Abstract
Background
To clarify the most beneficial treatment of the management modality based on our experience with adult moyamoya disease (MMD).
Methods
From 1998 to 2010, clinical results of 142 patients (ischemic, 98; hemorrhagic, 44) with adult MMD were investigated according to management modality. Revascularization surgery (direct, indirect, and combined bypass) was performed in 124 patients. We observed the clinical course of 18 patients who were treated conservatively. Clinical outcome, angiographic features, hemodynamic change, and incidence of recurrent stroke were investigated pre- and postoperatively.
Results
In patients with ischemic MMD, direct and combined bypasses were more effective treatments to prevent recurrent ischemic stroke than indirect bypass surgery (P < 0.05). In patients with hemorrhagic MMD, rebleeding was less likely to occur in patients who had undergone bypass surgery. However, no significant difference was observed in the rebleeding rate between patients with and without revascularization surgery (P > 0.05). An angiogram after bypass surgery comparing the extent of revascularization and reduction of moyamoya vessels in patients treated with direct, indirect, and combined bypass showed a significant difference (P < 0.05) in favor of direct and combined bypass. Postoperative angiographic changes and SPECT results demonstrated significant statistical correlation (P < 0.05).
Conclusion
Revascularization surgery was effective in further ischemic stroke prevention to a statistically significant extent. Direct and combined bypasses were more effective to prevent recurrent ischemic stroke than indirect bypass. However, there is still no clear evidence that revascularization surgery significantly prevents rebleeding in adult MMD patients. More significant angiographic changes were observed in direct and combined bypasses compared with indirect bypass.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
Introduction
Moyamoya disease, as first described in the Japanese medical literature in 1957 by Takeuchi and Shimizu, is a rare, cerebrovascular disorder characterized by idiopathic, progressive occlusion of bilateral supraclinoidal internal carotid arteries and the development of an extensive basal cerebral collateral vascular network [35, 36]. Moyamoya disease can be divided into two clinical entities: juvenile- and adult-onset types [11, 34]. Adult patients’ clinical features are much different from those seen in juvenile patients. Most juvenile patients develop ischemic events in all stages of MMD, whereas the hemorrhagic event is prevalent among adults [34, 40].
The incidence of disease progression in adult MMD is much higher than recognized before [8, 17, 22, 33, 37]. Therefore, symptomatic adult MMD should be treated as soon as possible, similar to juvenile MMD. Based on previous reports, revascularization surgery has been shown to improve clinical symptoms and reduce the incidence of subsequent ischemic stroke in pediatric patients [16, 18, 19, 24]. There is some controversy regarding the prevention of recurrent hemorrhagic events in adult MMD [1, 13, 14, 28, 31, 40]. We have used many surgical techniques to enhance cerebral revascularization in adult patients with MMD: direct revascularization via the superficial temporal artery (STA)–middle cerebral artery (MCA) anastomosis, indirect bypass surgery such as encephaloduroarteriosynangiosis (EDAS), encephalomyosynangiosis (EMS), encephaloduroarteriogaleosynangiosis (EDAGS), and a combined STA-MCA anastomosis with EDAGS surgery using an inverted STA-galeal flap (GF) and STA-galeal pedicle (GP).
We present a retrospective analysis of adults with MMD admitted and treated at our institution during the last 13 years. We aimed to clarify the most beneficial treatment for preventing recurrent stroke in symptomatic adult MMD patients. In addition we investigated which surgical modality was associated with postoperative angiographic change and SPECT results.
Clinical material and methods
Patient selection, inclusion criteria, and operative procedure
From 1998 to 2010, 169 patients were diagnosed with adult MMD (≥18 years of age) and admitted and treated at our institution. In this study, we retrospectively analyzed records of 142 patients who were followed up for over 1 year, from onset until 2010.
