Abstract
Moyamoya is a rare though important source of neurological morbidity as a result of both ischemic and hemorrhagic sequelae. Although a litany of series detailing the endovascular management of cerebral ischemia is present in the literature, only a paucity of such reports exists for moyamoya. A systematic review of the literature was performed for patients with moyamoya managed with endovascular techniques in addition to the contribution of an additional case managed at our institution. We evaluated treatment approach (angioplasty and/or stent), complications, and both angiographic and clinical outcomes at last follow-up. Results from a total of 28 endovascular procedures were collected (11 stenting, 17 angioplasty alone). Procedural success, defined as a lack of both angiographic and clinical recurrence at follow-up, was achieved after seven procedures (25 %). This rate did not significantly differ between disease type (moyamoya disease vs moyamoya syndrome, p = 1.0) and treatment approach (angioplasty alone vs stenting, p = 1.0). The overall monthly angiographic and clinical recurrence rates were 9.3 and 8.0 %, respectively. Clinically devastating intracerebral hemorrhage was seen after two procedures (7 %), and in an additional three procedures, the treated vessel could not be effectively dilated (11 %). There is no evidence that angioplasty or stenting improves the natural history of moyamoya. Both are associated with significant rates of early angiographic and/or clinical recurrence of symptoms. Taken with the risk of procedural complications, the current limited data should advise against attempted endovascular treatment of moyamoya.
We’re sorry, something doesn't seem to be working properly.
Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.
Avoid common mistakes on your manuscript.
Introduction
Moyamoya disease is an idiopathic, bilateral progressive stenotic vasculopathy with the resultant formation of fragile, collateral “moyamoya” vessels [22, 24]. Unilateral disease or disease occurring secondary to known predisposing conditions such as neurofibromatosis, Down’s syndrome, radiation, and sickle cell disease, among others, are referred to as moyamoya syndrome [22]. Both moyamoya disease and moyamoya syndrome can serve as a considerable source of neurological morbidity as a result of recurrent ischemic events, and, in adults, hemorrhage [7, 10, 22, 24]. Ischemic events in both are known to be mitigated by direct revascularization [8–12] and, in children, indirect revascularization as well [6, 22, 23]. These neurosurgical tenets have withstood the test of time, in light of the results of the original extracranial-intracranial (EC-IC) bypass study [2] and the more recent Carotid Occlusion Surgery Study (COSS) study [19]. Although results of SAMMPRIS may mitigate endovascular approaches to cerebral ischemic disease [1], results of this study do not apply to moyamoya as it is pathogenetically different from atheromatous disease. Rather, this specific phenomenon should be evaluated separately. Currently, there is only a paucity of reports detailing endovascular approaches to moyamoya [3, 4, 13, 14, 18, 20, 21]. It is important to address whether this is merely a result of a bias for proven surgical revascularization methods or whether it is also a result of a lack of efficacy of these approaches. In this manuscript, we comprehensively review the literature on endovascular approaches to moyamoya, incorporating a case of our own while we evaluate treatment approach (angioplasty and/or stent), complications, and both angiographic and clinical outcomes at last follow-up.
Methods
We performed a comprehensive review of the literature querying the PubMed and Embase databases with the search terms, “moyamoya,” “endovascular,” “stent,” “wingspan,” and “angioplasty.” All reports describing angioplasty and/or stenting of stenotic intracranial vessels in a patient with moyamoya were collected. One report that described stenting of an atherosclerotic, stenosed external carotid artery in a patient with moyamoya was thus excluded [15].
We extracted patient age stratified into pediatric (age less than 18) or adult, pathology type (moyamoya disease vs moyamoya syndrome) treatment modality (angioplasty alone vs stent), vessel treated, procedural complications, and angiographic and clinical results at last follow-up. We also incorporated an attempt of our own among these results, representing 1 attempted endovascular approach in our last 50 consecutive patients seen by our neurosurgical service with moyamoya. Results were initially pooled and then segregated by approach (stenting vs angioplasty alone). All comparisons were performed employing the Fisher exact test. Monthly rates of angiographic and/or clinical recurrence were calculated by dividing the number of angiographic recurrences by the follow-up period (in months). This follow-up period concluded at the time of surgical revascularization, if performed. A clinical recurrence was defined by at least one recurrent transient ischemic attack or stroke after treatment.
