Abstract
Moyamoya disease (MMD) is characterized by progressive stenosis or occlusion of the distal internal carotid artery and simultaneous formation of collateral vasculature. The fragile alteration and increased hemodynamic stress in the intra- and extracranial vasculature would conjointly result in the formation of intracranial aneurysms in MMD patients. According to our classification, the MMD-associated aneurysms are divided into the major artery aneurysms (MAAs) and non-MAAs. The non-MAAs are further subdivided into the distal choroidal artery aneurysms, moyamoya vessel aneurysms, transdural collateral aneurysms, and anastomosis aneurysms. Currently, endovascular treatment (EVT) has become the main stream for the MMD-associated aneurysms. There is no difference to EVT for the MMD-associated MAAs of the non-stenosed major arteries with that in the non-MMD patients. While it is a big challenge to perform EVT for MMD-associated aneurysms in the stenosed arteries. Generally speaking, the parent arteries of the non-MAAs are slim, and super-selective catheterization is technically difficult. Most of the times, parent artery occlusion with liquid embolic agents or coils can only be performed. The vasculature in MMD patients is fragile; perioperative management and meticulous intraoperative manipulation are also very important to avoid complications during EVT. In spites of the complications, the EVT can bring good outcome in selected cases of MMD-associated aneurysms.
Similar content being viewed by others
References
Aburakawa D, Fujimura M, Niizuma K, Sakata H, Endo H, Tominaga T (2017) Navigation-guided clipping of a de novo aneurysm associated with superficial temporal artery-middle cerebral artery bypass combined with indirect pial synangiosis in a patient with moyamoya disease. Neurosurg Rev 40:517–521. https://doi.org/10.1007/s10143-017-0866-4
Agarwalla PK, Walcott BP, Dunn IF, Thiex R, Frerichs K, Narang S, Friedlander RM (2014) Fusiform aneurysms of the lenticulostriate artery. J Clin Neurosci 21:373–377. https://doi.org/10.1016/j.jocn.2013.07.009
Amin-Hanjani S, Goodin S, Charbel FT, Alaraj A (2014) Resolution of bilateral moyamoya associated collateral vessel aneurysms: rationale for endovascular versus surgical intervention. Surg Neurol Int 5:S155–S160. https://doi.org/10.4103/2152-7806.134812
Ann Pollack D, Han SS (1994) Recurrent intracranial hemorrhage in an adult with moyamoya vasculopathy and a basilar artery aneurysm. J Stroke Cerebrovasc Dis 4:267–270. https://doi.org/10.1016/S1052-3057(10)80105-3
Arai Y, Matsuda K, Isozaki M, Nakajima T, Kikuta K (2011) Ruptured intracranial aneurysms associated with moyamoya disease: three case reports. Neurol Med Chir (Tokyo) 51:774–776. https://doi.org/10.2176/nmc.51.774
Arita K, Kurisu K, Ohba S, Shibukawa M, Kiura H, Sakamoto S, Uozumi T, Nakahara T (2003) Endovascular treatment of basilar tip aneurysms associated with moyamoya disease. Neuroradiology 45:441–444. https://doi.org/10.1007/s00234-003-0997-x
Bhattacharjee AK, Tamaki N, Minami H, Ehara K (1999) Moyamoya disease associated with basilar tip aneurysm. J Clin Neurosci 6:268–271. https://doi.org/10.1016/s0967-5868(99)90522-2
Chen H, Hou K, Wang X, Xu K, Yu J (2019) Spontaneous recession of a posterior cerebral artery aneurysm concurrent with carotid rete mirabile and moyamoya-pattern collateral vessels: a case report. BMC Neurol 19:51. https://doi.org/10.1186/s12883-019-1277-7
Chen Y, Dai D, Fang Y, Yang P, Huang Q, Zhao W, Xu Y, Liu J (2015) Endovascular treatment of ruptured large or wide-neck basilar tip aneurysms associated with moyamoya disease using the stent-assisted coil technique. J Stroke Cerebrovasc Dis 24:2229–2235. https://doi.org/10.1016/j.jstrokecerebrovasdis.2015.05.024
