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Table of Contents    
Year : 2021  |  Volume : 69  |  Issue : 5  |  Page : 1259-1264

Surgical Outcome of Encephaloduroarteriomyosynangiosis for Moyamoya Disease

1 Department of Neurosurgery, MS Ramaiah Medical College and Hospital, Bengaluru, Karnataka, India
2 Department of Neurology, MS Ramaiah Medical College and Hospital, Bengaluru, Karnataka, India
3 Department of Neurosurgery, Sri Sathya Sai Insitute of Higher Medical Sciences, Bengaluru, Karnataka, India

Date of Submission29-Jan-2021
Date of Acceptance06-Jul-2021
Date of Web Publication30-Oct-2021

Correspondence Address:
Sunil V Furtado
Department of Neurosurgery, MS Ramaiah Medical College and Hospital, Bengaluru - 560 054, Karnataka
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0028-3886.329538

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 » Abstract 

Objective: Indirect bypass surgeries for moyamoya disease have included modifications of procedures involving placement of the superficial temporal artery on the brain pial surface. We evaluate the functional and angiographic outcomes of patients treated with encephaloduroarteriomyosynangiosis (indirect) revascularization and examine the outcome in relation to demographic and radiological factors.
Materials and Methods: Patients treated surgically for moyamoya disease over a 14-year period were identified. Demographics, clinical presentation, and radiology were analyzed to assign a stage for the disease (Suzuki staging) and the extent of revascularization (Matsushima grade) at the last follow-up. A modified Rankin score was used to assess the clinical status at presentation and the functional outcome at follow-up.
Results: There were 46 patients operated on by a single surgeon over a 14-year period. A higher incidence of motor deficits, seizures, and speech deficits was seen in the pediatric population. Age, sex, preoperative Suzuki disease stage, and hemispheric involvement had no bearing on angiographic outcome at last follow-up. Three of 46 patients (6.5%) developed immediate postoperative complications. Among 43 patients on follow-up, 39 had stable disease or showed improvement in clinical symptoms with 90% event-free status at last follow-up.
Conclusions: Indirect revascularization procedures are an effective alternative to direct cerebral revascularizations in the early or advanced stages of moyamoya disease. This is effective in a predominant ischemic presentation as noted in our series.

Keywords: Angiographic outcome, encephaloduroarteriomyosynangiosis, indirect revascularization, moyamoya disease, Suzuki staging system
Key Message: Higher incidence of motor, speech deficits, and seizures was seen in the pediatric population. Age, sex, preoperative Suzuki stage, and hemisphere involvement had no bearing on angiographic outcome at last follow-up following encephaloduroarteriomyosynangiosis, with 90% of patients having event-free status.

How to cite this article:
Furtado SV, Basu E, Mehta A, Vala K, Mohan D. Surgical Outcome of Encephaloduroarteriomyosynangiosis for Moyamoya Disease. Neurol India 2021;69:1259-64

How to cite this URL:
Furtado SV, Basu E, Mehta A, Vala K, Mohan D. Surgical Outcome of Encephaloduroarteriomyosynangiosis for Moyamoya Disease. Neurol India [serial online] 2021 [cited 2022 May 29];69:1259-64. Available from: https://www.neurologyindia.com/text.asp?2021/69/5/1259/329538

Moyamoya disease (MMD) is caused by progressive stenosis or occlusion of the intracranial internal carotid arteries (ICAs), with the development of an abnormal vascular network at the base of the brain and basal ganglia.[1] Two forms exist: ischemic and hemorrhagic. The ischemic type is primarily seen in pediatric patients, whereas the hemorrhagic type predominates in adults.[2] Ischemic events are the most common presenting symptom in MMD, whereas the hemorrhagic presentation accounts for 20% to 50% of cases.[3] Hemorrhage in MMD is attributed to hemodynamic stress on fragile collateral vessels involving the lenticulostriate, choroidal, and other basal moyamoya vessels and also to microaneurysms in the collateral vasculature.[4],[5] The benefit of revascularization in the ischemic and hemorrhagic MMD type in improving patient outcomes is well accepted.[6],[7]

 » Materials and Methods Top

Study population and baseline radiological characteristics

Patients with MMD treated microsurgically by the SVF between January 2006 and March 2019 at two institutions were included in the study. Demographic, clinical, and radiological information was collected from the hospital electronic health records. The pediatric population was categorized as age 18 years or younger and adult as age above 18 years.