Results
We collected results across a total of seven reports [3, 4, 13, 14, 18, 20, 21], adding our own case. Two of these were North American case series, the remainder single case reports. Notably, one of the case series included patients with moyamoya disease [13] while the other incorporated patients with moyamoya syndrome [18]. Overall, a total of 17 patients underwent 28 endovascular procedures (11 stenting, 17 angioplasty alone). Six patients had moyamoya disease and 11 had moyamoya syndrome (3 with idiopathic unilateral disease, 6 secondary to atherosclerosis, 1 child secondary to essential thrombocythemia, and another child secondary to a complex congenital syndromic condition). The vessel treated was the internal carotid artery (ICA) in 11 cases and the middle cerebral artery, first segment (M1) in 17 cases. All patients had symptomatic ischemic disease, and all but two were adults.
Overall, in three procedures, the vessel could not be effectively dilated (11 %), and after two, the procedure was complicated by clinically devastating intracerebral hemorrhage (7 %). Two procedural failures occurred in patients with moyamoya syndrome (11 % of procedures) and one in a patient with moyamoya disease (11 % of procedures, p = 1.0 as compared to moyamoya syndrome). One hemorrhage occurred in a patient with moyamoya syndrome (5 % of procedures) and another in a patient with moyamoya disease (11 % of procedures, p = 1.0 as compared to moyamoya syndrome).
For the remaining 23 procedures, the mean subsequent follow-up was 7.0 months, corresponding to a total of 161.5 patient-months. Angiographic recurrence was seen in 16 cases (70 %) while recurrence of clinical symptoms was seen in 13 cases (57 %). The monthly rates of each of these were 9.3 and 8.0 %, respectively. Angiographic recurrence occurred after 5/7 procedures performed in patients with moyamoya disease (71 %) and in 11/16 performed in patients with moyamoya syndrome (69 %, p = 1.0). Clinical recurrence occurred after 5/7 procedures performed in patients with moyamoya disease (71 %) and in 8/16 performed in patients with moyamoya syndrome (50 %, p = 0.41). Procedural success, defined as a lack of both angiographic and clinical recurrence at follow-up, was achieved after seven procedures (25 %); five performed in patients with moyamoya syndrome (26 % of procedures) and two in patients with moyamoya disease (22 % of procedures, p = 1.0). Of 15 patients that did not suffer devastating intracranial hemorrhages from their procedure, 8 ultimately underwent surgical revascularization (53 %).
Results stratified by treatment modality are provided in Tables 1 and 2. Twelve patients underwent 17 angioplasty procedures (Table 1) while 9 patients underwent 11 stenting procedures (Table 2). Of note, 10 of 11 stents deployed were Wingspan [3, 13, 18, 21], while the other was an AVE INX3 coronary stent [14]. There was no statistically significant difference between the angioplasty alone and stenting groups in the rate of post-procedural hemorrhage (6 % for angioplasty vs 9 % for stenting, p = 1.0), angiographic recurrence (66 % for angioplasty vs 70 % for stenting, p = 1.0), or clinical recurrence (54 % for angioplasty vs 60 % for stenting, p = 1.0). Technical procedural failure was not seen in any of the stenting cases, while it was seen in 3/17 angioplasty procedures (18 %, p = 0.26 vs stenting). Procedural success, defined as a lack of both angiographic and clinical recurrence at follow-up, was achieved after 24 % of angioplasty procedures and after 27 % of stenting cases (p = 1.0).