Choulakian A, Drazin D, Alexander MJ (2010) NBCA embolization of a ruptured intraventricular distal anterior choroidal artery aneurysm in a patient with moyamoya disease. J Neurointerv Surg 2:368–370. https://doi.org/10.1136/jnis.2010.002253
da Costa LB, Valiante T, Terbrugge K, Tymianski M (2006) Anterior ethmoidal artery aneurysm and intracerebral hemorrhage. AJNR Am J Neuroradiol 27:1672–1674
Daou B, Chalouhi N, Tjoumakaris S, Rosenwasser RH, Jabbour P (2015) Onyx embolization of a ruptured aneurysm in a patient with moyamoya disease. J Clin Neurosci 22:1693–1696. https://doi.org/10.1016/j.jocn.2015.05.017
Eom KS, Kim DW, Kang SD (2010) Intracerebral hemorrhage caused by rupture of a giant aneurysm complicating superficial temporal artery-middle cerebral artery anastomosis for moyamoya disease. Acta Neurochir 152:1069–1073; discussion 1073. https://doi.org/10.1007/s00701-009-0550-8
Fukuda N, Kanemaru K, Hashimoto K, Yoshioka H, Senbokuya N, Yagi T, Kinouchi H (2019) Embolization of a peripheral cerebral aneurysm associated with intracranial major artery occlusion through a transdural anastomotic artery: case report. Interv Neuroradiol 25:172–176. https://doi.org/10.1177/1591019918801539
Furtado SV, Medress ZA, Teo M, Steinberg GK (2019) Pathogenesis of aneurysms on major vessels in moyamoya disease and management outcome. J Clin Neurosci 61:219–224. https://doi.org/10.1016/j.jocn.2018.09.023
Gaba RC, Shah RP, Muskovitz AA, Guzman G, Michals EA (2008) Synchronous moyamoya syndrome and ruptured cerebral aneurysm in Alagille syndrome. J Clin Neurosci 15:1395–1398. https://doi.org/10.1016/j.jocn.2007.05.033
Gross BA, Thomas AJ, Frerichs KU (2014) Endovascular treatment of symptomatic moyamoya. Neurosurg Rev 37:579–583. https://doi.org/10.1007/s10143-014-0542-x
Hamada J, Hashimoto N, Tsukahara T (1994) Moyamoya disease with repeated intraventricular hemorrhage due to aneurysm rupture. Report of two cases. J Neurosurg 80:328–331. https://doi.org/10.3171/jns.1994.80.2.0328
Harreld JH, Zomorodi AR (2011) Embolization of an unruptured distal lenticulostriate aneurysm associated with moyamoya disease. AJNR Am J Neuroradiol 32:E42–E43. https://doi.org/10.3174/ajnr.A1993
Hou K, Guo Y, Xu K, Yu J (2019) Clinical importance of the superficial temporal artery in neurovascular diseases: a PRISMA-compliant systematic review. Int J Med Sci 16:1377–1385. https://doi.org/10.7150/ijms.36698
Hou K, Ji T, Guo Y, Xu K, Yu J (2019) The coexistence of persistent primitive trigeminal artery, moyamoya disease. And Multiple Intracranial Aneurysms: A Case Report And Literature Review World Neurosurg. https://doi.org/10.1016/j.wneu.2019.01.030
Hou K, Xu K, Chen X, Ji T, Guo Y, Yu J (2019) Targeted endovascular treatment for ruptured brain arteriovenous malformations. Neurosurg Rev 1:10. https://doi.org/10.1007/s10143-019-01205-1
Hwang K, Hwang G, Kwon OK (2014) Endovascular embolization of a ruptured distal lenticulostriate artery aneurysm in patients with moyamoya disease. J Korean Neurosurg Soc 56:492–495. https://doi.org/10.3340/jkns.2014.56.6.492
Ito Y, Nakai Y, Kino H, Koiso T, Nakamura K, Uemura K, Matsumura A (2014) Exacerbation of major artery aneurysms after revascularization in patients with moyamoya disease: two case reports. Neurol Med Chir (Tokyo) 54:832–835. https://doi.org/10.2176/nmc.cr.2014-0014
Iwama T, Todaka T, Hashimoto N (1997) Direct surgery for major artery aneurysm associated with moyamoya disease. Clin Neurol Neurosurg 99(Suppl 2):S191–S193. https://doi.org/10.1016/s0303-8467(97)00081-4
