, Kwon OK, Hwang G, Oh CW. Epidemiology of Moyamoya Disease in Korea: based on National Health Insurance Service Data. J Korean Neurosurg Soc. 2015;57:390–395.
    1. Fukui M. Guidelines for the diagnosis and treatment of spontaneous occlusion of the circle of Willis (‘moyamoya’ disease). Research Committee on Spontaneous Occlusion of the Circle of Willis (Moyamoya Disease) of the Ministry of Health and Welfare, Japan. Clin Neurol Neurosurg. 1997;99(Suppl 2):S238–240.
    1. Narisawa A, Fujimura M, Tominaga T. Efficacy of the revascularization surgery for adult-onset moyamoya disease with the progression of cerebrovascular lesions. Clin Neurol Neurosurg. 2009;111:123–126.
    1. Kim T, Oh CW, Kwon OK, Hwang G, Kim JE, Kang HS, et al. Stroke prevention by direct revascularization for patients with adult-onset moyamoya disease presenting with ischemia. J Neurosurg. 2015:1–6.
    1. Miyamoto S, Yoshimoto T, Hashimoto N, Okada Y, Tsuji I, Tominaga T, et al. Effects of extracranial-intracranial bypass for patients with hemorrhagic moyamoya disease: results of the Japan Adult Moyamoya Trial. Stroke. 2014;45:1415–1421.
    1. Kim SH, Kwon OK, Jung CK, Kang HS, Oh CW, Han MH, et al. Endovascular treatment of ruptured aneurysms or pseudoaneurysms on the collateral vessels in patients with moyamoya disease. Neurosurgery. 2009;65:1000–1004.
    1. Kim T, Kwon OK, Oh CW, Bang JS, Hwang G, Lee YJ. Intracranial stenting using a drug-eluting stent for moyamoya disease involving supraclinoid ICA: a case report. Neurol Med Chir (Tokyo) 2014;54:136–138.
    1. Kuroda S, Ishikawa T, Houkin K, Nanba R, Hokari M, Iwasaki Y. Incidence and clinical features of disease progression in adult moyamoya disease. Stroke. 2005;36:2148–2153.
    1. Lee SC, Jeon JS, Kim JE, Chung YS, Ahn JH, Cho WS, et al. Contralateral progression and its risk factor in surgically treated unilateral adult moyamoya disease with a review of pertinent literature. Acta Neurochir (Wien) 2014;156:103–111.
    1. Kim SJ, Heo KG, Shin HY, Bang OY, Kim GM, Chung CS, et al. Association of thyroid autoantibodies with moyamoya-type cerebrovascular disease: a prospective study. Stroke. 2010;41:173–176.
    1. Im SH, Oh CW, Kwon OK, Kim JE, Han DH. Moyamoya disease associated with Graves disease: special considerations regarding clinical significance and management. J Neurosurg. 2005;102:1013–1017.
    1. Mineharu Y, Takagi Y, Takahashi JC, Hashikata H, Liu W, Hitomi T, et al. Rapid progression of unilateral moyamoya disease in a patient with a family history and an RNF213 risk variant. Cerebrovasc Dis. 2013;36:155–157.
    1. Kuroda S, Hashimoto N, Yoshimoto T, Iwasaki Y, Research Committee on Moyamoya Disease in Japan Radiological findings, clinical course, and outcome in asymptomatic moyamoya disease: results of multicenter survey in Japan. Stroke. 2007;38:1430–1435.
    1. Gross BA, Du R. The natural history of moyamoya in a North American adult cohort. J Clin Neurosci. 2013;20:44–48.
    1. Cho WS, Chung YS, Kim JE, Jeon JP, Son YJ, Bang JS, et al. The natural clinical course of hemodynamically stable adult moyamoya disease. J Neurosurg. 2015;122:82–89.
    1. Noh HJ, Kim SJ, Kim JS, Hong SC, Kim KH, Jun P, et al. Long term outcome and predictors of ischemic stroke recurrence in adult moyamoya disease. J Neurol Sci. 2015;359:381–388.
    1. Kraemer M, Berlit P, Diesner F, Khan N. What is the expert’s option on antiplatelet therapy in moyamoya disease? Results of a worldwide Survey. Eur J Neurol. 2012;19:163–167.
    1. Yamada S, Oki K, Itoh Y, Kuroda S, Houkin K, Tominaga T, et al. Effects of Surgery and Antiplatelet Therapy in Ten-Year Follow-Up from the Registry Study of Research Committee on Moyamoya Disease in Japan. J Stroke Cerebrovasc Dis. 2016;25:340–349.
