Moyamoya Disease in Adults: The Role of Cerebral Revascularization

Gregory J. Zipfel; Douglas J. Fox; Dennis J. Rivet

doi:10.1055/s-2005-868161

Skull Base, Inhaltsverzeichnis

Skull Base 2005; 15(1): 27-41
DOI: 10.1055/s-2005-868161

Moyamoya Disease in Adults: The Role of Cerebral Revascularization

Gregory J. Zipfel¹ ^, ² , Douglas J. Fox¹ Jr. , Dennis J. Rivet¹ ^, ³

¹Departments of Neurological Surgery, Washington University School of Medicine, St. Louis, Missouri
²Departments of Neurology, Washington University School of Medicine, St. Louis, Missouri
³Departments of Radiology, Washington University School of Medicine, St. Louis, Missouri

Abstract

ABSTRACT

Moyamoya disease is a disorder characterized by bilateral progressive steno-occlusion of the terminal internal carotid arteries with associated development of a fragile network of basal collateral vessels. It most commonly presents in children, but is also frequently seen in adults, especially in the third or fourth decade of life. Adults afflicted with this disease have very different clinical characteristics as compared with children. For example, adults more commonly present with hemorrhage than cerebral ischemia, while children present with cerebral ischemia nearly 75% of the time and very rarely present with hemorrhage. This significantly impacts treatment considerations for the adult-onset moyamoya patient, as cerebral revascularization, though well accepted in the context of cerebral ischemia, is relatively controversial for the prevention of rehemorrhage. The purpose of this article is to review the pertinent general features of moyamoya disease, examine the clinical characteristics associated with the adult-onset form of this disease, and provide a detailed discussion regarding the indications, operative techniques, and outcomes of direct and indirect revascularization surgical procedures.

