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Table of Contents    
Year : 2021  |  Volume : 69  |  Issue : 3  |  Page : 620-627

Outcome Following Surgical Revascularization in Patients of Moyamoya Disease with Focus on Graft Patency and Angiographic Changes

1 Department of Neurosurgery, Postgraduate Institute of Medical Education and Research, Chandigarh, India
2 Department of Radiodiagnosis, Postgraduate Institute of Medical Education and Research, Chandigarh, India

Date of Submission16-May-2020
Date of Decision17-Jul-2020
Date of Acceptance15-Dec-2020
Date of Web Publication24-Jun-2021

Correspondence Address:
Dr. Sunil K Gupta
Department of Neurosurgery, Postgraduate Institute of Medical Education and Research, Chandigarh - 160 012
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0028-3886.319228

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 » Abstract 

Background: Surgical revascularization is the mainstay of treatment in symptomatic patients of moyamoya disease (MMD).
Objective: The present study analyzed the postoperative angio-architecture in pediatric and adult patients of moyamoya disease.
Material and Methods: Patients with MMD, both ischemic and hemorrhagic, were subjected to surgery. A superficial temporal artery-middle cerebral artery (STA-MCA) anastomosis was attempted in all. It was augmented by an encephalo-duro-myo-synangiosis), this was labelled as the combined surgical group. In patients where a direct bypass was not possible encephalo-duro-arterio-myo-synangiosis (EDAMS) was performed and these patients were put in the indirect surgery group. In the postoperative period, MRA was performed in all patients to look for (a) graft patency, (b) regression of moyamoya vessels, and (c) degree of surgical neovascularization (as quantified on adapted Matsushima and Inaba grading system).
Results: Eighty-two patients underwent 131 surgical revascularization procedures. A combined surgery (STA-MCA bypass and EDAMS) was performed in 100 hemispheres and indirect surgery (EDAMS) on 31 sides. In children less than 5 years of age, STA-MCA anastomosis was possible in more than 50% of patients. Clinical improvement was seen in 85.4% of patients. Postoperative MRA demonstrated a patent bypass graft in 97% of cases. Regression of moyamoya vessels was seen in half of the cases and good surgical revascularization (type A and B) was seen in more than 80% of hemispheres in the combined surgery and indirect surgery group.
Conclusions: Revascularization procedures led to a regression of moyamoya collaterals, appearance of surgical neo angiogenesis, and a graft patency rate of 97%. Surgical group with combined revascularization had a trend towards better collateral development.

Keywords: Angiographic changes, moyamoya disease, STA-MCA bypass
Key Message: STA-MCA bypass with EDAMS should be the procedure of choice in patients of MMD.

How to cite this article:
Gupta SK, Narayanan R, Aggarwal A, Mohanty M, Ahuja C, Verma N, Praneeth K, Agarwal V. Outcome Following Surgical Revascularization in Patients of Moyamoya Disease with Focus on Graft Patency and Angiographic Changes. Neurol India 2021;69:620-7

How to cite this URL:
Gupta SK, Narayanan R, Aggarwal A, Mohanty M, Ahuja C, Verma N, Praneeth K, Agarwal V. Outcome Following Surgical Revascularization in Patients of Moyamoya Disease with Focus on Graft Patency and Angiographic Changes. Neurol India [serial online] 2021 [cited 2022 Dec 3];69:620-7. Available from: https://www.neurologyindia.com/text.asp?2021/69/3/620/319228

Moyamoya disease (MMD) is characterized by progressive stenosis or occlusion of the intracranial supraclinoid carotid arteries and/or the proximal segments of the anterior and middle cerebral arteries. This is accompanied by development of an abnormal vascular network: “moyamoya” to compensate for the insufficient cerebral perfusion.[1],[2] Insufficient blood flow leads to clinical events secondary to ischemia especially in the pediatric age group. In adults, the more common presentation is hemorrhage from the fragile collateral vessels or associated micro aneurysms.

