ABSTRACT
Moyamoya syndrome, a vasculopathy characterized by chronic progressive stenosis at the apices of the intracranial internal carotid arteries, is an increasingly recognized entity which is associated with cerebral ischemia. Diagnosis is made on the basis of clinical and radiographic findings, including a characteristic stenosis of the internal carotid arteries in conjunction with abundant collateral vessel development. Adult moyamoya patients often present with hemorrhage, leading to rapid diagnosis. In contrast, children usually present with transient ischemic attacks or strokes, which may prove more difficult to diagnose because of patient's inadequate verbal and other skills, leading to delayed recognition of the underlying moyamoya. The progression of disease can be slow, with rare, intermittent events, or it can be fulminant, with rapid neurologic decline. However, regardless of the course, it is apparent that moyamoya syndrome, both in terms of arteriopathy and clinical symptoms, inevitably progresses in untreated patients.
Surgery is generally recommended for the treatment of patients with recurrent or progressive cerebral ischemic events and associated reduced cerebral perfusion reserve. Many different operative techniques have been described, all with the main goal of preventing further ischemic injury by increasing collateral blood flow to hypoperfused areas of the cortex, using the external carotid circulation as a donor supply. This article discusses the various treatment approaches, with an emphasis on the use of pial synangiosis, a method of indirect revascularization. The use of pial synangiosis is a safe, effective, and durable method of cerebral revascularization in moyamoya syndrome and should be considered as a primary treatment for moyamoya, especially in the pediatric population.
KEYWORDS
Moyamoya - pial synangiosis - ischemia - stroke
REFERENCES
-
1
Nagaraja D, Verma A, Taly A B, Kumar M V, Jayakumar P N.
Cerebrovascular disease in children.
Acta Neurol Scand.
1994;
90
251-255
-
2
Soriano S G, Sethna N F, Scott R M.
Anesthetic management of children with moyamoya syndrome.
Anesth Analg.
1993;
77
1066-1070
-
3
K. TKS .
Hypoplasia of the bilateral internal carotid arteries.
Brain Nerve.
1957;
9
37-43
-
4
Suzuki J, Takaku A.
Cerebrovascular “moyamoya” disease: disease showing abnormal net-like vessels in base of brain.
Arch Neurol.
1969;
20
288-299
-
5
Suzuki J, Kodama N.
Moyamoya disease-a review.
Stroke.
1983;
14
104-109
-
6
Caldarelli M, Di Rocco C, Gaglini P.
Surgical treatment of moyamoya disease in pediatric age.
J Neurosurg Sci.
2001;
45
83-91
-
7
Yonekawa Y, Ogata N, Kaku Y, Taub E, Imhof H G.
Moyamoya disease in Europe, past and present status.
Clin Neurol Neurosurg.
1997;
99
S58-S60
-
8
Han D H, Kwon O K, Byun B J et al..
A co-operative study: clinical characteristics of 334 Korean patients with moyamoya disease treated at neurosurgical institutes (1976-1994). The Korean Society for Cerebrovascular Disease.
Acta Neurochir (Wien).
2000;
142
1263-1273
-
9
Yilmaz E Y, Pritz M B, Bruno A, Lopez-Yunez A, Biller J.
Moyamoya: Indiana University Medical Center experience.
Arch Neurol.
2001;
58
1274-1278
-
10 Nishimoto UK A, Onbe H. Cooperative study on moyamoya disease in Japan. Cooperative study on moyamoya disease in Japan. 1981: 53-58
-
10a
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
-
11
Nakakita K, Tanaka S, Fukuda A, Fujii C, Kohama A, Miyasato H.
Nontraumatic acute subdural hematoma caused by the rupture of transdural anastomotic vessels in moyamoya disease [in Japanese].
No Shinkei Geka.