KEYWORDS

Moyamoya disease - hemorrhage - ischemia - revascularization - adult

Volltext

Referenzen

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
2 Fukui M. Guidelines for the diagnosis and treatment of spontaneous occlusion of the circle of Willis (“Moyamoya” disease). Clin Neurol Neurosurg. 1997; 99 S238-S240
3 Kawano T, Fukui M, Hashimoto N, Yonekawa Y. Follow-up study of patients with “unilateral” moyamoya disease. Neurol Med Chir (Tokyo). 1994; 34 744-747
4 Hirotsune N, Meguro T, Kawada S, Nakashima H, Ohmoto T. Long-term follow-up study of patients with unilateral moyamoya disease. Clin Neurol Neurosurg. 1997; 99 S178-S181
5 Hosoda Y. Pathology of so-called “spontaneous occusion of the circle of Willis.” Pathol Annu. 1984; 19 221-244
6 Yamashita M, Oka K, Tanaka K. Histopathology of the brain vascular network in moyamoya disease. Stroke. 1983; 14 50-58
7 Masuda J, Ogata J, Yutani C. Smooth muscle cell proliferation and localization of macrophages and T cells in the occlusive intracranial major arteries in moyamoya disease. Stroke. 1993; 24 1960-1967
8 Mauro A J, Johnson E S, Chikos P M, Alvord E C Jr. Lipohyalinosis and miliary microaneurysms causing cerebral hemorrhage in a patient with moyamoya. A clinicopathological study. Stroke. 1980; 11 405-412
9 Oka K, Yamashita M, Sadoshima S, Tanaka K. Cerebral haemorrhage in Moyamoya disease at autopsy. Virchows Arch A Pathol Anat Histol. 1981; 392 247-261
10 Wakai K, Tamakoshi A, Ikezaki K et al.. Epidemiological features of moyamoya disease in Japan: findings from a nationwide survey. Clin Neurol Neurosurg. 1997; 99 S1-S5
11 Hoffman H J. Moyamoya disease and syndrome. Clin Neurol Neurosurg. 1997; 99 S39-S44
12 Chiu D, Shedden P, Bratina P, Grotta J C. Clinical features of moyamoya disease in the United States. Stroke. 1998; 29 1347-1351
13 Numaguchi Y, Gonzalez C F, Davis P C et al.. Moyamoya disease in the United States. Clin Neurol Neurosurg. 1997; 99 S26-S30
14 Maki Y, Enomoto T. Moyamoya disease. Childs Nerv Syst. 1988; 4 204-212
15 Suzuki J, Kodama N. Moyamoya disease-a review. Stroke. 1983; 14 104-109
16 Kudo T, Fukuta S. Spontaneous occlusion of the circle of Willis. Shinkei-Shimpo. 1976; 20 750-757
17 Kudou T. Obstruction of circle of Willis: moyamoya disease. Int Med (Tokyo). 1977; 28 465-469
18 Houkin K, Tanaka N, Takahashi A, Kamiyama H, Abe H, Kajii N. Familial occurrence of moyamoya disease. Magnetic resonance angiography as a screening test for high-risk subjects. Childs Nerv Syst. 1994; 10 421-425
19 Yamauchi T, Houkin K, Tada M, Abe H. Familial occurrence of moyamoya disease. Clin Neurol Neurosurg. 1997; 99 S162-S167
20 Yamauchi T, Tada M, Houkin K et al.. Linkage of familial moyamoya disease (spontaneous occlusion of the circle of Willis) to chromosome 17q25. Stroke. 2000; 31 930-935
21 Handa H, Yonekawa Y, Goto Y et al.. Analysis of the filing data bank of 1500 cases of spontaneous occlusion of the circle of Willis and follow‐up study of 200 cases for more than five years. In: Handa H Annual Report (1984) by Research Committee on Spontaneous Occlusion of the Circle of Willis Japan; Ministry of Health and Welfare 1985 14
22 Kobayashi E, Saeki N, Oishi H, Hirai S, Yamaura A. Long-term natural history of hemorrhagic moyamoya disease in 42 patients. J Neurosurg. 2000; 93 976-980
23 Han D H, Nam D H, Oh C W. Moyamoya disease in adults: characteristics of clinical presentation and outcome after encephalo-duro-arterio-synangiosis. Clin Neurol Neurosurg. 1997; 99 S151-S155
24 Takahashi A, Fujiwara S, Suzuki J. Long-term follow-up angiography of moyamoya disease-cases followed from childhood to adolescence [in Japanese]. No Shinkei Geka. 1986; 14 23-29
25 Houkin K, Aoki T, Takahashi A, Abe H. Diagnosis of moyamoya disease with magnetic resonance angiography. Stroke. 1994; 25 2159-2164
26 Suzuki J. Moyamoya Disease. Tokyo, Japan; Springer-Verlag 1986
27 McLean M J, Gebarski S S, van der Spek A F, Goldstein G W. Response of moyamoya disease to verapamil. Lancet. 1985; 1 163-164
28 Spittler J F, Smektala K. Pharmacotherapy in moyamoya disease. Hokkaido Igaku Zasshi. 1990; 65 235-240
29 Hosain S A, Hughes J T, Forem S L, Wisoff J, Fish I. Use of a calcium channel blocker (nicardipine HCl) in the treatment of childhood moyamoya disease. J Child Neurol. 1994; 9 378-380
30 Imaizumi T, Hayashi K, Saito K, Osawa M, Fukuyama Y. Long-term outcomes of pediatric moyamoya disease monitored to adulthood. Pediatr Neurol. 1998; 18 321-325
31 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
32 Isono M, Ishii K, Kamida T, Inoue R, Fujiki M, Kobayashi H. Long-term outcomes of pediatric moyamoya disease treated by encephalo-duro-arterio-synangiosis. Pediatr Neurosurg. 2002; 36 14-21
33 Karasawa J, Kikuchi H, Furuse S, Kawamura J, Sakaki T. Treatment of moyamoya disease with STA-MCA anastomosis. J Neurosurg. 1978; 49 679-688
34 Matsushima Y, Fukai N, Tanaka K et al.. A new surgical treatment of moyamoya disease in children: a preliminary report. Surg Neurol. 1981; 15 313-320
35 Houkin K, Kamiyama H, Abe H, Takahashi A, Kuroda S. Surgical therapy for adult moyamoya disease. Can surgical revascularization prevent the recurrence of intracerebral hemorrhage?. Stroke. 1996; 27 1342-1346
36 Iwama T, Hashimoto N, Murai B N, Tsukahara T, Yonekawa Y. Intracranial rebleeding in moyamoya disease. J Clin Neurosci. 1997; 4 169-170
37 Fujii K, Ikezaki K, Irikura K, Miyasaka Y, Fukui M. The efficacy of bypass surgery for the patients with hemorrhagic moyamoya disease. Clin Neurol Neurosurg. 1997; 99 S194-S195
