outcome of repeat revascularization surgery for moyamoya...

J Neurosurg 115:328–336, 2011

328 J Neurosurg / Volume 115 / August 2011

MoyaMoya disease is characterized by idiopathic, chronic, usually bilateral stenosis or occlusion of intracranial ICAs, proximal MCAs, and

ACAs, and is a cause of stroke or TIAs in children and adults.37 Both direct and indirect methods of revascular-ization are described in the literature, and are aimed at providing collateral blood supply through the ECAs to the ischemic hemisphere.

Outcome of repeat revascularization surgery for moyamoya disease after an unsuccessful indirect revascularization

Clinical articleParitosh Pandey, M.d., and Gary K. steinberG, M.d., Ph.d.Department of Neurosurgery, Stanford University School of Medicine, Stanford, California

Object. Revascularization for moyamoya disease, either by direct anastomosis or indirect procedures, is an ac-cepted and effective form of treatment for prevention of future ischemic events. Indirect procedures do not provide sufficient collateral vessels in a subset of patients, who then have persistent or new symptoms. Repeat revasculariza-tion procedures may be recommended for these patients.

Methods. Sixteen patients underwent repeat revascularization after undergoing an indirect procedure in the same hemisphere. These patients were included in the study, and a retrospective review of their clinical details, neuroim-aging results, surgical details, and outcome was performed. Direct revascularization was the procedure of choice; however, in patients with no acceptable recipient vessel (> 0.6 mm) the authors added a second indirect procedure for further revascularization.

Results. Over the last 19 years, 16 patients (8 male and 8 female patients, age range 5–48 years, mean 16.7 years, 10 pediatric and 6 adult patients) underwent repeat revascularization for moyamoya disease. Initially all patients presented with ischemic symptoms (4 transient ischemic attacks [TIAs] and 12 strokes; 2 patients had bilateral symp-toms). Angiography revealed that 13 patients had bilateral disease, and 3 had unilateral disease. Initial surgery was bilateral encephaloduroarteriosynangiosis (EDAS) in 9, unilateral EDAS alone in 3, unilateral EDAS with contralat-eral superficial temporal artery–middle cerebral artery (STA-MCA) bypass in 2, bilateral encephalomyosynangiosis (EMS) in 1, and unilateral EMS in 1. Thirteen of the 16 patients continued to have TIAs in the hemisphere ipsilateral to surgery, whereas 1 patient had seizures and cognitive deficit, 1 had asymptomatic infarct on MR imaging, and 1 had visual symptoms. Poor revascularization was seen on angiography studies in all patients. The median duration between the surgeries was 24 months (3 months–10 years).

Repeat revascularization was performed in 23 hemispheres (16 patients). Direct revascularization was performed in 14 hemispheres (60.9%): STA-MCA bypass in 10, external carotid artery–MCA vein bypass in 2, occipital artery (OA)–MCA in 1, and OA–posterior cerebral artery in 1 hemisphere. Indirect revascularization was performed for pa-tients without an acceptable recipient vessel, and was done in 9 hemispheres. The procedures included EMS (4 hemi-spheres), repeat EDAS (2), and omental transposition (3). There was 1 postoperative death in a patient undergoing a high-flow vein graft implantation. None of the other patients experienced any neurological worsening after surgery.

Follow-up was available in all patients, ranging from 3 to 144 months (mean 34 months, median 12 months). Of the 15 patients who survived repeat revascularization surgery, 12 (80%) were free from any TIA, stroke, or any other neurological symptoms. Two patients had occasional TIAs, less frequent than before, whereas 1 patient had frequent TIAs and underwent revision of the revascularization. Angiographic studies were available in 11 patients, and showed improved flow in the hemispheres in 10 patients. Follow-up MR imaging performed at 6 months did not reveal a new infarct in any patient.

Conclusions. Repeat revascularization procedures are effective for patients who are clinically symptomatic and have inadequate collateral vessels following indirect procedures. Although direct procedures are preferred, the choice of procedure depends on the operative findings and the status of donor and recipient vessels.(DOI: 10.3171/2011.3.JNS101908)

Key Words • moyamoya disease • repeat revascularization • superficial temporal artery–middle cerebral artery bypass • vascular disorders

Abbreviations used in this paper: ACA = anterior cerebral artery; CBF = cerebral blood flow; DS = digital subtraction; ECA = exter-nal carotid artery; EDAS = encephaloduroarteriosynangiosis; EEG = electroencephalography; EMAS = encephalomyoarteriosynangiosis; EMS = encephalomyosynangiosis; ICA = internal carotid artery; MCA = middle cerebral artery; OA = occipital artery; PCA = poste-rior cerebral artery; SSEP = somatosensory evoked potential; STA = superficial temporal artery; TIA = transient ischemic attack.