Most of the available literature supports the beneficial effects of revascularization strategies in both pediatric and adult age group. Revascularization strategies aim at improving the cerebral blood flow and in addition, leading to a faster regression of moyamoya vessels. Current literature has shown reduction or disappearance of ischemic events after revascularization procedures as well as reduction in the frequency of hemorrhagic episodes.[3],[4],[5],[6],[7],[8],[9],[10],[11],[12],[13],[14],[15],[16]

The revascularization strategies include direct superficial temporal artery-middle cerebral artery (STA-MCA) anastomosis, indirect surgeries in form of encaphalo-duro-arterio-synangiosis (EDAS), encaphalo-duro-myo-synangiosis (EDMS) or EDAMS (encaphalo-duro-arterio-myo-synangiosis) or combined direct and indirect surgical procedures. Many surgeons practice direct or combined surgery in older children and adults but only indirect procedures in smaller children due to small caliber of donor and recipient vessels.[1],[8],[11]

In the present study, a combined direct and indirect revascularization was attempted in all patients of MMD, regardless of age. In cases where a direct anastomosis was not possible, only indirect procedure was performed. Follow-up angiographic studies were performed to assess the angio-architecture after surgery, vis-à -vis, graft (STA-MCA) patency, degree of cerebral cortical revascularization, n and regression of moyamoya vessels. These angiographic changes were correlated with clinical parameters.

 » Materials and Methods Top

The study was conducted in a tertiary care teaching hospital and MMD patients of all age groups, and both genders who underwent revascularization surgery were included. In the preoperative period, all patients underwent evaluation on these three parameters: clinical, neuropsychological, and radiological. In the postoperative period, the same parameters were evaluated again, after a minimum of 3 months and the results were compared.

Clinical evaluation included patient symptomatology—paresis, seizures, etc., Disability was graded as per modified Rankin score (mRS).

In children below 5 years of age, Vineland Social Maturity Scale was used for cognition and information about Social quotient was collected after detailed interaction with parents by a trained neuropsychologist. For older children, Malin's Intelligence Scale for Children was used.

Radiological evaluation included MRI brain and MRA of intracranial vessels in every case. We avoided invasive catheter angiogram, especially in children. In a few cases of doubtful diagnosis in adult patients, DSA was done. The management was done as per department protocol including preoperative aspirin and antiepileptics.

Radiological assessment

  1. Parenchymal changes, viz., infarct, hemorrhage, encephalomalacia, gliosis, etc.
  2. The degree of stenosis of internal carotid artery (ICA), ACA, and MCA was determined and graded as normal, stenosed, or occluded and given score of 1, 2, and 3, respectively.
  3. The moyamoya vessels were assessed on pre-op MR angiograms and were graded as mild, moderate, or extensive vessels and scored as 1, 2, and 3, respectively.
  4. Suzuki stage[17] of the disease in each hemisphere.

Direct revascularization surgery (STA-MCA bypass) was attempted in every case. This was augmented by EDAMS. In cases where direct anastomosis was not feasible because of small caliber of donor/recipient vessel, an indirect revascularization (EDAMS) was done. Therefore for comparison, there were two surgical groups: combined and indirect revascularization.

Details of surgery: STA was palpated, marked, and harvested. Temporalis muscle and fascia were incised in a cruciate manner, and a plane of dissection was created between temporalis fascia and muscle. After lifting the muscle, a frontotemporal craniotomy was done. Dura was opened in a cruciate manner. The inferior two leaves of the dura were excised. A cortical branch of MCA on brain surface was selected for anastomosis. This was cleared off the arachnoid, and all the side branches were coagulated and cut to have about 1 cm of the vessel free for anastomosis. Two temporary clips were applied on this MCA segment, and an “end to side” STA-MCA anastomosis was done using 10-0 nonabsorbable nylon interrupted sutures. This was augmented by EDAMS. In cases where direct anastomosis was not feasible because of small caliber of donor/recipient vessel, the harvested STA along with the fascia was placed on the cortical surface after liberal opening of the arachnoid in addition to the EDAMS.

Postoperative assessment

Three months after surgery, clinical and radiological assessment was repeated. Vascular changes were evaluated on MR angiography.

On MRA, the following three parameters were evaluated:

  1. The status of graft patency,
  2. The extent of moyamoya vessels as compared to those in preoperative period, and
  3. The extent of surgical transdural collaterals at the synangiosis site.

For evaluating surgical collaterals, we extrapolated the Matsushima and Inaba grading (originally described on DSA) on the MRA appearance.