38 Okada Y, Shima T, Nishida M, Yamane K, Yamada T, Yamanaka C. Effectiveness of superficial temporal artery-middle cerebral artery anastomosis in adult moyamoya disease: cerebral hemodynamics and clinical course in ischemic and hemorrhagic varieties. Stroke. 1998; 29 625-630
39 Yoshida Y, Yoshimoto T, Shirane R, Sakurai Y. Clinical course, surgical management, and long-term outcome of moyamoya patients with rebleeding after an episode of intracerebral hemorrhage: an extensive follow-up study. Stroke. 1999; 30 2272-2276
40 Kawaguchi S, Okuno S, Sakaki T. Effect of direct arterial bypass on the prevention of future stroke in patients with the hemorrhagic variety of moyamoya disease. J Neurosurg. 2000; 93 397-401
41 Miyamoto S. Study design for a prospective randomized trial of extracranial-intracranial bypass surgery for adults with moyamoya disease and hemorrhagic onset-the Japan Adult Moyamoya Trial Group. Neurol Med Chir (Tokyo). 2004; 44 218-219
42 , [No authors listed]. Failure of extracranial-intracranial arterial bypass to reduce the risk of ischemic stroke. Results of an international randomized trial. The EC/IC Bypass Study Group. N Engl J Med. 1985; 313 1191-200
43 Houkin K, Ishikawa T, Yoshimoto T, Abe H. Direct and indirect revascularization for moyamoya disease surgical techniques and peri-operative complications. Clin Neurol Neurosurg. 1997; 99 S142-S145
44 Robertson R L, Burrows P E, Barnes P D, Robson C D, Poussaint T Y, Scott R M. Angiographic changes after pial synangiosis in childhood moyamoya disease. AJNR Am J Neuroradiol. 1997; 18 837-845
45 Houkin K, Kuroda S, Abe H. Operative record using intraoperative digital data in neurosurgery. Acta Neurochir (Wien). 2000; 142 913-919
46 Asforsa W T, West M, McClarty B. Angiography of encephalomyosynangiosis and superficial temporal artery to middle cerebral artery anastomosis in moyamoya disease. AJNR Am J Neuroradiol. 1993; 14 29-30
47 Wanebo J E, Zabramski J M, Spetzler R F. Superficial temporal artery-to-middle cerebral artery bypass grafting for cerebral revascularization. Neurosurgery. 2004; 55 395-398 , discussion 398-399
48 Newell D W, Vilela M D. Superficial temporal artery to middle cerebral artery bypass. Neurosurgery. 2004; 54 1441-1448 , discussion 1448-1449
49 Henschen C. Surgical revascularization of cerebral injury of circulatory origin by means of stratification of pedunculated muscle flaps [in German]. Langenbecks Arch Klin Chir Ver Dtsch Z Chir. 1950; 264 392-401
50 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
51 Ausman J I, Moore J, Chou S N. Spontaneous cerebral revascularization in a patient with STA-MCA anastomosis. Case report. J Neurosurg. 1976; 44 84-87
52 Tubokawa T, Kikuchi M, Asano S, Ito H, Urabe M. Surgical treatment for intracranial thrombosis. Case report of “durepexia” [in Japanese]. Neurol Med Chir (Tokyo). 1964; 6 47-48
53 Adelson P D, Scott R M. Pial synangiosis for moyamoya syndrome in children. Pediatr Neurosurg. 1995; 23 26-33
54 Scott R M, Smith J L, Robertson R L, Madsen J R, Soriano S G, Rockoff M A. Long-term outcome in children with moyamoya syndrome after cranial revascularization by pial synangiosis. J Neurosurg Spine. 2004; 100 142-149
55 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
56 Suzuki R, Matsushima Y, Takada Y, Nariai T, Wakabayashi S, Tone O. Changes in cerebral hemodynamics following encephalo-duro-arterio-synangiosis (EDAS) in young patients with moyamoya disease. Surg Neurol. 1989; 31 343-349
57 Kinugasa K, Mandai S, Tokunaga K et al.. Ribbon enchephalo-duro-arterio-myo-synangiosis for moyamoya disease. Surg Neurol. 1994; 41 455-461
58 Kim S K, Wang K C, Kim I O, Lee D S, Cho B K. Combined encephaloduroarteriosynangiosis and bifrontal encephalogaleo(periosteal)synangiosis in pediatric moyamoya disease. Neurosurgery. 2002; 50 88-96
59 Kawaguchi T, Fujita S, Hosoda K et al.. Multiple burr-hole operation for adult moyamoya disease. J Neurosurg. 1996; 84 468-476
60 Suzuki J, Takaku A, Kodama N, Sato S. An attempt to treat cerebrovascular “Moyamoya” disease in children. Childs Brain. 1975; 1 193-206
61 Yasargil M G, Yonekawa Y, Denton I, Piroth D, Benes I. Experimental intracranial transplantation of autogenic omentum majus. J Neurosurg. 1974; 40 213-217
62 Karasawa J, Kikuchi H, Kawamura J, Sakai T. Intracranial transplantation of the omentum for cerebrovascular moyamoya disease: a two-year follow-up study. Surg Neurol. 1980; 14 444-449
63 Imaizumi T, Hashi K. A basic study on omental transplantation. Vascular endothelial cell growth factor in human omentum [in Japanese]. Neurol Med Chir (Tokyo). 1991; 31 839-845
64 Endo M, Kawano N, Miyaska Y, Yada K. Cranial burr hole for revascularization in moyamoya disease. J Neurosurg. 1989; 71 180-185
65 Suzuki J, Iwabuchi T, Hori S. Cervical sympathectomy for cerebral vasospasm after aneurysm rupture. Neurol Med Chir (Tokyo). 1975; 15 41-50
66 Matsushima T, Inoue T, Suzuki S O, Fujii K, Fukui M, Hasuo K. Surgical treatment of moyamoya disease in pediatric patients-comparison between the results of indirect and direct revascularization procedures. Neurosurgery. 1992; 31 401-405
67 Kim D S, Kye D K, Cho K S, Song J U, Kang J K. Combined direct and indirect reconstructive vascular surgery on the fronto-parieto-occipital region in moyamoya disease. Clin Neurol Neurosurg. 1997; 99 S137-S141

Gregory J ZipfelM.D.

Washington University School of Medicine, Department of Neurological Surgery, 660 S. Euclid Ave.

Campus Box 8057, St. Louis, MO 63110

eMail: zipfelg@nsurg.wustl.edu