The patients were diagnosed with MMD based on the clinical presentation; neuroimaging studies that included computed tomography (CT) and magnetic resonance imaging (MRI); CT or MRI perfusion maps; and six-vessel cerebral angiography in line with the published guidelines.[1],[6],[8]

Preoperative MRI was also examined for the presence of signs of ischemic lesions and infarcts [Figure 1]a. Cerebral six-vessel digital subtraction angiography (DSA) was performed preoperatively and the MMD was staged as per the Suzuki staging system [Table 1]. CT cerebral perfusion study findings were used to quantify the severity of disease [Figure 1]b; further classification of perfusion imaging into normal augmentation, no augmentation, and steal could not be done as a diamox challenge was not administered at our institutes. The side with a larger perfusion deficit was operated on first. The patients' performance status prior to the treatment, at discharge, and at follow-up as determined by the modified Rankin score (mRS; 0–5) was also recorded in addition to other clinical details.
Figure 1: (a) MRI brain FLAIR (fluid-attenuated inversion recovery) image demonstrating left frontal stroke and “ivy-sign” in the left parietal region due to lepta-meningeal collaterals. (b) CT perfusion imaging showing reduced cerebral blood flow in the left frontoparietal region in the same patient

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Table 1: Suzuki staging system for moyamoya disease based on cerebral angiogram

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Radiological and clinical follow-up

The patients were clinically evaluated beginning 3 months after discharge. MRI and cerebral angiography was performed 6 months after the last surgery. Selective external carotid artery (ECA) injections evaluated the bypass patency and the extent of collateralization and revascularization per the Matsushima and Inaba system [Table 2].[9] [Figure 2]a and [Figure 2]b demonstrates preoperative bihemispheric Stage 4 MMD in a pediatric patient, and [Figure 2]c and [Figure 2]d demonstrates Matsushima Grade A revascularization after indirect bypass. Postoperative complications were recorded, including infection, wound dehiscence, infarct, or hemorrhage. Surgical morbidity was included within the 30-day period after the revascularization. The occurrence of stroke, transient ischemic attacks, or rehemorrhage was noted at the last follow-up. The outcome at follow-up was evaluated using the mRS. A good clinical outcome was recorded with an mRS of 2 or less.
Figure 2: Digital subtraction angiography (a) left and (b) right internal carotid artery demonstrating Suzuki Stage IV moyamoya disease; (c) and (d) demonstrating Matsushima Grade A revascularization of the left and right hemispheres, respectively, on external carotid artery injections

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Table 2: Postoperative collateral cerebral revascularization grading on external carotid angiogram (Matsushima and Inaba system)

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Surgical technique

Some indications for indirect revascularization are children younger than 4 years; patients with severe stenosis of ICA or middle cerebral artery (MCA) with preserved antegrade blood flow, but not complete occlusion, or when the donor or the recipient vessels are too small to perform an anastomosis (<0.8 mm in size). Repeat revascularization in a different vascular territory not perfused by the prior procedure may also require an indirect bypass.[10] The superficial temporal artery (STA) is exposed through an incision placed over the artery after it has been mapped using a handheld Doppler (Minidop ES-100VX, Hadeco Inc, Kanagawa, Japan). The mean arterial pressure of 80 to 90 mmHg is maintained in adult patients during the initial arterial dissection and an end-tidal pressure of CO2 is maintained between 35 and 40 mmHg for adequate cerebral vasodilation. The artery is carefully dissected out with a cuff of soft tissue along an 8 to 10 cm length. The vessel patency is preserved. The temporalis muscle is cut in a cruciate fashion and dissected off the bone using a periosteum elevator. A 7- to 8-cm craniotomy is then performed. The dura is opened in a radial fashion at multiple locations [Figure 3]a; the pia overlying fissures and cortical vessels is generally opened in multiple locations using an ophthalmic knife [Figure 3]b. The STA is then placed on the brain surface.[11] In encephaloduroarteriomyosynangiosis (EDAMS) a wider craniotomy is performed to maximize exposure of the brain. The muscle is placed over the STA and over the surface of the brain. The dural margins are inverted and tucked under the craniotomy bone margin to allow the muscle to be sutured over pial surface [Figure 3]c. The dura is inverted because the outer layer of dura is vascularized by the meningeal vessels, whereas the inner layer is avascular. The muscle is sutured over the STA with 3-0 vicryl sutures so that the muscle contacts the incisions placed on the pial surface.
Figure 3: (a) STA placed over pia after stellate dural opening (b) pial incisions being placed with ophthalmic knife (c) Muscle sutured over superficial temporal artery and pial surface with 3-0 vicryl suture