All patients had ischemic or hemorrhagic symptoms. The diagnosis of MMD was made based on angiography according to published guidelines [9]. All patients presenting ischemic and hemorrhagic symptoms were evaluated with computed tomography (CT), computed tomographic perfusion (CTP), magnetic resonance imaging (MRI) including diffusion-weighted imaging (DWI), and fluid attenuated inversed recovery (FLAIR) imaging to assess the overall stroke burden. Preoperative 6-vessel angiography was performed in all patients to determine disease severity and to evaluate the presence of the superficial temporal artery (STA). Preoperative angiographic staging was performed based on Suzuki’s angiographic criteria [35]. All patients underwent a cerebral blood flow analysis using single-photon emission computed tomography (SPECT) studies with an acetazolamide (Diamox) challenge preoperatively.
Bypass surgery was indicated for (1) symptomatic patients, e.g., those with transient ischemic attack (TIA), cerebral ischemia, and hemorrhage; (2) patients with impaired cerebral blood flow (CBF) and cerebral reserve capacity on acetazolamide SPECT. In patients with conservative treatment, their neurological status was inadequate for bypass surgery because of major cerebral infarction or a large amount of hemorrhage. Some patients refused revascularization surgery because of their mild symptoms. We included those patients who were available for over 1 year of follow-up. We did not operate on asymptomatic patients with a normal hemodynamic study. Revascularization surgery was performed more than 1 month after the onset of initial hemorrhage or infarction. In patients with symptoms of transient ischemic attack (TIA), revascularization surgery was performed as soon as possible to prevent a secondary ischemic attack.
In this series, revascularization surgery for MMD was divided into three categories: direct bypass, indirect bypass, and combined bypass. Direct bypass procedures include only STA-MCA anastomosis [18]. If a suitable recipient artery could not be found during surgery, indirect surgery was performed instead of the STA-MCA bypass. We performed EDAGS, EDAMS, or EMS as indirect methods [10, 32]. Combined bypass surgery was performed by direct STA-MCA anastomosis, and EDAGS was performed using inverted STA-GF/GP [20].
Clinical and radiological data
Clinical and radiological data were reviewed for the following characteristics: demographics, surgical modalities, clinical outcome, recurrence of ischemic and hemorrhagic stroke after bypass, postoperative angiographic change, and cerebral blood flow (CBF) change by SPECT. Each patient’s clinical status was assessed pre- and postoperatively using the modified Rankin Disability Scale (mRDS) [39]. Recurrence of ischemic and hemorrhagic attack was confirmed using CT or MRI scanning. Postoperative angiographic change was evaluated according to the extent of revascularization and changes in moyamoya vessels observed on a postoperative angiogram obtained 6–12 months after surgery. The change of moyamoya vessels was determined if the number of moyamoya vessels decreased or did not change compared with the preoperative angiogram. We measured the revascularization area and area of MCA territory in the capillary phase of the lateral view in the external carotid angiogram (Fig. 1). We calculated the relative percentage of the revascularization area compared to the area of the MCA territory [4]. The revascularization area was measured on a PACS workstation (Marosis, Marotech, Korea) using its free-hand region of interest measurement tools. The postoperative angiographic change was categorized into good, moderate, and poor groups. If the extent of revascularization area supplied by the surgical bypass covered more than two thirds (66%) of the middle cerebral artery (MCA) distribution and the number of moyamoya vessels decreased, the change was classified as “good.” If the extent of the revascularization area covered between one third (33%) and two thirds (65%) of the MCA distribution and the number of moyamoya vessels decreased, the change was determined to be “moderate.” If the aforementioned criteria were not met or there were no changes, the angiographic change was determined to be “poor.” These data were calculated by a neurosurgical resident who was not involved in the surgery. We checked those areas twice and gained the mean to reduce the error.
Basal and acetazolamide-challenged brain perfusion SPECT was performed to evaluate CBF pre- and postoperatively. Routine postoperative evaluation with SPECT was accomplished 3–6 months after surgical treatment. The postoperative CBF was compared with the preoperative value. We classified SPECT results into three categories as follows: improved, unchanged, and worsened. Improved, unchanged, and worsened definitions are based on radiological readings. We also investigated the correlation between postoperative angiographic change and SPECT results.