Jang DK, Lee KS, Rha HK, Huh PW, Yang JH, Park IS, Ahn JG, Sung JH, Han YM (2014) Clinical and angiographic features and stroke types in adult moyamoya disease. AJNR Am J Neuroradiol 35:1124–1131. https://doi.org/10.3174/ajnr.A3819
Kanamori F, Takasu S, Ota S, Seki Y (2018) Prevention of the rerupture of collateral artery aneurysms on the ventricular wall by early surgical revascularization in moyamoya disease: report of two cases and review of the literature. World Neurosurg 109:393–397. https://doi.org/10.1016/j.wneu.2017.10.059
Kawaguchi S, Sakaki T, Morimoto T, Kakizaki T, Kamada K (1996) Characteristics of intracranial aneurysms associated with moyamoya disease. A review of 111 cases. Acta Neurochir 138:1287–1294. https://doi.org/10.1007/bf01411057
Kim JH, Kwon TH, Kim JH, Chong K, Yoon W (2018) Intracranial aneurysms in adult moyamoya disease. World Neurosurg 109:e175–e182. https://doi.org/10.1016/j.wneu.2017.09.127
Kim SH, Choi JU, Yang KH, Kim TG, Kim DS (2005) Risk factors for postoperative ischemic complications in patients with moyamoya disease. J Neurosurg 103:433–438. https://doi.org/10.3171/ped.2005.103.5.0433
Kim SH, Kwon OK, Jung CK, Kang HS, Oh CW, Han MH, Kim YS, Baik SK (2009) Endovascular treatment of ruptured aneurysms or pseudoaneurysms on the collateral vessels in patients with moyamoya disease. Neurosurgery 65:1000–1004; discussion 1004. https://doi.org/10.1227/01.NEU.0000345648.46096.CE
Kim YS, Joo SP, Lee GJ, Park JY, Kim SD, Kim TS (2017) Ruptured choroidal artery aneurysms in patients with moyamoya disease: two case series and review of the literatures. J Clin Neurosci 44:236–239. https://doi.org/10.1016/j.jocn.2017.06.055
Koebbe CJ, Horowitz MB (2004) A rare case of a ruptured middle meningeal aneurysm causing intracerebral hematoma in a patient with moyamoya disease. AJNR Am J Neuroradiol 25:574–576
Lama S, Dolati P, Sutherland GR (2014) Controversy in the management of lenticulostriate artery dissecting aneurysm: a case report and review of the literature. World Neurosurg 81(441):e441–e447. https://doi.org/10.1016/j.wneu.2012.12.006
Larrazabal R, Pelz D, Findlay JM (2001) Endovascular treatment of a lenticulostriate artery aneurysm with N-butyl cyanoacrylate. Can J Neurol Sci 28:256–259. https://doi.org/10.1017/s0317167100001426
Lee CY (2018) Embolization with NBCA for ruptured aneurysm located in the moyamoya-like collateral network associated with isolated middle cerebral artery occlusion. Asian J Neurosurg 13:1236–1238. https://doi.org/10.4103/ajns.AJNS_127_17
Lee JK, Lee JH, Kim SH, Lee MC (2001) Distal anterior choroidal artery aneurysm in a patient with moyamoya disease: case report. Neurosurgery 48:222–225. https://doi.org/10.1097/00006123-200101000-00043
Leung GK, Lee R, Lui WM, Hung KN (2010) Thalamo-perforating artery aneurysm in moyamoya disease - case report. Br J Neurosurg 24:479–481. https://doi.org/10.3109/02688697.2010.487128
Li Q, Qu L, Yuan Y, Xu B, Guo Y, Xu K, Yu J (2018) Analysis of the clinical characteristics of hemorrhagic moyamoya disease in the Jilin province of northeastern China: a single-center study of 212 cases. Biomedical reports 8:191–197. https://doi.org/10.3892/br.2017.1030
Liu P, Lv X, Li Y, Lv M (2015) Onyx embolization of a ruptured rotundum foramen artery aneurysm in a patient with moyamoya disease: a case report. World Neurosurg 84(1178):e1171–e1173. https://doi.org/10.1016/j.wneu.2015.06.039
Luo Q, Wang H, Xu K, Yu J (2012) Endovascular treatments for distal posterior cerebral artery aneurysms. Turk Neurosurg 22:141–147. https://doi.org/10.5137/1019-5149.JTN.4079-11.0