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The free bone flap is thinned out at the inner cortex to accommodate the muscle volume under it. The flap is then replaced over the muscle and arterial tissue by creating a semilunar divot at the base of the craniotomy to accommodate the vascular pedicle. In bihemispheric bypass procedures, the second surgery is performed 3 to 4 weeks after the first surgery.[11]

Statistical analysis

This is a longitudinal retrospective study. We categorized the stage of MMD based on the Suzuki grading system.[12] A stage up to Stage III was considered early stage and Stage IV and above as advanced stage. The angiographic outcome was categorized as good under Matsushima Grade A and poor with Grade B or C. A good clinical outcome was defined as an mRS of 2 or less.

The patient characteristics were described by the percentages for categorical variables and by medians and standard deviations for continuous data. For categorical variables, significant differences between groups were examined by the two-sided Fisher's exact test at the 0.05 level, using SPSS for Windows (SPSS Inc., Chicago, IL). Descriptive statistics of improvement in symptomatic progression were analyzed and summarized in terms of percentage, and its 95% confidence interval was estimated. Chi-squared test at the 0.05 level was used to compare the improvement in symptomatology progression between age and gender.

 » Results Top

Presentation and management

There were 46 patients who underwent surgery during this time period; 25 males (54.3%) and 21 females (45.7%). Twenty-six (56.5%) of the patients were from the East Indian state of West Bengal. The mean age of the patients was 16.62 years (range 2–53 years; median 11.5 years). There were 28 pediatric patients and 18 adults. [Table 3] illustrates the clinical presentation of the patient series with a higher incidence of motor deficits, seizures, and speech deficits in the pediatric group and headache (10 of 20 patients) in the adult group. Seven adults and 20 pediatric patients had an evidence of acute stroke on MRI or CT imaging performed at presentation. Two patients (one adult and a pediatric case) presented with intracerebral bleed that needed a craniotomy and hematoma evacuation. Sixteen patients had undergone CT perfusion scans before surgery. Thirty-three (11 adult and 22 pediatric) patients had bihemispheric and 13 (6 adult and seven pediatric patients) had unilateral hemispheric involvement on cerebral DSA. Six of these patients had left-sided involvement, and seven had right-sided disease. Thirteen patients underwent unilateral indirect bypass procedure, and 33 patients underwent bihemispheric indirect bypass procedures making it a total of 79 hemispheric bypass procedures.
Table 3: Symptoms at presentation in pediatric and adult population

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Age (below or above 18 years) and sex of the patient independently had no significant relation with the stage of the MMD or hemispheric (unilateral or bihemispheric) involvement. The angiographic outcome based on the Matsushima grade for each hemisphere did not show any significant correlation with the preoperative Suzuki stage for the operated hemisphere. We also divided the patient population into pediatric and adult groups and compared the preoperative Suzuki stage with the postoperative Matsushima grade for the operated hemisphere and mRS at discharge. The outcomes did not show any significant correlation. Similar or dissimilar disease stages in bihemipsheric disease did not significantly correlate with angiographic outcome at the last follow-up. Since there was an insignificant difference in the presurgical and follow-up mRS score, we did not compare the mRS outcome at follow-up with the Suzuki stage for the MMD before surgery or the Matsushima angiographic score after surgery.


Two pediatric patients (9 and 13 years old) developed unilateral MCA infarcts in the immediate postoperative period. The first patient presented with facial weakness and dysphasia, and the other presented with aphasia. The symptoms in the second patient improved at discharge, though the first patient continued with the deficits at follow-up. An 8-year old child developed an acute subdural hematoma that required reexploration and evacuation. Two patients developed seizures in the postoperative period that settled at 6-month follow-up and required administration of additional antiepileptic medications. One adult patient developed wound dehiscence that required a scalp flap rotation and closure by a plastic surgeon. There were no perioperative mortalities recorded.