Clinical outcomes were assessed by a neurosurgeon (T-G Lee), who did not participate in the bypass surgery, and radiological data were reviewed by a neuroradiologist who was unaware of the clinical results. All SPECT data were interpreted by a nuclear medicine doctor who was not involved in the surgery.
Statistical analysis
The incidence of hemorrhagic or ischemic events, demographic data, the angiographic revascularization at the operated sites, and the effect of revascularization surgery were analyzed using the chi-square test according to treatment modality. The change in clinical status (mRDS) was analyzed using the Wilcoxon signed-rank test according to treatment modality. Correlations between the angiographic change, postoperative SPECT results, and incidence of recurrence stroke were analyzed using linear-by-linear association. Stroke-free time from recurrent hemorrhagic and ischemic stroke were estimated using the Kaplan-Meier product-limit method. The log-rank test was applied to evaluate differences between two or more hemorrhage- and ischemia-free time curves. SPSS software (version 15.0, 2006; SPSS, Inc., Chicago, IL, USA) was used, and probability values < 0.05 were considered statistically significant.
Results
Among the 142 adult patients with MMD, 147 hemispheres of 124 adult MMD patients underwent revascularization surgery (103 hemispheres of 89 ischemic MMD patients, 44 hemispheres of 35 hemorrhagic MMD patients), and 18 patients were treated conservatively. Table 1 summarizes the general demographic features of the patients. Among the 18 patients with conservative treatment, 4 refused bypass surgery because of their mild neurological symptoms, and 6 patients refused bypass surgery for other reasons (such as financial problems, etc.). Eight patients could not undergo bypass surgery because of their poor neurological status. Of these patients, three underwent decompressive surgery. No significant differences were observed for age, gender, or length of follow-up period among patients when grouped according to treatment modalities in this series. Weakness was the most common symptom. A significant difference was observed in the initial RDS score between patients with ischemic and hemorrhagic MMD (P < 0.05). Six-vessel angiography was performed preoperatively in all patients, and the predominant angiographic finding was disease progression to stages III and IV. The follow-up duration ranged from 12 to 112 months (mean, 54.5 months). During the follow-up period, 23 (15.6%) of 147 hemispheres presented recurrent stroke (ischemic events, 14 patients; hemorrhagic events, 9 patients) after revascularization surgery. In 18 patients treated conservatively, 10 (55.6%) experienced recurrent stroke (ischemic events, 6 patients; hemorrhagic events, 4 patients). After the second ischemic and hemorrhagic events, 20 of 33 patients (60.6%) experienced worsening of their clinical symptoms. Poor prognosis was seen in patients with recurrent hemorrhagic events. Of the 13 patients who experienced recurrent intracranial hemorrhage, 5 (38.4%) died, 4 (30.8%) deteriorated to a persistent vegetative state, and 4 (30.8 %) were severely disabled.
Recurrent stroke events and final clinical status in patients with ischemic MMD
Follow-up periods ranged from 12 to 112 months (mean, 56.2 months). A total of 103 hemispheres of 89 patients were treated surgically, and 9 patients were treated conservatively. Fourteen patients had bilateral bypass surgeries, and 75 patients had unilateral bypass surgery. The incidence of recurrent stroke events for each treatment modality is presented in Table 2. Seventeen (16.5%) of 103 hemispheres had recurrent stroke events (ischemic events, 14 patients; hemorrhagic events, 3 patients) after revascularization surgery, whereas 6 of 9 patients (66.7%) who underwent conservative treatment presented with recurrent ischemic stroke. The incidence of recurrent stroke in patients who underwent direct and combined bypass surgery was significantly lower (P < 0.05, χ2-test) than that in patients treated with indirect bypass or conservative treatment. Kaplan-Meier plots demonstrated that patients who underwent revascularization surgery had significantly longer stroke-free times (P < 0.05) than patients who were treated conservatively (Fig. 2). Significant improvement in the RDS score was seen after surgery (P < 0.05, χ2-test), but no improvement was observed in patients who were treated conservatively. However, no significant difference was observed according to the bypass method.