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Repeat revascularization surgery for moyamoya disease

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A variety of indirect procedures have been described, including EDAS,25,28,29 EMS,17 omental transpositions,11,18 placement of multiple bur holes,34 and a combination of these procedures.15,22,42 Although they are successful in the majority of patients, especially in the pediatric pop-ulation, a potential disadvantage of these procedures is that sometimes they do not provide sufficient collateral vessels to prevent symptoms.2,27 Repeat revascularization procedures are required for these patients with persistent or new symptoms. Depending on the donor and recipient vessels available, these might be either direct or indirect procedures. There have been a few reports describing the outcomes of repeat revascularization procedures, mostly from Japan.12,24,27,31,39–41 We present our experience and outcomes in patients undergoing repeat revasculariza-tion for moyamoya disease after an unsuccessful indirect procedure. This is the first report from North America describing repeat revascularization in moyamoya disease.

MethodsA prospectively maintained database (MD Analyze;

Medtamic, Inc.) of patients with vascular malformations treated at Stanford University Medical Center was used to identify all patients with moyamoya disease. Over the last 19 years, we have performed revascularization pro-cedures in 502 patients with moyamoya disease. Of these patients, 16 had repeat revascularization after undergoing indirect procedures in the same hemisphere. These pa-tients were included in this study, and were analyzed ret-rospectively. A total of 23 hemispheres were revascular-ized in these 16 patients. Fifteen underwent initial revas-cularization at another institution, whereas 1 had the first revascularization at our institution. One other patient had a third revascularization procedure at another institution after undergoing the repeat revascularization procedure at our institution, as mentioned later in the paper. Thus, of the 502 patients undergoing revascularization surgery at our institution, the percentage of patients requiring a repeat surgery was 0.4%.

The clinical presentation, neuroimaging, and surgical details of the patients previous to the first procedure were obtained from the initial institutions. After the referral to our institution, all 16 patients were evaluated with a clini-cal history and examination, MR imaging of the brain with perfusion, a 6-vessel angiogram, and CBF studies with either SPECT or Xe-CT scanning before and after administration of acetazolamide. The clinical findings and the radiological data were discussed in a multidisci-plinary conference comprising the neurosurgeon, the neu-roradiologist, and sometimes the stroke neurologist. The adequacy of the previous revascularization was assessed using the results from all the investigations, as well as from clinical examination. A patient was considered for repeat revascularization if he/she was symptomatic, and if the angiographic and/or CBF data suggested incomplete revascularization. A second surgery for revascularization was also considered if the patient was asymptomatic but had new infarcts on MR imaging of the brain, with angio-graphic and/or CBF studies suggesting incomplete revas-cularization. All these data were analyzed retrospectively

by the authors with the neuroradiologist, and the charts, radiology films, and records were reviewed.

Choice of ProceduresIn most of the patients, direct revascularization with

STA-MCA bypass was our procedure of choice. The technique of STA-MCA bypass for moyamoya disease has been described before.3,10 In most of the patients, the branch used for EDAS was left intact, and another branch of the STA (or in 1 case, the OA) was used for direct re-vascularization. This was done to avoid disrupting the collateral vessels from the previous indirect surgery, and the potential ischemic sequelae. In only 2 instances, we used the same branch that was previously used for EDAS for direct revascularization, because the other branch was very small and the revascularization from the indirect procedure was extremely limited. In these patients the dissection of the STA was difficult, and there were adhe-sions to the brain from the previous indirect procedure. However, with careful dissection, it was possible to sepa-rate the vessel from the underlying brain. Although exact measurements were not performed, the craniotomies in the previous surgeries were not any different from those in the other patients in whom the indirect revasculariza-tion was successful. In patients in whom there was no ac-ceptable (> 0.6 mm) recipient vessel available, we added a second indirect procedure, such as EMS, omental trans-positions, or EDAS performed using another branch of the STA, for further revascularization. The techniques for these procedures have been described before in the litera-ture.11,17,18,22,25,34

Follow-Up DataFollow-up was obtained from the clinic visit notes

or through telephone communication when there was no clinic visit following the surgery. Imaging studies, in-cluding MR images of the brain, SPECT scans with and without acetazolamide, and a 6-vessel angiogram, were obtained at 6 months and 3 years following surgery.