The mean follow-up period was 16.1 months (median 12 months, range 6–78 months). Forty-three patients were on follow-up in this period. Thirty-three patients had stable disease at the last follow-up, and six patients showed improvement in symptoms (four pediatric patients with seizures and an adult and pediatric patient with motor power). Consequently 90% of patients with indirect bypass surgery did not report fresh events at follow-up. At follow-up among 13 patients with unilateral disease, eight demonstrated Matsushima Grade A (six pediatric and two adult), four adults Grade B, and one pediatric patient had Grade C angiographic outcome on ECA angiography. In patients with bilateral disease, 10 demonstrated Grade A (eight pediatric and two adult), 15 showed Grades A and B (nine pediatric and five adult) on individual hemispheres, two pediatric and one adult case demonstrated Grade B in both hemispheres, and two had Grade C (1 pediatric and adult) angiographic outcome at follow-up. One patient each with seizures, dystonia, sensory symptoms, and hemiparesis at presentation did not demonstrate improvement or worsened after surgery. However, fresh infarcts were not seen on MRI. Three patients with hemorrhagic presentation did not have rebleed during follow-up. The mean mRS at the last follow-up was 1 (median 1, range 0–4).

 » Discussion Top

The various indirect bypass surgeries are encephaloduroarteriosynangiosis, encephalomyosynangiosis, EDAMS, encephalogaleosynangiosis, bifrontal encephalogaleoperiostealsynangiosis, and multiple burr hole surgery.[13]

Indirect revascularization is said to develop due to ischemia induced neoangiogenesis from vascular tissues exposed to the brain.

Indian scenario

There are few publications on MMD from the Indian subcontinent.[2],[14],[15],[16] A large majority of research has analyzed the outcome of series of direct versus indirect revascularization procedures.[14],[15],[16] Our analysis is based on pure indirect revascularization of 79 hemispheres in 46 Indian MMD patients, operated over a 14-year period and with 93% of the series with a median follow-up of 1 year. We noticed a higher incidence of ischemic presentation in our patient population with 27 of the 46 (56%) patients with an ischemic presentation, either infarction or TIA, and three patients presented with an intracranial bleed. If we include patients with seizure and headache along with frank ischemic presentation then the incidence of clinical cerebral hypoperfusion as a presenting phenomenon increases to 93.5%. This corresponds to a 90% presentation reported by Sadashiva et al.[2] in an Indian scenario. Garg et al.[15] and Chinchure et al.[14] reported a 32% and 46% incidence of ischemic presentation in their MMD series, respectively. A 100% incidence of ischemic presentation was noted in 15 pediatric patients, and a 47.6% incidence of hemorrhage was noted in 21 adults patients operated at a South Indian center.[17] In a series of 26 patients from northwest India, Srivastava et al.[16] reported a 54% ischemic presentation. Fifty percent of the patients in the same series had posterior circulation involvement. Interestingly, although our hospitals were based in the South Indian city of Bangalore, 28 (60%) of the patient population was from the eastern states of West Bengal, Orissa, and Assam. This can be attributed to a referral bias. Sahoo et al.[18] devised an angiographic scoring system based on visualization of the anterior and MCAs and basal, transdural, and leptomeningeal collaterals to alternately quantify the MMD on angiograms pre- and postoperatively. A positive correlation between Matushima grade and angiographic outcome score was recorded in a series of 33 patients who underwent EDAMS or combined revascularization procedure.

Ishikawa et al.[19] noted no difference in the outcome at long-term follow-up in patients who have undergone either direct or indirect cerebral bypass surgeries, although there was a significantly higher incidence of postoperative stroke in the indirect group. Indirect bypass takes a shorter duration to perform in comparison with direct bypass procedures. The hemodynamic, metabolic, and anesthetic risks such as hypotension, hypoxia, and hypo/hypercarbia are relatively less.[8] A 3-month duration is needed to develop revascularization after an indirect procedure, and the procedure may continue to provide new vessels years after surgery, as the primary disease progresses. This is relevant when a direct bypass is attempted in the early stages of the disease. Competing flows at and around the bypass site between the STA flow and the parent MCA vessel may close the bypass.[10],[20] In a dynamic pathology such as MMD, there are instances of acute contralateral ICA occlusion following direct revascularization procedures, hyperperfusion injuries and stroke, postoperative intracerebral bleed, and intracerebral steal syndrome.[21],[22]

Chou et al.[23] demonstrated Matsushima Grades A and B perfusion in 19 of 21 patients who had undergone indirect bypass over a mean follow-up of 38.6 months. In a large series of 629 pediatric patients who underwent indirect bypass, Ha noted a favorable outcome in 95% of the patients. The 10-year event-free survival rates for symptomatic infarction and hemorrhage were 99.2% and 99.8% in the study. Also, an annual risk of symptomatic infarction and hemorrhage of 0.08% and 0.04%, respectively, was noted on the operated hemispheres.[7] Better collateralization after indirect bypass is seen in patients with anterior hemorrhagic MMD. It is postulated that a lower hemodynamic stress in the lenticulostriate vessels in comparison with thalamic and choroidal arteries contributes to robust collateralization.[24]