Recurrent stoke events and final clinical status in patients with hemorrhagic MMD
Follow-up periods ranged from 12 to 105 months (mean, 55.4 months). A total of 44 hemispheres of 35 patients were surgically treated, and 9 patients were treated conservatively. Nine patients had bilateral bypass surgeries, and 26 patients had unilateral bypass surgery. The incidences of recurrent hemorrhagic events for each treatment modality are presented in Table 3. Six (15.9%) of 44 hemispheres had recurrent hemorrhagic events after revascularization surgery. In contrast, four (44.4%) of nine patients who were treated conservatively experienced recurrent hemorrhagic events. However, the incidence of recurrent hemorrhagic events in patients who underwent revascularization surgery tended to be lower than that in patients treated conservatively, but no significant difference was observed (P > 0.05 , χ2-test). No significant difference was found between the bypass methods. Kaplan-Meier plots demonstrated that patients who underwent revascularization surgery remained stroke-free longer than those treated conservatively (Table. 3). However, no statistical difference (P > 0.05) was observed between patients who underwent revascularization surgery and patients who were treated conservatively (Fig. 3). Significant improvement was observed in the RDS score after revascularization surgery (P < 0.05, χ2-test). No improvement was seen in patients with conservative treatment.
Angiographic changes and SPECT analysis
Postoperative angiograms were obtained for 138 hemispheres in 114 patients with revascularization surgery, and postoperative SPECT was done in 111 patients. Table 4 shows the results. Among the 138 hemispheres, good angiographic change was found in seven hemispheres (23.3%) with direct bypass, in eight (10.4%) with indirect bypass, and in nine (29%) with combined bypass. More significant angiographic changes were observed in patients who underwent direct and combined bypasses compared to those in patients who underwent indirect bypass (P < 0.05, χ2-test).
Correlation between the postoperative angiographic changes and stroke recurrence was investigated (Table 5). Statistical analysis between the angiographic change and recurrent ischemic events demonstrated significant statistical correlation (P-value = 0.036, linear-by-linear association). However, no statistical correlation was observed between the angiographic change and rebleeding (p-value = 0.426, linear-by-linear association).
We also investigated postoperative SPECT results and compared them with the angiographic changes. Table 6 shows the postoperative SPECT results. Statistical analysis between the angiographic changes and SPECT result demonstrated significant statistical correlation. This result shows that the angiographic changes are well correlated with CBF change (p-value = 0.001, linear-by-linear association).
Discussion
Moyamoya disease has been recognized as a devastating condition and has a specific pattern of age distribution in adults and children, with a higher incidence in childhood [34, 40]. The clinical symptoms of MMD relate directly to abnormal vasculature. The incidence of hemorrhage is reported to exceed 60% in adults, whereas it is only 10% in children [30]. The reason why intracranial hemorrhage frequently occurs in adult patients is unclear. The difference in the presenting symptoms between juvenile and adult patients may reflect the differences in cerebral hemodynamics and metabolism [15, 23, 28]. The clinical presentations of patients in this study were slightly different from those in other reports. In the present study, patients with ischemic symptoms were more predominant than those with hemorrhagic symptoms [ischemic symptoms, 98 patients (69%), hemorrhagic symptom, 44 patients (31%)]. It is true that hemorrhagic MMD is more predominant in adult patients compared to pediatric patients. However, in our study, ischemic MMD was more predominant than hemorrhagic MMD for several reasons. This study was limited to a single institution in Gyung-gi Province, and the number of cases was small and limited; thus, referral and selection bias could not be excluded. Additionally, with recent advances in neuroradiological diagnostic modalities, including MR angiography and three-dimensional CT angiography, the diagnosis of adult MMD has become more frequent, and these diagnostic tools are now used more easily in an outpatient setting than in the past. Furthermore, MMD is detected earlier before hemorrhagic attacks occur [3].