Discussion
Early enthusiasm for the endovascular management of non-acute cerebrovascular ischemic disease [16, 26] was tempered by the recent results of the SAMMPRIS trial [1], demonstrating greater rates of stroke or death at 30 days and 1 year after Wingspan stenting as compared to medical management of severe intracranial stenosis. However, these results do not apply to moyamoya given its significant pathophysiologic difference from atheromatous disease [5, 22]. More germane to moyamoya patients, a separate study evaluating patterns of Wingspan stent restenosis found significantly greater rates in younger patients and those with supraclinoid ICA stenosis [25].
Although a lack of efficacy was seen for surgical revascularization in patients with cerebral ischemic disease in the original EC-IC bypass [2] and COSS studies [1], results of these studies strongly contrast with the litany of reports describing the efficacy of surgical revascularization for moyamoya [6, 8–12, 23]. This review illustrates the remarkable lack of such studies evaluating endovascular approaches, a topic that is still reportable in a case report format [3, 4, 21]. Although the known success of surgical revascularization may limit consideration of endovascular approaches, the relative potential technical ease of endovascular therapies may have catalyzed an espousal of these approaches if they were efficacious. We feel the lack of reports detailing endovascular management of moyamoya underscores the limited efficacy of these approaches, as unsuccessful attempts such as our contributed case are less likely to be reported. Indeed, one of our incorporated case series comes from a tertiary referral center for surgical revascularization [13]. This center reported prior outside hospital endovascular results that preceded its own surgical revascularization. Interestingly, this series illustrated the efficacy of surgical revascularization after failed attempted endovascular treatment, as all patients were asymptomatic after direct revascularization procedures after a mean follow-up of 18 months [13].
It is noteworthy that the procedural success rate in our study, defined as freedom from angiographic and clinical recurrence, was only 25 %, almost a similar number to the procedural complication and failure rate (18–7 % hemorrhage rate, 11 % failure to dilate vessel rate). Intuitively, the success rate is also influenced by the follow-up period, which was frequently very limited, thus potentially inflating the actual procedural success rate. Although procedural risk other than hemorrhage was not clearly provided in all studies, it is likely in itself quite significant. Remarkably, 53 % of patients that did not suffer from hemorrhagic complications of the procedure ultimately underwent surgical revascularization anyhow. Most importantly, the rates of angiographic and clinical recurrence were exceedingly high, requiring analysis and reporting at a monthly rate—9.3 and 8.0 %, respectively. The relative lack of efficacy of endovascular approaches for moyamoya likely takes root in fundamental pathophysiologic differences of the disease [5, 22]. In particular, the fact that affected vessels do not show arteriosclerotic or inflammatory changes but rather smooth muscle cell hyperplasia and luminal thrombosis [5, 22] may in part explain a lack of efficacy of both angioplasty and stenting, with high rates of recurrence.
This study is limited by its very small size, brief reported follow-up periods, retrospective design, and incorporation of all reports, including case reports, which subjects results to a considerable degree of publication bias. Both cases series were from North American centers [13, 18], potentially limiting the external validity of our results to other patient populations. Nevertheless, this report strongly suggests against attempted endovascular approaches in the management of moyamoya, as both angioplasty alone and stenting are ostensibly fraught with high angiographic and clinical recurrence rates with procedural success rates similar to the combined procedural complication and initial failure rate. Although unproven, it would also seem intuitive that these approaches may prove detrimental in adult patients that may ultimately suffer from hemorrhagic moyamoya. Specifically, dual antiplatelet dependence would pose a significant problem in the context of a hemorrhagic event occurring as a result of the natural history of the disease. Although surgical revascularization is of unproven benefit for hemorrhagic moyamoya [17], it has demonstrated considerable promise in the prevention of recurrent ischemic events and should thus remain the treatment of choice.
Conclusion
An amalgamation of reports to date, although limited in number, demonstrates that endovascular treatment of symptomatic moyamoya via angioplasty and/or stenting is fraught with relatively high complication and recurrence rates. This early evidence should suggest against attempted endovascular management of symptomatic moyamoya.