ResultsPatient Population

Over the last 19 years, 16 patients underwent repeat revascularization for moyamoya disease. There were 8 male and 8 female patients, whose ages ranged from 5 to 48 years (16.7 ± 12.57 years; mean ± SD). There were 10 pediatric (< 18 years of age) and 6 adult patients. Table 1 lists the demographic details of the patients.

Initial SurgeryInitial presentation was with ischemic symptoms

in all patients; 4 presented with TIAs, whereas 12 had stroke with deficits. Two patients had bilateral symptoms. Of the 12 patients presenting with stroke, 5 had major hemispheric stroke with residual deficits, whereas the other 7 had small cortical/subcortical infarcts with minor deficits, which improved prior to surgery. None of the pa-tients had hemorrhage as the clinical presentation of the

P. Pandey and G. K. Steinberg


disease. Brain MR imaging showed watershed infarcts in 6 patients, small hemispheric infarcts in 2, and large cor-tical infarcts in 8. Angiographic studies were done in all the patients and revealed bilateral moyamoya disease in 13 patients, whereas 3 had unilateral disease.

The predominant form of indirect surgery was EDAS, with bilateral procedures in 9 patients and unilateral in 5 (2 of these latter patients also underwent contralateral STA-MCA bypass). One patient underwent bilateral EMS and 1 had a unilateral EMS (Table 1). One patient had a major postoperative hemispheric infarct, and 1 patient had a major stroke 1 month after the indirect surgery. Two other patients had mild worsening of power in the contra-lateral hand, which recovered over a period of 1 month.

Indications for Repeat SurgeryThirteen of the 16 patients continued to have TIAs in

the hemisphere ipsilateral to their surgery after their in-direct revascularization procedures. All of these patients had had recent TIAs (within the preceding month) when they presented to our clinic. One of these patients had a mild stenosis of the M1 segment, which progressed and caused severe M1 stenosis at follow-up. Of 3 other pa-tients, 1 had seizures and also complained of increasing cognitive deficits. Another patient was clinically asymp-tomatic, but had evidence of recent infarcts on follow-up MR imaging. One patient who had a major hemispheric infarct with homonymous hemianopia had contralateral visual symptoms, which were thought to be posterior circulation TIAs. The median duration between the two surgeries was 24 months (3 months–10 years). New (or recent) infarcts on MR imaging on the side ipsilateral to indirect surgery were documented in 5 patients. Details of CBF studies were available in 12 patients. Imaging us-ing HMPAO-SPECT was done in 8 patients, whereas 4 patients underwent Xe-CT with and without the adminis-

tration of acetazolamide. All of them had perfusion defi-cits on the baseline CBF studies, with 7 patients showing acetazolamide reactivity, whereas 5 patients did not show expected augmentation after acetazolamide administra-tion. Details of flow studies were not available in 4 pa-tients. Angiography was performed in all patients, and showed poor revascularization in all of them, character-ized by filling of fewer than 2 cortical branches of the MCA.

Repeat SurgeryRepeat revascularization was performed in 23 hemi-

spheres, in 16 patients (Table 2). Direct revasculariza-tion with STA-MCA bypass was performed in 10 hemi-spheres, whereas an ECA-MCA anastomosis was done using a vein graft in 2 hemispheres. Direct revascular-ization in the form of OA-PCA and OA-MCA anastomo-sis was done in 1 hemisphere each. Thus, a total of 14 hemispheres (60.9%) underwent direct revascularization. In most of the STA-MCA anastomosis procedures, the branch used for initial EDAS was left intact, and another branch of the STA was used for anastomosis. In only 2 patients was the same branch of the STA used for direct anastomosis because the collateral vessels supplied by the EDAS were extremely limited on the preoperative angio-gram, and the other branch of the STA was unavailable. This procedure was done after temporary clipping of the donor vessel, and waiting for 10 minutes to observe any changes in the EEG findings or SSEPs. Indirect revas-cularization was performed in 9 hemispheres, including EMS (4 hemispheres), repeat EDAS using another branch of the STA (2), and omental transposition (3). All of these patients underwent indirect revascularization because there were no acceptable recipient vessels available. One patient undergoing ECA-MCA bypass suffered reperfu-sion hemorrhage and a large intracerebral hematoma and