    1. Wang KC, Phi JH, Lee JY, Kim SK, Cho BK. Indirect revascularization surgery for moyamoya disease in children and its special considerations. Korean J Pediatr. 2012;55:408–413.
    1. Kim SK, Cho BK, Phi JH, Lee JY, Chae JH, Kim KJ, et al. Pediatric moyamoya disease: An analysis of 410 consecutive cases. Ann Neurol. 2010;68:92–101.
    1. Karasawa J, Kikuchi H, Furuse S, Kawamura J, Sakaki T. Treatment of moyamoya disease with STA-MCA anastomosis. J Neurosurg. 1978;49:679–688.
    1. Cho WS, Kim JE, Kim CH, Ban SP, Kang HS, Son YJ, et al. Long-term outcomes after combined revascularization surgery in adult moyamoya disease. Stroke. 2014;45:3025–3031.
    1. Fujimura M, Tominaga T. Lessons learned from moyamoya disease: outcome of direct/indirect revascularization surgery for 150 affected hemispheres. Neurol Med Chir (Tokyo) 2012;52:327–332.
    1. Bang JS, Kwon OK, Kim JE, Kang HS, Park H, Cho SY, et al. Quantitative angiographic comparison with the OSIRIS program between the direct and indirect revascularization modalities in adult moyamoya disease. Neurosurgery. 2012;70:625–632.
    1. Guzman R, Lee M, Achrol A, Bell-Stephens T, Kelly M, Do HM, et al. Clinical outcome after 450 revascularization procedures for moyamoya disease. Clinical article. J Neurosurg. 2009;111:927–935.
    1. Mesiwala AH, Sviri G, Fatemi N, Britz GW, Newell DW. Long-term outcome of superficial temporal artery-middle cerebral artery bypass for patients with moyamoya disease in the US. Neurosurg Focus. 2008;24:E15.
    1. Miyamoto S, Akiyama Y, Nagata I, Karasawa J, Nozaki K, Hashimoto N, et al. Long-term outcome after STA-MCA anastomosis for moyamoya disease. Neurosurg Focus. 1998;5:E5.
    1. Hayashi T, Shirane R, Tominaga T. Additional surgery for postoperative ischemic symptoms in patients with moyamoya disease: the effectiveness of occipital artery-posterior cerebral artery bypass with an indirect procedure: technical case report. Neurosurgery. 2009;64:E195–196.
    1. Amin-Hanjani S, Du X, Mlinarevich N, Meglio G, Zhao M, Charbel FT. The cut flow index: an intraoperative predictor of the success of extracranial-intracranial bypass for occlusive cerebrovascular disease. Neurosurgery. 2005;56:75–85.
    1. Matsushima T, Fukui M, Kitamura K, Hasuo K, Kuwabara Y, Kurokawa T. Encephalo-duro-arterio-synangiosis in children with moyamoya disease. Acta Neurochir (Wien) 1990;104:96–102.
    1. Karasawa J, Kikuchi H, Furuse S, Sakaki T, Yoshida Y. A surgical treatment of “moyamoya” disease “encephalo-myo synangiosis”. Neurol Med Chir (Tokyo) 1977;17:29–37.
    1. Matsushima Y. Encephalo-duro-arterio-synangiosis: surgical anatomy associated with procedure. No Shinkei Geka. 1990;18:989–999.
    1. Kinugasa K, Mandai S, Kamata I, Sugiu K, Ohmoto T. Surgical treatment of moyamoya disease: operative technique for encephalo-duro-arterio-myo-synangiosis, its follow-up, clinical results, and angiograms. Neurosurgery. 1993;32:527–531.
    1. Irikura K, Miyasaka Y, Kurata A, Tanaka R, Yamada M, Kan S, et al. The effect of encephalo-myo-synangiosis on abnormal collateral vessels in childhood moyamoya disease. Neurol Res. 2000;22:341–346.
    1. Kawamoto H, Kiya K, Mizoue T, Ohbayashi N. A modified burr-hole method ‘galeoduroencephalosynangiosis’ in a young child with moyamoya disease. A preliminary report and surgical technique. Pediatr Neurosurg. 2000;32:272–275.
    1. Takeuchi S, Abe H, Ozawa T, Tanaka R. Surgical treatment for moyamoya disease. Surgical effect of encephalo-galeo-synangiosis on moyamoya disease. Surgery for Cerebral Strok. 2000;28:98–103.
    1. Kim CY, Wang KC, Kim SK, Chung YN, Kim HS, Cho BK. Encephaloduroarteriosynangiosis with bifrontal encephalogaleo (periosteal) synangiosis in the pediatric moyamoya disease: the surgical technique and its outcomes. Childs Nerv Syst. 2003;19:316–324.