References
Chimowitz MI, Lynn MJ, Derdeyn CP et al (2011) Stenting versus aggressive medical therapy for intracranial arterial stenosis. N Engl J Med 365:993–1003
EC/IC Bypass Study Group (1985) Failure of extracranial-intracranial arterial bypass to reduce the risk of ischemic stroke. Results of an international randomized trial. N Engl J Med 313:1191–1200
Eicker S, Etminan N, Turowski B, Steiger HJ, Hanggi D (2011) Intracranial carotid artery stent placement causes delayed severe intracranial hemorrhage in a patient with moyamoya disease. J Neurointervent Surg 3:160–162
El-Hakam LM, Volpi J, Mawad M, Clark G (2010) Angioplasty for acute stroke with pediatric moyamoya syndrome. J Child Neurol 25:1278–1283
Fukui M, Kono S, Sueishi K, Ikezaki K (2000) Moyamoya disease. Neuropathology 20(Suppl):S61–64
Fung LW, Thompson D, Ganesan V (2005) Revascularization surgery for paediatric moyamoya: a review of the literature. Childs Nerv Syst 21:358–364
Gross BA, Du R (2013) The natural history of adult moyamoya in a North American cohort. J Clin Neurosci 20:44–48
Gross BA, Du R (2013) Adult moyamoya after revascularization. Acta Neurochir 155:247–254
Guzman R, Lee M, Achrol A et al (2009) Clinical outcome after 450 revascularization procedures for moyamoya disease. J Neurosurg 111:927–935
Hallemeier CL, Rich KM, Grubb RL, Chicoine MR, Moran CJ, Cross DT et al (2006) Clinical features and outcome in North American adults with moyamoya phenomenon. Stroke 37:1490–1496
Karasawa J, Kikuchi H, Furuse S, Kawamura J, Sakaki T (1978) Treatment of moyamoya disease with STA-MCA anastomosis. J Neurosurg 49:679–688
Karasawa J, Touho H, Ohnishi H, Miyamoto S, Kikuchi H (1992) Long-term follow-up study after extracranial-intracranial bypass surgery for anterior circulation ischemia in childhood moyamoya disease. J Neurosurg 77:84–89
Khan N, Dodd R, Marks MP, Bell-Stephens T, Vavao J, Steinberg GK (2011) Failure of primary percutaneous angioplasty and stenting in the prevention of ischemia in Moyamoya angiopathy. Cerebrovasc Dis 31:147–153
Kornblihtt LI, Cocorullo S, Miranda C, Lylyk P, Heller PG, Molinas FC (2005) Moyamoya syndrome in an adolescent with essential thrombocythemia: successful intracranial carotid stent placement. Stroke 36:E71–73
Lee SJ, Ahn JY (2007) Stenosis of the proximal external carotid artery in an adult with moyamoya disease: moyamoya or atherosclerotic change? Neurol Med Chir (Tokyo) 47:e9
Marks MP, Wojak JC, Al-Ali F, Jayaraman M, Marcellus ML, Connors JJ, Do HM (2006) Angioplasty for symptomatic intracranial stenosis: clinical outcome. Stroke 37:1016–1020
Miyamoto S (2004) Japan Adult Moyamoya Trial Group: 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) 44:218–219
Natarajan SK, Karmon Y, Tawk RG, Hauck EF, Hopkins LN, Siddiqui AH, Levy EI (2011) Endovascular treatment of patients with intracranial stenosis with moyamoya-type collaterals. J Neurointervent Surg 3:369–374
Powers WJ, Clarke WR, Grubb RL et al (2011) Extracranial-intracranial bypass surgery for stroke prevention in hemodynamic cerebral ischemia. The Carotid Occlusion Surgery Study Randomized Trial. JAMA 306:1983–1992
Rodriguez GJ, Kirmani JF, Ezzeddine MA, Qureshi AI (2007) Primary percutaneous transluminal angioplasty for early moyamoya disease. J Neuroimaging 17:48–53
Santirso D, Oliva P, Gonzalez M, Murias E, Vega P, Gil A, Calleja S (2012) Intracranial stent placement in a patient with moyamoya disease. J Neurol 259:170–171
Scott RM, Smith ER (2009) Moyamoya disease and moyamoya syndrome. N Engl J Med 360:1226–1237
Scott RM, Smith JL, Robertson RL, Madsen JR, Soriano SG, Rockoff MA (2004) Long-term outcome in children with moyamoya syndrome after cranial revascularization by pial synangiosis. J Neurosurg. 100 (2Suppl Pediatrics): 142–149