In our series, 18 of 43 (42%) patients on follow-up had good revascularization (Matsushima Grade A) per our definition. Eight patients (18.6%) had Matsushima Grade B revascularization, 15 (43%) patients with bilateral revascularization had a combination of Grade A or B revascularization on individual hemispheres at follow-up. Forty of 43 (93%) patients demonstrated either Grade A or B revascularization. This compares favorably with previously documented revascularization grades based on the Matsushima grading system.[14],[18] It corresponds to a 90% event-free status noted clinically at last follow-up. Our complication rate was 6.5%. Progressive occlusion of the anterior circulation reduced moyamoya vessels due to disease progression, disruption of transdural collaterals following durotomy for indirect bypass procedure, and the latency period for the development of collaterals that may extend up to 12 months following indirect revascularization are some of the proposed mechanisms for postoperative strokes.[13],[21]

There are some limitations of the study. The study population is small to derive a meaningful statistical outcome between pediatric and adult cases. Only 35% of the patients had a preoperative CT perfusion study due to financial or logistical issues. Patients with unilateral disease and uni-hemispheric procedure need a more robust follow-up to study the disease involvement of the opposite side. Thirty-one out of the 43 patients had follow-up of more than 2 years, indicating a need for longer follow-up for disease progression and treatment outcome.

The role of indirect bypass procedure in providing symptomatic relief and lowering the risk of stroke during follow-up when compared with conservative management is well established in a North American cohort.[25] Kazumata and Feghali et al.[8] showed that the postoperative stroke rate after direct or combined bypass procedure was similar to that observed after indirect revascularization procedure, thus supporting its safety.[13]

 » Conclusions Top

Indirect bypass procedure can be employed in situations where a direct bypass would be associated with an increased risk of hemorrhage as in hemorrhagic MMD or risk of hyperperfusion injury and stroke is high, as in patients with bilateral disease and poor cerebrovascular reserve. Additionally, the phenomenon of competing flows at the site of a direct bypass in the early stages of MMD has been described above. The indirect procedure can also be employed when the area of hypoperfusion is away from the direct bypass territory as noted in follow-up angiogram or perfusion studies performed in patients who continue to be symptomatic after direct bypass surgery. The procedure is easy to perform for a young neurosurgeon, and it is safer to monitor patients in the postoperative period when compared with direct bypass procedure for MMD.

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Conflicts of interest

There are no conflicts of interest.

 » References Top

Guzman R, Lee M, Achrol A, Bell- Stephens T, Kelly M, Do HM, et al. Clinical outcome after 450 revascularization procedures for moyamoya disease. J Neurosurg 2009;111:927-93.  Back to cited text no. 1
Sadashiva N, Reddy YV, Arima A, Saini J, Shukla D, Pandey P. Moyamoya disease: Experience with direct and indirect revascularization in 70 patients from a nonendemic region. Neurol India 2016;64(Suppl 1):78-86.  Back to cited text no. 2
Kobayashi E, Saeki N, Oishi H, Hirai S, Yamaura A. Long-term natural history of hemorrhagic moyamoya disease in 42 patients. J Neurosurg 2000;93:976-80.  Back to cited text no. 3
Jiang H, Ni W, Xu B, Lei Y, Tian Y, Xu F, et al. Outcome in adult patients with hemorrhagic moyamoya disease after combined extracranial-intracranial bypass. J Neurosurg 2014;121:1048-55.  Back to cited text no. 4
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Abhinav K, Furtado SV, Nielsen TH, Iyer A, Gooderham PA, Teo M, et al. Functional outcomes after revascularization procedures in patients with hemorrhagic moyamoya disease. Neurosurgery 2020;86:257-65.  Back to cited text no. 6
Ha EJ, Kim KH, Wang KC, Phi JA, Lee JY, Choi JW, et al. Long-term outcomes of indirect bypass for 629 children with moyamoya disease: Longitudinal and cross-sectional analysis. Stroke 2019;50:3177-83.  Back to cited text no. 7
Feghali J, Xu R, Yang W, Liew JA, Blakeley J, Ahn ES. Moyamoya disease versus moyamoya syndrome: Comparison of presentation and outcome in 338 hemispheres. J Neurosurg 2019;1-9. doi: 10.3171/2019.6.JNS191099.  Back to cited text no. 8
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  [Figure 1], [Figure 2], [Figure 3]

  [Table 1], [Table 2], [Table 3]


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