    1. Kim SK, Wang KC, Kim IO, Lee DS, Cho BK. Combined encephaloduroarteriosynangiosis and bifrontal encephalogaleo (periosteal) synangiosis in pediatric moyamoya disease. Neurosurgery. 2002;50:88–96.
    1. Park JH, Yang SY, Chung YN, Kim JE, Kim SK, Han DH, et al. Modified encephaloduroarteriosynangiosis with bifrontal encephalogaleoperiosteal synangiosis for the treatment of pediatric moyamoya disease. Technical note. J Neurosurg. 2007;106:237–242.
    1. Song YS, Oh SW, Kim YK, Kim SK, Wang KC, Lee DS. Hemodynamic improvement of anterior cerebral artery territory perfusion induced by bifrontal encephalo(periosteal) synangiosis in pediatric patients with moyamoya disease: a study with brain perfusion SPECT. Ann Nucl Med. 2012;26:47–57.
    1. Kim DS, Kye DK, Cho KS, Song JU, Kang JK. Combined direct and indirect reconstructive vascular surgery on the frontoparieto-occipital region in moyamoya disease. Clin Neurol Neurosurg. 1997;99(Suppl 2):S137–141.
    1. Lee JY, Kim SK, Phi JH, Wang KC. Posterior Cerebral Artery Insufficiency in Pediatric Moyamoya Disease. J Korean Neurosurg Soc. 2015;57:436–439.
    1. Bruzoni M, Steinberg GK, Dutta S. Laparoscopic harvesting of omental pedicle flap for cerebral revascularization in children with moyamoya disease. J Pediatr Surg. 2015;19
    1. Havlik RJ, Fried I, Chyatte D, Modlin IM. Encephalo-omental synangiosis in the management of moyamoya disease. Surgery. 1992;111:156–162.
    1. Zhao X, Wang C, Ji Y, Han C, Wang M. Therapeutic effect of multiple burr hole operation combined with dural inversion and periosteal synangiosis for moyamoya disease. Br J Neurosurg. 2015:1–7.
    1. Kawaguchi T, Fujita S, Hosoda K, Shose Y, Hamano S, Iwakura M, et al. Multiple burr-hole operation for adult moyamoya disease. J Neurosurg. 1996;84:468–476.
    1. Kazumata K, Ito M, Tokairin K, Ito Y, Houkin K, Nakayama N, et al. The frequency of postoperative stroke in moyamoya disease following combined revascularization: a single-university series and systematic review. J Neurosurg. 2014;121:432–440.
    1. Funaki T, Takahashi JC, Takagi Y, Kikuchi T, Yoshida K, Mitsuhara T, et al. Unstable moyamoya disease: clinical features and impact on perioperative ischemic complications. J Neurosurg. 2015;122:400–407.
    1. Choi H, Lee JY, Phi JH, Kim SK, Cho BK, Wang KC. Postoperative epidural hematoma covering the galeal flap in pediatric patients with moyamoya disease: clinical manifestation, risk factors, and outcomes. J Neurosurg Pediatr. 2013;12:181–186.
    1. Fujimura M, Kaneta T, Mugikura S, Shimizu H, Tominaga T. Temporary neurologic deterioration due to cerebral hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in patients with adult-onset moyamoya disease. Surg Neurol. 2007;67:273–282.
    1. Fujimura M, Shimizu H, Inoue T, Mugikura S, Saito A, Tominaga T. Significance of focal cerebral hyperperfusion as a cause of transient neurologic deterioration after extracranial-intracranial bypass for moyamoya disease: comparative study with non-moyamoya patients using N-isopropyl-p-[(123)I]iodoamphetamine single-photon emission computed tomography. Neurosurgery. 2011;68:957–964.
    1. Uchino H, Kuroda S, Hirata K, Shiga T, Houkin K, Tamaki N. Predictors and clinical features of postoperative hyperperfusion after surgical revascularization for moyamoya disease: a serial single photon emission CT/positron emission tomography study. Stroke. 2012;43:2610–2616.
    1. Kim JE, Oh CW, Kwon OK, Park SQ, Kim SE, Kim YK. Transient hyperperfusion after superficial temporal artery/middle cerebral artery bypass surgery as a possible cause of postoperative transient neurological deterioration. Cerebrovasc Dis. 2008;25:580–586.
    1. Hayashi K, Horie N, Suyama K, Nagata I. Incidence and clinical features of symptomatic cerebral hyperperfusion syndrome after vascular reconstruction. World Neurosurg. 2012;78:447–454.
    1. Katsuta T, Inoue T, Arakawa S, Uda K. Cutaneous necrosis after superficial temporal artery-to-middle cerebral artery anastomosis: is it predictable or avoidable? Neurosurgery. 2001;49:879–882.