Grade A and B signified presence of arterial branches in > 2/3 and 1/3–2/3 of the MCA territory, respectively, which was visualized as flow related linear channels on TOF MRA. Grade C represented TOF signal in less than 1/3 MCA territory.

Though subjective, this evaluation was performed by consensus opinion of qualified neuroradiologists. In the present study, we have labeled it as adapted Matsushima and Inaba grading.

The angio-architectural findings were correlated with age, type of surgery, and clinical outcome.

Statistical analysis

All data was analyzed using SPSS 26 (Statistical Package for the Social Sciences Software, IBM). Mean, median, and percentages of demographic details, symptoms, clinical findings, radiological parameters, and outcome parameters. Comparison of MMV collaterals pre- and postprocedure across the treatment groups was done using one sample Chi-Square test and Pearson Chi-Square test, where applicable, with a confidence interval of 95%. Two-sided was considered if P < 0.05.

 » Results Top

Out of 82 patients of MMD, 49 underwent surgery bilaterally and 33 unilaterally making a total of 131 cerebral hemispheres.

The age of the patients ranged from 1 to 52 years (mean = 14 and median = 11 years). There were 64 patients (78%) in the pediatric age group (age less than 18 years) and 18 were adults. In the pediatric age group, 21 (26%) patients were less than 5 years of age.

For the combined surgical group, the age range was from 3 to 52 years with a mean of 14.3 years. For the indirect group, the age range was from 1 to 47 years with a mean age of 11 years. There were 45 (54.9%) male and 37 (45.1%) female patients.

Clinical presentation and imaging

Majority of the patients presented with ischemia; the most common clinical presentation was paresis in 67 patients (81.7%), seizures in 46 (56%), Transient ischemic attack (TIA) in 20 (24.3%), and aphasia in 12 patients (14.6%). Besides these, we also encountered less common symptoms like decreased vision (7.3%), delayed milestones (2.4%), decreased scholastic performance (2.4%), memory disturbances (2), and chorea (1.2%). Adults presented with headaches and hemorrhage. Seven adult patients (47%) had hemorrhage, and out of them, two (11.11%) had features suggestive of raised intracranial pressure [Table 1]. Seventy patients (85.36%) had a mRS score of either 3 or 4. Nine patients had score of 2, while three patients had a score of 1.
Table 1: Clinical features at presentation

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Infarcts in brain were identified in MRI in 67 patients, hemorrhage in seven and atrophy/encephalomalacia in eight patients. All seven patients of hemorrhage were adults. ICA was involved in all hemispheres. The degree of involvement of ICA was further categorized as normal (none), mild stenosis (8 sides), severe stenosis (39 sides), and total occlusion (84 sides). The extent of moyamoya vessels was categorized as mild (17 sides), moderate (45 sides), and extensive collaterals (69 sides).

The disease was then staged as per the Suzuki staging system. There were 61 patients (46.6%) in stage 5 at presentation, 31 patients were in stage 3, while 29 were in stage 4.

Surgical procedures

Forty-nine patients were operated on both sides and 33 were operated on one side, thus making a total of 131 hemispheres.

STA-MCA bypass was done in 99 hemispheres, and MMA-MCA bypass in one patient. The direct revascularization was augmented by EDMS in all 100 patients. EDAMS only, as revascularization strategy, was done in 31 hemispheres, as in these, adequate donor/recipient vessel was not available.

Post-operative assessment

Clinical outcome

Seventy patients (85.4%) had symptomatic improvement. This was seen as improvement of paresis, reduction in seizure frequency, and cessation of further attacks of TIA. In pediatric patients especially, there was improvement in cognition, attention span, and speech. Two patients (2.4%) reported worsening of clinical status and 10 patients (12.2%) had same clinical status as in pre op period.

Sixty-seven patients (81.7%) showed improvement in mRS scores, while two patients (2.4%) had deterioration. No change was seen in 13 patients (15.85%).

Clinical outcome was was observed in three different age groups—less than 5 years, 6–18 years and more than 18 years. In these age groups, 72.7, 88.09, and 94.4% improved after surgery, respectively. However, this difference was statistically not significant. In total, 86.56% patients showed clinical improvement after surgery in ischemic group, while this number was 85.71% in hemorrhagic group.