Massoud TF, Guglielmi G, Vinuela F, Duckwiler GR (1994) Saccular aneurysms in moyamoya disease: endovascular treatment using electrically detachable coils. Surg Neurol 41:462–467. https://doi.org/10.1016/0090-3019(94)90008-6
Melot A, Chazot JV, Troude L, De la Rosa S, Brunel H, Roche PH (2016) Ruptured posterior ethmoidal artery aneurysm and moyamoya disease in an adult patient. Case report Neurochirurgie 62:171–173. https://doi.org/10.1016/j.neuchi.2016.04.001
Miyawaki S, Imai H, Takayanagi S, Mukasa A, Nakatomi H, Saito N (2012) Identification of a genetic variant common to moyamoya disease and intracranial major artery stenosis/occlusion. Stroke 43:3371–3374. https://doi.org/10.1161/STROKEAHA.112.663864
Moughamian AJ, Morshed RA, Colorado RA, Liner Z, Cooke D, Hemphill JC (2017) Teaching NeuroImages: artery of Percheron aneurysm masquerading as ICH spot sign. Neurology 89:e64–e65. https://doi.org/10.1212/WNL.0000000000004212
Mun HY, Nam TK, Choi HH, Park YS (2018) Rupture of a middle meningeal artery pseudoaneurysm in moyamoya syndrome related with Tuberculous meningitis. J Cerebrovasc Endovasc Neurosurg 20:187–190. https://doi.org/10.7461/jcen.2018.20.3.187
Nagamine Y, Takahashi S, Sonobe M (1981) Multiple intracranial aneurysms associated with moyamoya disease. Case report J Neurosurg 54:673–676. https://doi.org/10.3171/jns.1981.54.5.0673
Nishimoto T, Yuki K, Sasaki T, Murakami T, Kodama Y, Kurisu K (2005) A ruptured middle cerebral artery aneurysm originating from the site of anastomosis 20 years after extracranial-intracranial bypass for moyamoya disease: case report. Surg Neurol 64:261–265; discussion 265. https://doi.org/10.1016/j.surneu.2004.09.041
Nishio A, Hara M, Otsuka Y, Tsuruno T, Murata T (2004) Endovascular treatment of posterior cerebral aneurysm associated with moyamoya disease. J Neuroradiol 31:60–62
Ohba S, Shibao S, Tomita H, Nakagawa T, Akaji K, Murakami H (2014) Concurrent unilateral moyamoya disease and vertebrobasilar junction aneurysm associated with fenestration - case report and management. Clin Neurol Neurosurg 120:113–115. https://doi.org/10.1016/j.clineuro.2014.03.003
Park YS, Suk JS, Kwon JT (2010) Repeated rupture of a middle meningeal artery aneurysm in moyamoya disease. Case Report J Neurosurg 113:749–752. https://doi.org/10.3171/2009.11.JNS09895
Qi L, Jinlu Y (2013) Moyamoya disease with posterior communicating artery aneurysm: a case report. Turk Neurosurg 23:546–550. https://doi.org/10.5137/1019-5149.JTN.5668-11.1
Raabe A, Seidel K (2016) Prevention of ischemic complications during aneurysm surgery. J Neurosurg Sci 60:95–103
Rhim JK, Cho YD, Jeon JP, Yoo DH, Cho WS, Kang HS, Kim JE, Han MH (2018) Ruptured aneurysms of collateral vessels in adult onset moyamoya disease with hemorrhagic presentation. Clin Neuroradiol 28:191–199. https://doi.org/10.1007/s00062-016-0554-8
Robert T, Ciccio G, Sylvestre P, Chiappini A, Weil AG, Smajda S, Chaalala C, Blanc R, Reinert M, Piotin M, Bojanowski MW (2018) Anatomic and angiographic analyses of ophthalmic artery collaterals in moyamoya disease. AJNR Am J Neuroradiol 39:1121–1126. https://doi.org/10.3174/ajnr.A5622
Saito A, Kon H, Nakamura T, Sasaki T (2016) A dissecting aneurysm of the distal medial lenticulostriate artery: case report. World Neurosurg 89(725):e721–e724. https://doi.org/10.1016/j.wneu.2015.11.066
Satoh T, Yamamoto Y, Asari S, Sakurai M, Suzuki K (1983) Disappearance and development of cerebral aneurysms in moyamoya disease. Case Report J Neurosurg 58:949–953. https://doi.org/10.3171/jns.1983.58.6.0949