1994;
22
561-565
-
12 Ohaegbulam C, Scott R M. Moyamoya syndrome. In: McLone D Pediatric Neurosurgery Philadelphia, PA; WB Saunders 2001: 1077-1092
-
13
Hoshimaru M, Takahashi J A, Kikuchi H, Nagata I, Hatanaka M.
Possible roles of basic fibroblast growth factor in the pathogenesis of moyamoya disease: an immunohistochemical study.
J Neurosurg.
1991;
75
267-270
-
14
Takahashi A, Sawamura Y, Houkin K, Kamiyama H, Abe H.
The cerebrospinal fluid in patients with moyamoya disease (spontaneous occlusion of the circle of Willis) contains high level of basic fibroblast growth factor.
Neurosci Lett.
1993;
160
214-216
-
15
Suzui H, Hoshimaru M, Takahashi J A et al..
Immunohistochemical reactions for fibroblast growth factor receptor in arteries of patients with moyamoya disease.
Neurosurgery.
1994;
35
20-24
, discussion
24-25
-
16
Malek A M, Connors S, Robertson R L, Folkman J, Scott R M.
Elevation of cerebrospinal fluid levels of basic fibroblast growth factor in moyamoya and central nervous system disorders.
Pediatr Neurosurg.
1997;
27
182-189
-
17
Soriano S G, Cowan D B, Proctor M R, Scott R M.
Levels of soluble adhesion molecules are elevated in the cerebrospinal fluid of children with moyamoya syndrome.
Neurosurgery.
2002;
50
544-549
-
18
Ikeda E.
Systemic vascular changes in spontaneous occlusion of the circle of Willis.
Stroke.
1991;
22
1358-1362
-
19
Gordon N, Isler W.
Childhood moyamoya disease.
Dev Med Child Neurol.
1989;
31
103-107
-
20
Kitahara T, Ariga N, Yamaura A, Makino H, Maki Y.
Familial occurrence of moya-moya disease: report of three Japanese families.
J Neurol Neurosurg Psychiatry.
1979;
42
208-214
-
21
Sogaard I, Jorgensen J.
Familial occurrence of bilateral intracranial occlusion of the internal carotid arteries (Moya Moya).
Acta Neurochir (Wien).
1975;
31
245-252
-
22
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
-
23
Inoue T K, Ikezaki K, Sasazuki T, Matsushima T, Fukui M.
Linkage analysis of moyamoya disease on chromosome 6.
J Child Neurol.
2000;
15
179-182
-
24
Kestle J R, Hoffman H J, Mock A R.
Moyamoya phenomenon after radiation for optic glioma.
J Neurosurg.
1993;
79
32-35
-
25
Okuno T, Prensky A L, Gado M.
The moyamoya syndrome associated with irradiation of an optic glioma in children: report of two cases and review of the literature.
Pediatr Neurol.
1985;
1
311-316
-
26
Bitzer M, Topka H.
Progressive cerebral occlusive disease after radiation therapy.
Stroke.
1995;
26
131-136
-
27
Maki Y, Enomoto T.
Moyamoya disease.
Childs Nerv Syst.
1988;
4
204-212
-
28
Fukuyama Y, Umezu R.
Clinical and cerebral angiographic evolutions of idiopathic progressive occlusive disease of the circle of Willis (“moyamoya” disease) in children.
Brain Dev.
1985;
7
21-37
-
29
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
-
30
Chabbert V, Ranjeva J P, Sevely A, Boetto S, Berry I, Manelfe C.
Diffusion- and magnetisation transfer-weighted MRI in childhood moya-moya.
Neuroradiology.
1998;
40
267-271
-
31
Yamada I, Suzuki S, Matsushima Y.
Moyamoya disease: comparison of assessment with MR angiography and MR imaging versus conventional angiography.
Radiology.
1995;
196
211-218
-
32
Yamada I, Matsushima Y, Suzuki S.
Childhood moyamoya disease before and after encephalo-duro-arterio-synangiosis: an angiographic study.
Neuroradiology.
1992;
34
318-322
-
33
Yamada I, Matsushima Y, Suzuki S.