Clinical improvement was seen in 85/100 (85%) patients in combined surgical group and 24/31 patients (77.4%) in indirect surgical group.

There was no statistically significant difference in clinical outcome with respect to age, mode of presentation or type of surgery (combined vs. indirect) (P = 0.193) [Table 2].
Table 2: Clinical outcome in combined and indirect revascularization group

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Seven patients (7.3%) developed postoperative complications. Six patients had post-op wound dehiscence, and one patient had post-op meningitis. There was no mortality.

Postoperative MRA [Figure 1], [Figure 2], [Figure 3], [Figure 4]

Three parameters were analyzed: A) patency of the STA-MCA anastomosis, B) the degree of regression of the moyamoya collaterals at the base of the brain, and C) the extent of vascular neo-angiogenesis in the operated hemisphere. [Figure 1], [Figure 2], [Figure 3], [Figure 4].
Figure 1: Combined anastomosis. (a) Pre op MRA images showing bilateral ICA stenosis with extensive skull base moyamoya vessels. (b) post op MRA showing bilateral patent bypass. Regression of moyamoya vessels is seen bilaterally. Neo synangiosis is type A on the right side and Type B on the left side. (c) Pre op MRA of another patient showing severe stenosis of bilateral ICA with extensive basal collaterals. (d) Post op MRA after the left-sided surgery showing patent STA MCA bypass graft with regression of moyamoya collaterals and appearance of Grade B surgical synangangiotic vessels

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Figure 2: (a) Combined anastomosis. Pre op DSA in a 45/F showing the right ICA stenosis and moyamoya vessels. (b) Post op DSA showing patent bypass and Type A surgical synangiogenesis

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Figure 3: Combined anastomosis. (a) 6-year female pre op MRA showing bilateral ICA stenosis with extensive moyamoya vessels, more on the left side. (b) Post op MRA after left sided surgery shows patent bypass; Type B surgical synangiotic vessels and extensive regression of moyamoya vessels (c) Pre op MRA in a 4-year male (d) Post op MRA after surgery on the left side showing patent bypass; Type B surgical synangiotic vessels and regression of moyamoya vessels

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Figure 4: Indirect anastomosis. (a) Pre op MRA showing predominantly right-sided disease. (b) EDMS alone was done on the right side. Post op MRA showing Type C surgical synangangiotic vessels

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A): In 100 hemispheres where direct revascularization plus EDAMS was done, a patent STA-MCA graft was seen in 97 hemispheres. Graft patency could not be seen in three hemispheres and 31 patients underwent only EDAMS. Therefore, 34 hemispheres had effectively only indirect revascularization.

In children less than five years of age, direct bypass was surgically feasible in 20 hemispheres, and out of these, 18 (90%) showed a patent graft on postoperative MRA.

In older children and adults, the graft patency rate was 100 and 96.3%, respectively, when a direct anastomosis was successful. [Table 3].
Table 3: No of hemispheres with patent bypass in different age groups

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B): The extent of moyamoya collaterals at skull base in the post op period was evaluated

In the combined surgical group (a patent bypass along with EDAMS), 51 patients (52.5%) showed radiological improvement in the form of regression of moyamoya collaterals. In patients who underwent indirect revascularization as the only procedure, 17 patients (50%) had regression of moyamoya collaterals with the rest 50% being same with no radiological deterioration.

The number of patients showing regression was significant in both the groups as compared to pre-operative images (P < 0.05), but intergroup analysis did not reveal superiority of one procedure over another [Table 4].
Table 4: Extent of moyamoya collaterals in cases of combined and indirect revascularization

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C): The extent of formation of transdural and leptomeningeal collaterals at the synangiosis site due to surgical intervention was graded according to the adapted Mitsushima and Inaba system.

In the combined revascularization group, the extent of surgical neoangiogenesis was type A in 48.5% patients and type B in 33% hemispheres. There was a significant trend towards type A neoangiogenesis in combined revascularization group (P = 0.001) [Table 5].
Table 5: Adapted Matsushima and Inaba grading system in combined and indirect revascularization group

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In the indirect group, Type A surgical neo-angiogenesis was present in 35.29%, while 47% of hemispheres had a Type B neo-angiogenesis [Table 5]. Intergroup comparison between combined and indirect revascularization showed no significance (P = 0.18).