Schmalz PGR, Alturki A, Ogilvy CS, Thomas AJ (2017) Ruptured distal anterior choroidal artery aneurysm treated with superselective provocative testing and coil embolization. World Neurosurg 105:1032 e1019–1032 e1022. https://doi.org/10.1016/j.wneu.2017.05.176
Takeuchi S, Nawashiro H, Uozumi Y, Otani N, Osada H, Wada K, Shima K (2014) Chronic subdural hematoma associated with moyamoya disease. Asian J Neurosurg 9:165–167. https://doi.org/10.4103/1793-5482.142738
Umehara T, Goto Y, Kajikawa R, Wakayama A, Kishima H (2018) Life-threatening hemorrhagic moyamoya disease: report of rare case of atraumatic acute subdural hematoma due to ruptured transdural anastomosis. World Neurosurg 118:16–20. https://doi.org/10.1016/j.wneu.2018.06.197
Waldron JS, Hetts SW, Armstrong-Wells J, Dowd CF, Fullerton HJ, Gupta N, Lawton MT (2009) Multiple intracranial aneurysms and moyamoya disease associated with microcephalic osteodysplastic primordial dwarfism type II: surgical considerations. J Neurosurg Pediatr 4:439–444. https://doi.org/10.3171/2009.6.PEDS08137
Yamada H, Saga I, Kojima A, Horiguchi T (2019) Short-term spontaneous resolution of ruptured peripheral aneurysm in moyamoya disease. World Neurosurg 126:247–251. https://doi.org/10.1016/j.wneu.2019.02.193
Yamashita M, Oka K, Tanaka K (1983) Histopathology of the brain vascular network in moyamoya disease. Stroke 14:50–58. https://doi.org/10.1161/01.str.14.1.50
Yang S, Yu JL, Wang HL, Wang B, Luo Q (2010) Endovascular embolization of distal anterior choroidal artery aneurysms associated with moyamoya disease. A report of two cases and a literature review. Interv Neuroradiol 16:433–441. https://doi.org/10.1177/159101991001600410
Yeon JY, Kim JS, Hong SC (2011) Incidental major artery aneurysms in patients with non-hemorrhagic moyamoya disease. Acta Neurochir 153:1263–1270. https://doi.org/10.1007/s00701-011-0948-y
Yokota H, Yokoyama K, Noguchi H (2016) De novo aneurysm associated with superficial temporal artery to middle cerebral artery bypass: report of two cases and review of literature. World Neurosurg 92:583 e587–583 e512. https://doi.org/10.1016/j.wneu.2016.05.075
Yu J, Lv X, Li Y, Wu Z (2016) Therapeutic progress in pediatric intracranial dural arteriovenous shunts: a review. Interv Neuroradiol 22:548–556. https://doi.org/10.1177/1591019916653254
Yu J, Shi L, Guo Y, Xu B, Xu K (2016) Progress on complications of direct bypass for moyamoya disease. Int J Med Sci 13:578–587. https://doi.org/10.7150/ijms.15390
Yu JL, Wang HL, Xu K, Li Y, Luo Q (2010) Endovascular treatment of intracranial aneurysms associated with moyamoya disease or moyamoya syndrome. Interv Neuroradiol 16:240–248. https://doi.org/10.1177/159101991001600302
Yu JL, Wang HL, Xu N, Xu K, Wang B, Luo Q (2010) Endovascular treatment of aneurysms arising from the basilar artery trunk and branches. Interv Neuroradiol 16:369–383. https://doi.org/10.1177/159101991001600403
Yuasa H, Tokito S, Izumi K, Hirabayashi K (1982) Cerebrovascular moyamoya disease associated with an intracranial pseudoaneurysm. Case report J Neurosurg 56:131–134. https://doi.org/10.3171/jns.1982.56.1.0131
Zhang L, Xu K, Zhang Y, Wang X, Yu J (2015) Treatment strategies for aneurysms associated with moyamoya disease. Int J Med Sci 12:234–242. https://doi.org/10.7150/ijms.10837
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Kun Hou and Guichen Li are co-first authors.
Rights and permissions
About this article
Cite this article
Hou, K., Li, G., Luan, T. et al. The prospects and pitfalls in the endovascular treatment of moyamoya disease–associated intracranial aneurysms. Neurosurg Rev 44, 261–271 (2021). https://doi.org/10.1007/s10143-020-01261-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10143-020-01261-y