Moyamoya disease: diagnosis with three-dimensional time-of-flight MR angiography.
Radiology.
1992;
184
773-778
-
34
Yamada I, Suzuki S, Matsushima Y.
Moyamoya disease: diagnostic accuracy of MRI.
Neuroradiology.
1995;
37
356-361
-
35
Katz D A, Marks M P, Napel S A, Bracci P M, Roberts S L.
Circle of Willis: evaluation with spiral CT angiography, MR angiography, and conventional angiography.
Radiology.
1995;
195
445-449
-
36
Takanashi J I, Sugita K, Niimi H.
Evaluation of magnetic resonance angiography with selective maximum intensity projection in patients with childhood moyamoya disease.
Eur J Paediatr Neurol.
1998;
2
83-89
-
37
Chang K H, Yi J G, Han M H, Kim I O.
MR imaging findings of moyamoya disease.
J Korean Med Sci.
1990;
5
85-90
-
38
Kodama N, Aoki Y, Hiraga H, Wada T, Suzuki J.
Electroencephalographic findings in children with moyamoya disease.
Arch Neurol.
1979;
36
16-19
-
39
Takase K, Kashihara M, Hashimoto T.
Transcranial Doppler ultrasonography in patients with moyamoya disease.
Clin Neurol Neurosurg.
1997;
99
S101-S105
-
40
Morgenstern C, Griewing B, Muller-Esch G, Zeller J A, Kessler C.
Transcranial power-mode duplex ultrasound in two patients with moyamoya syndrome.
J Neuroimaging.
1997;
7
190-192
-
41
Takeuchi S, Tanaka R, Ishii R, Tsuchida T, Kobayashi K, Arai H.
Cerebral hemodynamics in patients with moyamoya disease. A study of regional cerebral blood flow by the 133Xe inhalation method.
Surg Neurol.
1985;
23
468-474
-
42
Nambu K, Suzuki R, Hirakawa K.
Cerebral blood flow: measurement with xenon-enhanced dynamic helical CT.
Radiology.
1995;
195
53-57
-
43
Liu H M, Peng S S, Li Y W.
The preoperative and postoperative cerebral blood flow and vasoreactivity in childhood moyamoya disease.
Keio J Med.
2000;
49
A86-A89
-
44
Shirane R, Yoshida Y, Takahashi T, Yoshimoto T.
Assessment of encephalo-galeo-myo-synangiosis with dural pedicle insertion in childhood moyamoya disease: characteristics of cerebral blood flow and oxygen metabolism.
Clin Neurol Neurosurg.
1997;
99
S79-S85
-
45
Scott R M.
Moyamoya syndrome: a surgically treatable cause of stroke in the pediatric patient.
Clin Neurosurg.
2000;
47
378-384
-
46
Scott R M.
Surgery for moyamoya syndrome? Yes.
Arch Neurol.
2001;
58
128-129
-
47
Matsushima T, Inoue T, Katsuta T et al..
An indirect revascularization method in the surgical treatment of moyamoya disease-various kinds of indirect procedures and a multiple combined indirect procedure.
Neurol Med Chir (Tokyo).
1998;
38
297-302
-
48
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
-
49
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
-
50
Sencer S, Poyanli A, Kiris T, Sencer A, Minareci O.
Recent experience with Moyamoya disease in Turkey.
Eur Radiol.
2000;
10
569-572
-
51
Houkin K, Kuroda S, Nakayama N.
Cerebral revascularization for moyamoya disease in children.
Neurosurg Clin N Am.
2001;
12
575-584
, ix
-
52
Dauser R C, Tuite G F, McCluggage C W.
Dural inversion procedure for moyamoya disease [technical note].
J Neurosurg.
1997;
86
719-723
-
53
Sato H, Ogawa A, Takahashi A et al..
Influence of superior cervical ganglion on cerebral hemodynamics-measurements of cerebral blood flow and metabolism during superior cervical ganglionectomy in patients with moyamoya disease [in Japanese].