 » Discussion Top

This study was conducted on 82 operated patients of MMD involving 131 hemispheres. A direct revascularization procedure, STA-MCA bypass, was attempted in each patient. This was augmented by indirect revascularization (EDAMS) in all cases undergoing direct surgery. In cases where direct anastomosis was not feasible because of small caliber of donor/recipient vessel, only EDAMS was done.

Evidence for surgical treatment of MMD

The management of patients with MMD is directed towards reducing the incidence of repeated strokes due to ischemia as well as preventing rebleeding in patients presenting with hemorrhage. Medical therapy has been tried in some cases but its efficacy remains doubtful.[18] There is no convincing evidence that drug therapy is able to delay or reverse the progression of MMD.[18],[19] A 10-year follow-up evaluation from the Registry study of Research Committee in Japan stated that antiplatelets did not influence the rate of cerebral infarction in patients with MMD.[20]

In last two decades, sufficient evidence has accumulated to support the beneficial effects of revascularization surgeries in patients with MMD. The Japanese stroke guidelines recommended that revascularization surgery should be performed for patients with ischemic MMD.[21] In a meta-analysis including 961 from eight studies, surgical treatment of MMD showed significant efficacy in recurrent stroke prevention. There has been a lot of debate on the ideal treatment for hemorrhagic MMD and the surgical management of hemorrhagic MMD has been considered controversial in the past.[22],[23] However, the results of a multicentered, prospective randomized controlled trial in Japan revealed that a direct bypass could prevent rebleeding.[15] In a topical review in Stroke, it was categorically stated that revascularization surgery is the most effective treatment for hemorrhagic MMD as demonstrated by an RCT and most likely the most effective treatment for ischemic MMD.[3]

Therefore, the widely accepted view at present is that patients with either ischemic or hemorrhagic MMD should receive surgical treatment.

At our institute, we have consistently followed the practice of surgical revascularization in all symptomatic patients of MMD.

Comparative analysis of direct, indirect, and combined revascularization treatment for procedures

The ideal surgical treatment for MMD is still not established.

There are conflicting reports on the relative efficacy of different surgical strategies. Many authors have suggested that a combined approach including a direct vascular bypass (STA-MCA or other) and an indirect vascular synangiosis (EDMS, EDAS, EDAMS) offers the benefit of an immediate augmentation of cerebral blood flow supplemented by long-term potentiation by development of collaterals from the patchwork of muscle, dura, or fascia graft.[24],[25] Zhao et al.[26] in their publication proposed that direct procedures provide almost immediate augmentation of cerebral perfusion, whereas indirect procedures lead to gradual but more sustained revascularization in the long term with a complementary association between the direct and indirect revascularization procedures.

In recent years, reports demonstrated the superiority of combined surgery over either direct or indirect surgery alone.[27],[28],[29],[30],[31] A randomized controlled trial comparing hemodynamic outcome of indirect vs combined revascularization concluded that only combined revascularization improved cerebrovascular reserve capacity.[28] At the same time, there are reports that a direct bypass alone works equally well.[3],[6] However, in a literature search involving 33 studies and having data of 4197 patients – both adult and pediatric patients- the authors concluded direct bypass to be inferior to indirect/combined revascularization.[32]

Direct surgery requires the availability of adequate sized donor and recipient vessels. We were successful in a direct bypass in 100 out of 131 hemispheres (76.3%). In 18 of these, the patients' age was less than 5 years. Bot et al.[31] reported that STA-MCA bypass was feasible in patients 3 years or younger. The perioperative complication rate was low and similar in both combined and indirect groups, in our series, as well as others.[2],[33],[34]

Patients undergoing direct vascular bypass may suffer neurological deterioration due to cerebral hyperperfusion syndrome.[6],[35],[36],[37] We did not encounter this phenomenon, at least clinically, in any of patients, possibly because we did not perform surgery during an acute event. Clinical improvement was seen in more than 85% patients. Age, type of presentation (ischemic/hemorrhagic), or type of surgery did not have any significant impact on the outcome. A successful patent bypass was achieved in more than 50% of children less than 5 years of age.