TABLE 1: Demographic details and original surgery in 16 patients with moyamoya disease*

Case No. Age (yrs), Sex Initial Presentation Angio Findings Preop Indirect Op

1 5, M lt hemi TIA bilat bilat EDAS 2 5, M rt hemi stroke unilat rt EMS 3 6, M lt hemi stroke bilat bilat EDAS 4 7, M rt hemi stroke unilat lt EDAS 5 8, F rt hemi stroke bilat rt EDAS w/ multiple bur holes 6 8, M bilat TIAs, lt hemi stroke bilat bilat EDAS 7 8, M lt hemi stroke bilat bilat EMS 8 10, F rt hemi stroke bilat bilat EDAS 9 11, F lt hemi TIA bilat lt EDAS, rt STA-MCA bypass10 14, F lt hemi stroke/TIA bilat bilat EDAS11 24, F lt hemi stroke bilat lt STA-MCA bypass, rt EDAS12 26, M lt hemi stroke/TIA bilat bilat EDAS13 28, F lt hemi stroke bilat bilat EDAS14 28, M rt hemi stroke/bilat TIAs bilat bilat EDAS15 31, F lt hemi TIA unilat rt EDAS16 48, F lt hemi TIA bilat bilat EDAS

* Angio = angiography; hemi = hemisphere.



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died. Two patients had a postoperative seizure, which was treated with antiepileptic drugs. None of the other pa-tients had any neurological worsening following surgery.

Follow-Up FindingsClinical follow-up was available in all patients, with

the range of follow-up duration being 3–144 months (34 ± 37.9 months [mean ± SD]; median 12 months). Twelve (80%) of the 15 patients who survived repeat revascular-ization surgery were well and free from any TIA, stroke, or new symptoms. Two patients had occasional TIAs, the frequency and severity of which were significantly less than prior to their repeat surgery. One patient did well for 1 year, when he developed frequent TIAs. He was evalu-ated at another institution, and his MR imaging studies showed no new ischemic lesions. However, the angio-gram revealed nonvisualization of the graft/anastomo-sis. Hence, he underwent repeat EMS and multiple bur holes, after which he did well, with no further ischemic episodes.

Studies of CBF obtained at 6 months were available in 12 patients, and showed normalization of flow, with good augmentation following acetazolamide in all pa-tients, except in the areas of prior infarct. An angiogram was available in 11 patients. There was improved flow in the hemispheres in 10 patients, and the graft was not vi-sualized in 1 patient (only the report was available from the other institution). Figures 1–3 are representative MR imaging and angiography studies from the patients show-ing inadequate revascularization after the first procedure and robust revascularization following repeat surgery. The MR imaging studies obtained at 6 months revealed no new infarcts in any patients.

DiscussionMoyamoya disease is characterized by idiopathic,

chronic occlusion of bilateral supraclinoid ICAs, proxi-mal MCAs, and ACAs, along with the formation of moya-

TABLE 2: Repeat surgery and outcomes in 16 patients with moyamoya disease*

Case No. 1st Op Sx After 1st Op

Duration Btwn 2 Ops

(mos)Op in Previously Revascular-

ized Hemi(s)

No. of Hemis Re-revascu-

larized Outcome at FU

1 bilat EDAS bilat TIA 36 bilat STA-MCA bypass 2 occasional TIAs, flow normal, robust collaterals on angio

2 rt EMS rt hemi TIA 10 rt STA-MCA bypass 1 no TIA/stroke 3 bilat EDAS seizures, cognitive de-

cline 18 lt STA-MCA bypass 1 no TIA/stroke

4 lt EDAS lt hemi TIAs 48 lt STA-MCA bypass 1 TIA; possible graft occlusion, repeat EMS performed elsewhere