    1. Takanari K, Araki Y, Okamoto S, Sato H, Yagi S, Toriyama K, et al. Operative wound-related complications after cranial revascularization surgeries. J Neurosurg. 2015:1–6.
    1. Arias EJ, Dunn GP, Washington CW, Derdeyn CP, Chicoine MR, Grubb RL, Jr., et al. Surgical Revascularization in North American Adults with Moyamoya Phenomenon: Long-Term Angiographic Follow-up. J Stroke Cerebrovasc Dis. 2015;24:1597–1608.
    1. Bao XY, Duan L, Li DS, Yang WZ, Sun WJ, Zhang ZS, et al. Clinical features, surgical treatment and long-term outcome in adult patients with Moyamoya disease in China. Cerebrovasc Dis. 2012;34:305–313.
    1. Bao XY, Duan L, Yang WZ, Li DS, Sun WJ, Zhang ZS, et al. Clinical features, surgical treatment, and long-term outcome in pediatric patients with moyamoya disease in China. Cerebrovasc Dis. 2015;39:75–81.
    1. Funaki T, Takahashi JC, Takagi Y, Yoshida K, Araki Y, Kikuchi T, et al. Incidence of late cerebrovascular events after direct bypass among children with moyamoya disease: a descriptive longitudinal study at a single center. Acta Neurochir (Wien) 2014;156:551–559.
    1. Goda M, Isono M, Ishii K, Kamida T, Abe T, Kobayashi H. Long-term effects of indirect bypass surgery on collateral vessel formation in pediatric moyamoya disease. J Neurosurg. 2004;100:156–162.
    1. Gross BA, Du R. Adult moyamoya after revascularization. Acta Neurochir (Wien) 2013;155:247–254.
    1. Imai H, Miyawaki S, Ono H, Nakatomi H, Yoshimoto Y, Saito N. The importance of encephalo-myo-synangiosis in surgical revascularization strategies for moyamoya disease in children and adults. World Neurosurg. 2015;83:691–699.
    1. Karasawa J, Touho H, Ohnishi H, Miyamoto S, Kikuchi H. Long-term follow-up study after extracranial-intracranial bypass surgery for anterior circulation ischemia in childhood moyamoya disease. J Neurosurg. 1992;77:84–89.
    1. Kuroda S, Houkin K, Ishikawa T, Nakayama N, Iwasaki Y. Novel bypass surgery for moyamoya disease using pericranial flap: its impacts on cerebral hemodynamics and long-term outcome. Neurosurgery. 2010;66:1093–1101.
    1. Scott RM, Smith JL, Robertson RL, Madsen JR, Soriano SG, Rockoff MA. Long-term outcome in children with moyamoya syndrome after cranial revascularization by pial synangiosis. J Neurosurg. 2004;100:142–149.
    1. Han JS, Abou-Hamden A, Mandell DM, Poublanc J, Crawley AP, Fisher JA, et al. Impact of extracranial-intracranial bypass on cerebrovascular reactivity and clinical outcome in patients with symptomatic moyamoya vasculopathy. Stroke. 2011;42:3047–3054.
    1. Phi JH, Wang KC, Cho BK, Lee MS, Lee JH, Yu KS, et al. Long-term social outcome in children with moyamoya disease who have reached adulthood. J Neurosurg Pediatr. 2011;8:303–309.
    1. Shim KW, Park EK, Kim JS, Kim DS. Cognitive Outcome of Pediatric Moyamoya Disease. J Korean Neurosurg Soc. 2015;57:440–444.
    1. Nakagawa Y, Gotoh S, Shimoyama M, Ohtsuka K, Mabuchi S, Sawamura Y, et al. Reconstructive operation for moyamoya disease. Surgical indication for the hemorrhagic type, and preferable operative methods. Neurol Med Chir (Tokyo) 1983;23:464–470.
    1. Aoki N. Cerebrovascular bypass surgery for the treatment of Moyamoya disease: unsatisfactory outcome in the patients presenting with intracranial hemorrhage. Surg Neurol. 1993;40:372–377.
    1. Liu X, Zhang D, Shuo W, Zhao Y, Wang R, Zhao J. Long term outcome after conservative and surgical treatment of haemorrhagic moyamoya disease. J Neurol Neurosurg Psychiatry. 2013;84:258–265.
    1. Ahn JH, Wang KC, Phi JH, Lee JY, Cho BK, Kim IO, et al. Hemorrhagic moyamoya disease in children: clinical features and surgical outcome. Childs Nerv Syst. 2012;28:237–245.

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