Regardless of whether patients initially experienced an ischemic attack or an intracranial hemorrhage, a secondary ischemic or hemorrhagic attack may have occurred during the follow-up period. Therefore, patients with MMD should be treated with the aim of preventing recurrent ischemic or hemorrhagic attacks. Although direct, indirect, or combined direct and indirect bypass has been utilized in patients with MMD, especially with ischemic MMD, it is unclear what the best treatment is for preventing recurrent hemorrhage or ischemic events in adult MMD patients [1, 13, 14, 28, 31]. Direct and combined bypasses provide an immediate increase of the blood supply to the ischemic brain compared to indirect bypass, and favorable results have been reported [10, 18, 20, 27]. However, direct bypass has some considerable drawbacks; it is difficult to find both good donor and recipient arteries of sufficient caliber in some patients with moyamoya disease, and some complications are related to direct bypass surgery, such as symptomatic hyperperfusion, cerebral infarction, intracerebral hemorrhage, or even death [7, 12, 16, 27, 38]. In contrast, indirect bypass is generally considered easier, safer, and less invasive than direct bypass, and is more feasible in patients with inadequate recipient or donor artery grafts [24, 25]. Although it has low rates of perioperative complications, formation of collateral vessels takes longer, and during this time, recurrent episodes of stroke attack can still be expected to develop [16, 38]. In our series, a total of 23 (15.6%) stroke cases occurred among 147 hemispheres after revascularization surgery. This was similar to other studies where the rates of recurrent stroke range from 5-31% [5, 27, 40]. In patients with ischemic MMD, the incidence of future stoke events in patients who underwent direct and combined bypass surgery was significantly lower than that in patients treated with indirect bypass or conservative treatment. Moreover, the stroke-free time of patients who underwent revascularization surgery was also longer than that of patients treated conservatively (P < 0.05). From these results, direct and combined bypasses appear to be effective to prevent recurrent stroke, especially ischemic events, because these bypasses provide immediate improvement of CBF as compared with indirect bypass, which can require several weeks to form collateral vessels [2, 10].
In hemorrhagic MMD, recurrent hemorrhagic events tended to be lower in patients who underwent revascularization surgery (15.9%) than in patients who were treated conservatively (44.4%), but no significant difference was observed. No statistical difference in hemorrhagic stroke recurrence was observed among surgical modalities. Even with a long-term follow-up of 13 years in this study, no correlation was observed between hemorrhagic stroke recurrence and surgical method. A major cause of this lack of correlation was that the area for investigation was limited to a single institution, which further narrowed the already limited number of cases. Also, sampling error may affect the results because the number of direct/combined bypasses was relatively small (11/10 cases) compared with indirect bypasses (23 cases). Another postulated cause was that even though direct and combined bypasses provide an immediate increase in the blood supply to the brain and favorable results have been reported [10, 18, 29], this direct anastomosis alone does not promote long-lasting filling of the MCA, which is presumably due to progression of the occlusive process with involvement of the recipient artery in MMD [2, 29]. These findings supported the results of our study, which did not show significant statistical differences among the three surgical procedures with respect to hemorrhagic stroke recurrence.
In this study, we investigated whether the extent of revascularization was influenced by the surgical modality. The extent of revascularization does not mean the whole hemodynamic status, but rather the degree of angiogenesis because the hemodynamic status was influenced by the collateral circulation. The results showed that the extent of revascularization was significantly greater in patients treated with direct and combined bypass surgery than in those treated with indirect revascularization surgery. The reason why indirect bypass was not as effective in adult cases is unclear. The extent of the postoperative collateral circulation seemed to be limited in indirect bypasses because the operative field was usually made along the course of the parietal branch of the STA compared with the combined bypass, which covered the widest surgical field for revascularization.