5 rt EDAS w/ multiple bur holes

rt hemi ischemic stroke w/ sequelae

3 rt EMS 1 no TIA/stroke

6 bilat EDAS bilat TIA, fresh infarct on MRI

36 rt STA-MCA bypass, lt omental transposition w/ STA anastomosis

2 no TIA/stroke

7 bilat EMS lt hemi TIA, fresh infarct on MRI

60 rt OA-MCA bypass, lt omental transposition

2 no TIA/stroke

8 bilat EDAS visual 30 lt OA-PCA bypass 1 occasional TIAs, flow normal, robust collaterals on angio

9 lt EDAS, rt STA-MCA bypass

lt hemi TIAs 6 lt STA-MCA bypass 1 no TIA/stroke

10 bilat EDAS lt hemi TIAs 120 bilat EDAS, frontal branch 2 no TIA/stroke11 lt STA-MCA bypass, rt

EDASlt hemi TIAs 6 rt EMS 1 no TIA/stroke

12 bilat EDAS rt hemi ischemic stroke 84 rt STA-MCA bypass, lt omental transposition

2 no TIA/stroke

13 bilat EDAS lt hemi TIAs 96 bilat STA-MCA bypass 2 no TIA/stroke14 bilat EDAS asymptomatic infarct

on MRI 14 rt EMS 1 no TIA/stroke

15 rt EDAS rt hemi TIA 9 rt EMS 1 no TIA/stroke16 bilat EDAS bilat TIA, fresh infarct

on MRI 6 bilat ECA-MCA bypass (w/ vein

graft)2 died

* FU = follow-up.



Fig. 1. Digital subtraction angiography studies (lateral projection) of the right ECA (A) and left ECA (B) showing inadequate revascularization following bilateral EDAS. Bilateral revascularization was performed with the frontal branch of the STA, leading to robust revascularization in the right ECA (C) and left ECA (D). The branch of the STA used for EDAS is marked with a black arrowhead, and the branch used for the STA-MCA bypass is marked with a black arrow.

Fig. 2. Left: A DS angiography study (lateral projection) of the left ECA injection showing inadequate revascularization from EDAS performed on the left side. Right: A DS angiography study (lateral projection) of the left ECA injection showing better filling of two-thirds of the hemisphere following addition of an STA-MCA bypass. The branch of the STA used for EDAS is marked with a black arrowhead, and the branch used for the STA-MCA bypass is marked with a black arrow.



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moya vessels at the base of the brain, and transdural col-lateral vessels attempting to compensate for the ischemia resulting from the occlusion.3,37 The treatment of moya-moya disease is to augment the blood supply of the brain

from the ECA system. This is achieved either through direct anastomosis to a cortical MCA branch (or in some cases, an ACA or PCA branch), or through stimulation of collateral formation through a variety of indirect meth-

Fig. 3. A: Axial T2-weighted MR imaging study of the brain showing left-sided watershed infarcts. B and C: Digital subtrac-tion angiography studies, right ICA and left ICA injections, lateral projection, showing occlusion of bilateral ICAs with moyamoya vessels. D and E: Digital subtraction angiography studies, right ECA and left ECA injections, lateral projection, showing very small areas of revascularization following bilateral EDAS. F–I: Left ECA injection, anteroposterior (F) and lateral (G) projec-tions, and right ECA injection, anteroposterior (H) and lateral (I) projections, showing excellent revascularization, predominantly from meningeal collateral vessels following bilateral STA-MCA anastomosis and overlaying of the artery on the brain.



ods. This is achieved by placing either an ECA branch (typically the STA) or muscle and dura mater over the ischemic brain to promote angiogenesis. The choice of procedure in both the pediatric and adult population is a matter of debate, with proponents of both procedures publishing their findings in the literature.