Angiographic changes

The clinical outcome following surgery for MMD is a function of the angio-architectural changes. Reduction in ischemic events is dependent on the degree of augmentation of the cerebral circulation by direct anastomosis and/or development of collateral network of vessels following onlay of temporalis muscle, dura, or arterial graft. Equally important is the regression of moyamoya vessels. These vessels are prone to bleed because of their weak wall and associated micro aneurysms.

The graft patency rate of 97% in our series is consistent with the graft patency rate mentioned in the recent literature.[4],[27] Cho et al.[27] in their study observed that the patency of the direct STA-MCA anastomosis was 96.1% at the immediate assessment, 94.4% in the short term (at 6 months follow up), and 76.1% in the long term (at 5 years follow up).

Regression of moyamoya vessels was seen in about 50% of cases in both the surgical groups, suggesting the type of surgical procedure had no effect on determining the degree of attenuation of the abnormal vasculature at the skull base. A 51.2% regression rate of moyamoya vessels was reported by Jiang et al.,[38] in their series of 105 adult patients of hemorrhagic MMD in which all patients underwent STA-MCA bypass combined with EDMS.

The degree of vascular neoangiogenesis is generally measured by the grading system proposed by Matsushima and Inaba.[19] Different rates of good/poor revascularization have been reported by various authors. Good grade revascularization (adapted Matsushima and Inaba A and B) was observed in 85.3%, and poor (grade C) revascularization was observed in 14.7%. Jiang et al.[38] also noted good collaterals (grades A and B) and poor collaterals (grade C) in 85.3 and 14.7% patients, respectively. Bao et al.[4] followed up the postoperative angiograms of 109 adult patient hemispheres who underwent EDAS and found that 45% had grade A collateral circulation, 34% grade B, and 21% grade C collateral circulation.

Zhang et al.,[39] in 100 pediatric patients observed excellent, good, and fair neovascularization in 57.02, 22.81, and 17.54% hemispheres, respectively, whereas 2.63% hemispheres showed no neovascularization at all.

A multivariate analysis in hemorrhagic MMD[26] demonstrated that bypass patency graft and dural neoangiogenesis both independently contributed to good angiographic outcome. Typically, 64.5% hemispheres had satisfactory revascularization and 36.6% had poor neoangiogenesis. No significant difference was found regarding graft patency and decrease of moyamoya vessels in different surgical groups. Arias et al.[40] in their retrospective review of adult MMD found that the direct bypass group (either alone or along with an indirect procedure) had a significantly higher number of patients (90%) with a good angiographic outcome when compared to the indirect group (30%). In another study similar to ours, authors concluded that patients undergoing combined revascularization had better clinical status compared to those who had only indirect revascularization.[41]

Good development of collaterals (grade A and B) was seen in more than 80% hemispheres in both the surgical groups—combined revascularization and only indirect revascularization. Although the proportion of patients with grade A collaterals was more in the combined surgery group, it was not statistically significant.

 » Conclusions Top

Revascularization procedures (combined and indirect) led to a regression of moyamoya collaterals, appearance of surgical neo angiogenesis, and a graft patency rate of 97%. This has a dual benefit of improving cerebral perfusion and decreasing the chances of later hemorrhage. Vast majority of patients improved clinically after revascularization. The surgical group with combined revascularization had a trend towards better collateral development. Combined surgery offers the benefit of immediate as well as sustained augmentation of cerebral blood flow and should be the procedure of choice in all patients of MMD. Technically, direct anastomosis was possible even in small calibre vessels and could be achieved in more than 50% cases in children less than 5 years of age.

The degree of cerebral revascularization was statistically same in both the combined surgery group and the indirect surgery group, although there was a trend towards better collaterals in the combined group.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

 » References Top

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Acker G, Fekonja L, Vajkoczy P. Surgical management of moyamoya disease. Stroke 2018;49:476-82.  Back to cited text no. 3
Bao XY, Zhang Y, Wang QN, Zhang Q, Wang H, Zhang ZS, et al. Longterm outcomes after encephaloduroarteriosynangiosis in adult patients with moyamoya disease presenting with ischemia. World Neurosurg 2018;115:e482-9.  Back to cited text no. 4
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  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]

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