Suzuki J, Takaku A (1969) Cerebrovascular “moyamoya” disease: disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288–299
Turk AS, Levy EI, Albuquerque FC et al (2008) Influence of patient age and stenosis location on wingspan in-stent restenosis. AJNR Am J Neuroradiol 29:23–27
Wojak JC, Dunlap DC, Hargrave KR, DeAlvareLA CHS, Connors JJ 3rd (2006) Intracranial angioplasty and stenting: long term results from a single center. AJNR AmJ Neuroradiol 27:1882–1892
Conflict of interest
The authors both declare no conflicts of interest/disclosures.
Author information
Authors and Affiliations
Corresponding author
Additional information
Comments
Gerasimos Baltsavias, Zurich, Switzerland
This report by Gross et al. is a well-presented review of the literature on the methods of treatment, results, and complications of endovascular management of symptomatic moyamoya disease and syndrome. The few reports existing in the literature and reviewed by the authors included mostly adult cases. They demonstrated relatively high recurrence and complication rates, suggesting against endovascular treatment and in favor of surgical revascularization. No significant difference in their response to endovascular treatment was found between disease and syndromic cases. Although the collected reports reflect a relatively early and limited experience, this is in accordance with our own experience and current view.
Lotfi Hacein-Bey, Sacramento, USA
In this issue of Neurosurgical Review, Gross et al. present a comprehensive review of endovascular therapy for moyamoya disease or syndrome. Although the lack of effectiveness of angioplasty or stenting in moyamoya has long been an established concept for specialized teams, eloquently reported in a relatively large case series by Khan et al. (reference 13 in the article), this review is helpful in educating the readership in this time of rapid development of minimally invasive endovascular options for cerebrovascular disease. Since the initial description by Suzuki and Takaku in 1969, our understanding of the molecular foundation and the natural history of moyamoya disease has progressed in a relatively modest way. Certain features appear to be common to all varieties of moyamoya, including the Japanese, North American, and European forms of moyamoya disease and moyamoya syndrome. First, overexpression of basic fibroblast growth factor (bFGF) and transforming growth factor-beta (TGF-β) and a local inflammatory response result in marked intimal thickening from elastin accumulation and significant thinning of the internal elastic lamina which affect large arterial trunks, i.e., the carotid artery and the proximal MCA as well as pial arteries; in addition, there is overexpression of an angiogenic response within the meninges. Second, adult patients present with both ischemic and hemorrhagic events, including a risk of hyperperfusion after treatment. Third, there is often lack of correlation between the severity of angiographic findings and the clinical expression of the disease, in large part because of complex and dynamic rearrangements of global and regional cerebral blood flow. The histopathological changes which affect arteries in moyamoya are for a large part responsible for both a high risk of arterial rupture with angioplasty and a very high incidence of restenosis. Therefore, until the advent of a successful therapy for moyamoya, possibly relying on endothelial progenitor cells or vascular growth factors, the only effective treatment remains surgical, with either direct or indirect revascularization techniques.
Rights and permissions
About this article
Cite this article
Gross, B.A., Thomas, A.J. & Frerichs, K.U. Endovascular treatment of symptomatic moyamoya. Neurosurg Rev 37, 579–583 (2014). https://doi.org/10.1007/s10143-014-0542-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10143-014-0542-x