No To Shinkei.
1990;
42
203-208
-
54
Ohtaki M, Uede T, Morimoto S, Nonaka T, Tanabe S, Hashi K.
Intellectual functions and regional cerebral haemodynamics after extensive omental transplantation spread over both frontal lobes in childhood moyamoya disease.
Acta Neurochir (Wien).
1998;
140
1043-1053
-
55
Matsushima T, Inoue T, Ikezaki K et al..
Multiple combined indirect procedure for the surgical treatment of children with moyamoya disease. A comparison with single indirect anastomosis with direct anastomosis.
Neurosurgical Focus.
1998;
5
, Article 4
-
56
Matsushima Y.
Indirect anastomoses for moyamoya disease [in Japanese].
No Shinkei Geka.
1998;
26
769-786
-
57
Yoshioka N, Tominaga S, Inui T.
Cerebral revascularization using omentum and serratus anterior muscle free flap transfer for adult moyamoya disease: case report.
Surg Neurol.
1996;
46
430-435
, discussion
435-436
-
58
Yoshioka N, Tominaga S, Suzuki Y et al..
Cerebral revascularization using omentum and muscle free flap for ischemic cerebrovascular disease.
Surg Neurol.
1998;
49
58-65
, discussion
65-56
-
59
Touho H, Karasawa J, Tenjin H, Ueda S.
Omental transplantation using a superficial temporal artery previously used for encephaloduroarteriosynangiosis.
Surg Neurol.
1996;
45
550-558
, discussion
558-559
-
60
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
-
61
Karasawa J, Touho H, Ohnishi H, Miyamoto S, Kikuchi H.
Cerebral revascularization using omental transplantation for childhood moyamoya disease.
J Neurosurg.
1993;
79
192-196
-
62
Havlik R J, Fried I, Chyatte D, Modlin I M.
Encephalo-omental synangiosis in the management of moyamoya disease.
Surgery.
1992;
111
156-162
-
63
Suzuki J, Takaku A, Kodama N, Sato S.
An attempt to treat cerebrovascular “Moyamoya” disease in children.
Childs Brain.
1975;
1
193-206
-
64
Mizoi K, Kayama T, Yoshimoto T, Nagamine Y.
Indirect revascularization for moyamoya disease: is there a beneficial effect for adult patients?.
Surg Neurol.
1996;
45
541-548
, discussion
548-549
-
65
Kashiwagi S, Kato S, Yasuhara S, Wakuta Y, Yamashita T, Ito H.
Use of a split dura for revascularization of ischemic hemispheres in moyamoya disease.
J Neurosurg.
1996;
85
380-383
-
66
Takemura S, Sato S, Kuroki A, Saito S, Kayama T.
New ideas for indirect revascularization surgery for moyamoya disease [in Japanese].
No Shinkei Geka.
1999;
27
987-992
-
67
Ikezaki K.
Rational approach to treatment of moyamoya disease in childhood.
J Child Neurol.
2000;
15
350-356
-
68
Nomura S, Kashiwagi S, Uetsuka S, Uchida T, Kubota H, Ito H.
Perioperative management protocols for children with moyamoya disease.
Childs Nerv Syst.
2001;
17
270-274
-
69
Lin Y, Yoshiko K, Negoro T, Watanabe K, Negoro M.
Cerebral oxygenation state in childhood moyamoya disease: a near-infrared spectroscopy study.
Pediatr Neurol.
2000;
22
365-369
-
70
Fujiwara J, Nakahara S, Enomoto T, Nakata Y, Takita H.
The effectiveness of O2 administration for transient ischemic attacks in moyamoya disease in children.
Childs Nerv Syst.
1996;
12
69-75
Edward R SmithM.D.
Department of Neurosurgery, The Children's Hospital Boston/Harvard Medical School
300 Longwood Ave., Boston, MA 02115
Email: edward.smith@childrens.harvard.edu