Some authors reported on the cerebral hemodynamics after bypass with SPECT and showed good correlation between clinical outcome and CBF/vasomotor reactivity [6, 27]. SPECT is considered to be very useful for visualizing not only the CBF, but also the cerebral vascular reservoir (CVR). However, the surgical effect does not always improve the CBF and CVR on the treated side [26]. In our study, the correlation between the angiographic changes and postoperative SPECT results was analyzed, and statistical significance was observed (P-value = 0.001, linear-by-linear association). These results may reflect the significant correlation between the decrease in the number of moyamoya vessels and a recovery of vascular reactivity via newly formed angiogenesis after bypass surgery. However, further study is needed to clarify this.
We were also curious about the correlation between the postoperative angiographic change and stroke recurrence. Although there was statistical correlation between the angiographic change and recurrent ischemic event, no statistical correlation was observed for hemorrhagic stroke recurrence. Kobayashi et al. reported that the second bleeding episode was frequently characterized by a change in hemisphere and the type of bleeding that occurred, as observed on CT scans [21]. This result suggests that recurrent hemorrhage does not result from a breakdown of a specific weak point, but from diffuse vulnerability of collateral vessels adjacent to the lateral ventricle, and unpredictability is thought to be one of the main reasons that the efficacy of bypass surgery has still not been clarified. Therefore, it seems too early to conclude that good angiographic change equates with a reduced number of recurrent hemorrhagic events.
There are some limitations to our study. First, it was not a prospective and controlled study. There may have been a potential bias in patient selection and demographics. Referral and selection bias cannot be excluded from this single-institution study. Secondly, we did not choose a constant period of time after the bypass surgery to analyze the angiographic and clinical outcomes. This made our results slightly difficult to compare with different treatment modalities. Additionally, there were no strict indications in which a bypass was performed in individual cases. In the initial years, our institution’s policy was to perform an indirect bypass for these patients. Currently, as more studies demonstrate the efficacy of direct and combined bypass and more surgical expertise is available, we try to perform direct or combined bypass on adult-onset MMD patients. Indirect bypass is performed only as a salvage surgical procedure if there is no proper recipient artery for a STA–MCA bypass.
Conclusion
The usefulness of direct and combined bypasses in patients with ischemic MMD for preventing recurrent stroke, especially ischemic events, was statistically confirmed in this study. However, there is still no clear evidence that revascularization surgery prevents rebleeding in patients with hemorrhagic MMD to a significant extent. We statistically confirmed that both direct and combined bypasses were much more effective for achieving a good extent of revascularization and decrease of moyamoya vessels than an indirect bypass. The extent of revascularization was well correlated with the CBF change of SPECT. Although statistical analysis between the extent of revascularization and ischemic stroke recurrence demonstrated significant statistical correlation, no statistical correlation was observed in hemorrhagic stroke recurrence. Therefore, it seems too early to conclude that good revascularization equates with a reduced number of recurrences of hemorrhagic events. A long-term prospective study of a large number of patients with hemorrhagic moyamoya disease is required to determine whether bypass surgery prevents rebleeding.
Reference
Aoki N (1993) Cerebrovascular bypass surgery for the treatment of moyamoya disease: unsatisfactory outcome in the patients presenting with intracranial hemorrhage. Surg Neurol 40:372–377
Asfora WT, West M, McClarty B (1993) Angiography of encephalomyosynangiosis and superficial temporal artery to middle cerebral artery anastomosis in Moyamoya disease. Am J Neuroradiol 14:29–30
Baba T, Houkin K, Kuroda S (2008) Novel epidemiological features of moyamoya disease. J Neurol Neurosurg Psychiatry 79:900–904
Bang JS, Kwon OK, Kim JE, Kang HS, Park H, Cho SY, Oh CW (2011) Quantitative angiographic comparison with OSIRIS program between the direct and indirect revascularization modalities in adult moyamoya disease. Neurosurgery [Epub ahead of print] 19
Dusick JR, Gonzalez NR, Martin NA (2011) Clinical and angiographic outcomes from indirect revascularization surgery for Moyamoya disease in adults and children: a review of 63 procedures. Neurosurgery 68:34–43
Fujimura M, Kaneta T, Tominaga T (2008) Efficacy of superficial temporal artery-middle cerebral artery anastomosis with routine postoperative cerebral blood flow measurement during the acute stage in childhood moyamoya disease. Childs Nerv Syst 24:827–832
Fujimura M, Mugikura S, Kaneta T, Shimizu H, Tominaga T (2009) Incidence and risk factors for symptomatic cerebral hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in patients with moyamoya disease. Surg Neurol 71:442–447
Fujiwara F, Yamada H, Hayashi S, Tamaki N (1997) A case of adult moyamoya disease showing fulminant clinical course associated with progression from unilateral to bilateral involvement. No Shinkei Geka 25:79–84
Fukui M (1997) Guidelines for the diagnosis and treatment of spontaneous occlusion of the circle of Willis (‘Moyamoya’ disease). Clin Neurol Neurosurg 99:S238–S240
Golby AJ, Marks MP, Thompson RC, Steinberg GK (1999) Direct and combined revascularization in pediatric moyamoya disease. Neurosurgery 45:50–58
Han D, Nam DH, Oh CW (1997) Moyamoya disease in adult: characteristics of clinical presentation and outcome after encephalo-duroarterio-synangiosis. Clin Neurol Neurosurg 99:S151–S155
Hayashi T, Shiran R, Fujimura M, Tominaga T (2010) Postoperative neurological deterioration in pediatric moyamoya disease: watershed shift and hyperperfusion. J Neurosurg Pediatrics 6:73–81
Houkin K, Kamiyama H, Abe H, Takahashi A, Kuroda S (1996) Surgical therapy for adult moyamoya disease. Can surgical revascularization prevent the recurrence of intracerebral hemorrhage? Stroke 27:1342–1346
Ikezaki K, Fukui M, Inamura T, Kinukawa N, Wakai K, Ono Y (1997) The current status of the treatment for hemorrhagic moyamoya disease based on a 1995 nationwide survey in Japan. Clin Neurol Neurosurg 99:S183–S186
Ikezaki K, Matsushima T, Kuwabara Y, Suzuki SO, Nomura T, Fukui M (1994) Cerebral circulation and oxygen metabolism in childhood moyamoya disease: a perioperative positron emission tomography study. J Neurosurg 81:843–850
Ishikawa T, Houkin K, Kamiyama H, Abe H (1997) Effects of surgical revascularization on outcome of patients with pediatric moyamoya disease. Stroke 28:1170–1173
Kagawa R, Okada Y, Moritake K, Takamura M (2004) Magnetic resonance angiography demonstrating adult moyamoya disease progressing from unilateral to bilateral involvement– case report. Neurol Med Chir (Tokyo) 44:183–186
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
Kim DS, Yoo DS, Huh PW, Kang SG, Cho KS, Kim MC (2006) Combined direct anastomosis and encephaloduroarteriogaleosynangiosis using inverted superficial temporal artery-galeal flap and superficial temporal artery-galeal pedicle in adult moyamoya disease. Surg Neurol 66:389–394
Kobayashi E, Saeki N, Oishi H, Hirai S, Yamaura A (2000) Long term natural history of hemorrhagic moyamoya disease in 42 patients. J Neurosurg 93:976–980
Kuroda S, Ishikawa T, Houkin K, Nanba R, Hokari M, Iwasaki Y (2005) Incidence and clinical features of disease progression in adult moyamoya disease. Stroke 36:2148–2153
Kuwabara Y, Ichiya Y, Otsuka M, Tahara T, Gunasekera R, Hasuo K, Masuda K, Matsushima T, Fukui M (1990) Cerebral hemodynamic change in the child and the adult with moyamoya disease. Stroke 21:272–277
Matsushima T, Fujiwara S, Nagata S, Fujii K, Fukui M, Kitamura K, Hasuo K (1989) Surgical treatment for paediatric patients with moyamoya disease by indirect revascularization procedures (EDAS, EMS, EMAS). Acta Neurochir (Wien) 98:135–140
Matsushima T, Inoue T, Suzuki SO, Fujii K, Fukui M, Hasuo K (1992) Surgical treatment of moyamoya disease in pediatric patients–comparison between the results of indirect and direct revascularization procedures. Neurosurgery 31:401–405
McAuley DJ, Poskitt K, Steinbok P (2004) Predicting stroke risk in pediatric moyamoya disease with xenon-enhanced computed tomography. Neurosurgery 55:327–333
Mesiwala AH, Sviri G, Fatemi N, Britz GW, Newell DW (2008) Long-term outcome of superficial temporal artery-middle cerebral artery bypass for patients with moyamoya disease in the US. Neurosurg Focus 24:E15
Morimoto M, Iwama T, Hashimoto N, Kojima A, Hayashida K (1999) Efficacy of direct revascularization in adult moyamoya disease: haemodynamic evaluation by positron emission tomography. Acta Neurochir (Wien) 141:377–384
Nakagawa Y, Abe H, Sawamura Y, Kamiyama H, Gotoh S, Kashiwaba T (1988) Revascularization surgery for Moyamoya disease. Neurol Res 10:32–39
Nishimoto A (1979) Moyamoya disease. Neurol Med Chir 19:221–228
Okada Y, Shima T, Nishida M, Yamane K, Yamada T, Yamanaka C (1998) Effectiveness of superficial temporal artery-middle cerebral artery anastomosis in adult moyamoya disease: Cerebral hemodynamics and clinical course in ischemic and hemorrhagic varieties. Stroke 29:625–630
Patel NN, Mangano FT, Klimo P Jr (2010) Indirect revascularization techniques for treating moyamoya disease. Neurosurg Clin N Am 21:553–563
Shirane R, Mikawa S, Ebina T (1999) A case of adult moyamoya disease showing progressive angiopathy on cerebral angiography. Clin Neurol Neurosurg 101:210–214
Suzuki J, Kodama N (1983) Moyamoya disease—a review. Stroke 14:104–109
Suzuki J, Takaku A (1969) Cerebrovascular “moyamoya” disease: Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288–299
Takeuchi K, Shimuzu K (1957) Hypogenesis of bilateral internal carotid arteries. No To Shinkei 9:37–43
Tomida M, Muraki M, Yamasaki K (2000) Angiographically verified progression of moyamoya disease in an adult. Case report J Neurosurg 93:1055–1057
Ueki K, Meyer FB, Mellinger JF (1994) Moyamoya disease: the disorder and surgical treatment. Mayo Clin Proc 69:749–757
UK-TIA study group (1988) The UK-TIA Aspirin Trial: Interim results. Brit Med J 296:316–320
Yoshida Y, Yoshimoto T, Shirane R, Sakurai Y (1999) 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 30:2272–2276
Conflict of interest
None.
Author information
Authors and Affiliations
Corresponding author
Additional information
Comment
This is a valuable contribution to the literature in that the study provides high-quality, rigorous follow-up of a large patient sample. It provides potentially important data to guide the choice of bypass (direct/combined vs. indirect). This is achieved by correlating the treatment with an evaluation of the clinical and imaging outcomes, and provides comparative evidence as to the clinical value of direct/combined, indirect, and conservative management. A caveat remains that this is a retrospective study in which the treatments were not randomly allocated. Nonetheless, it is of significant interest to those who treat patients with adult moyamoya disease.
Michael Tymianski
Toronto, Canada
Rights and permissions
About this article
Cite this article
Lee, SB., Kim, DS., Huh, PW. et al. Long-term follow-up results in 142 adult patients with moyamoya disease according to management modality. Acta Neurochir 154, 1179–1187 (2012). https://doi.org/10.1007/s00701-012-1325-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00701-012-1325-1