Direct revascularization for moyamoya disease is an established technique, and a number of authors including our group have described good results, both in adult and pediatric populations.1,8–10,19 The main advantages of the direct anastomosis are the establishment of augmented flow immediately following the surgery and more consis-tent formation of collateral vessels. The results of direct revascularization in adults have been well described by many authors. Long-term studies following delayed re-vascularization describe patency rates as high as 91%.1,9,10 The direct anastomoses also have very good clinical outcomes, particularly in reducing or preventing further ischemic events. In our study comprising 264 patients un-dergoing 450 revascularization procedures, with 89.4% of procedures being direct revascularization, the 5-year risk of perioperative or subsequent stroke or death was 5.5%, with 91.8% of patients free of any ischemic event at 1-year follow-up.9 Other authors have published equally good re-sults in smaller series. The results of direct revasculariza-tion in the pediatric population are published less often. However, small case series have described good results in preventing ischemic events in children. Some authors have combined STA-MCA with the indirect procedure in an attempt to improve long-term revascularization.15,30,44 The disadvantages of the direct procedures are as follows: the requirement of technical expertise for this procedure; the nonavailability of appropriate donor or recipient ves-sels, particularly in the pediatric population; and a higher incidence of complications compared with the indirect procedures.7 Some authors have noted the occurrence of a hyperperfusion syndrome and transient neurological deficits due to the sudden increase in the blood flow to an ischemic brain.5,6,21,26,38 On the other hand, indirect pro-cedures have become very popular, especially in the pe-diatric population, because of the ease of the surgery, its effectiveness, and lower rates of complications. Although the efficacy of various indirect procedures has been well established in children,6,7,13,14,16,18,20–23,25,30,33–35,43 the ef-ficacy in adults is still controversial. Although a recent publication suggests that indirect revascularization is also effective in reducing the risk of future ischemic events for adults with moyamoya disease,36 many authors have published superior results after performing direct proce-dures.1,4,19,23,32,33

One of the disadvantages of the indirect procedures, especially the EDAS, is the inconsistent and sometimes incomplete development of adequate collateral vessels. In a study comparing various forms of revascularization, Matsushima et al.25 found that collateral formation in more than two-thirds of the hemisphere occurred in only 44% of the hemispheres after a single indirect procedure, compared with 52% after multiple combined indirect procedures and 74% after STA-MCA anastomosis. Other authors have also reported on failed EDAS procedures, in which the collateral formation is inadequate, the patients

continue to be clinically symptomatic, or both.2,12,27,31 Various procedures have been described to augment the collateral formation with EDAS, but still there is a sub-set of patients who have inadequate collateral formation, and who remain clinically symptomatic. The treatment options for this subset of patients have been poorly de-scribed in the literature. Most of the reports of recon-struction after failed indirect anastomosis are from the Japanese literature. Ours is the first series from North America describing repeat revascularization of failed in-direct anastomosis.

Miyamoto et al.31 reported a series of 11 patients with failed indirect anastomosis and documented good results, with newly formed collateral vessels on repeat angiography studies after additional STA-MCA bypass or omental transposition. Matsushima et al.24 described the addition of an EMS or EMAS procedure in 3 patients with failed EDAS, and obtained better collateral vessels. Touho et al.41 performed omental transplantation by using a branch of the STA previously used in the EDAS that did not provide adequate collateral vessels, with good clini-cal and angiographic results in all 5 patients. The same group later treated 28 hemispheres that had previously been treated with indirect revascularization using EDAS, after which patients presented with continuing symptoms and inadequate collateral formation.40 These practitioners performed STA-MCA anastomosis in all patients, and ad-ditional omental transposition in 1 individual, leading to excellent recovery in all of them. The investigators used the same branch of the STA used in the EDAS proce-dures, and reported no new deficits. They thus concluded that the small amount of collaterals around the EDAS vessel was clinically insignificant.

On the other hand, in our series, we performed direct anastomosis for 14 (60.9%) of the 23 hemispheres revas-cularized. In the rest of the hemispheres, we could not find an adequate recipient vessel, or there was extensive adhesion as a result of the first operation, and we per-formed indirect procedures. In most of the cases, we left the branch used for EDAS intact, to avoid disrupting the collaterals formed around it, and because of dense adhe-sions associated with EDAS. In only 2 cases did we use the same branch of the STA; in those cases we monitored any changes in the SSEP and EEG findings following clip occlusion of the STA, and only when there were no sig-nificant changes in the electrophysiological potentials did we sacrifice the minimal collateral vessels from the previ-ous procedure. Other authors have also reported on small series of patients with failed indirect procedures, and the reconstruction with further addition of indirect or direct procedures.12,39 In the series by Touho et al.,40 all patients were symptomatic, with recurrent ischemic events. In our patients, all except 3 had TIAs; of those 3, 1 had recent infarcts, 1 had seizures and cognitive decline, and 1 had progression of posterior circulation ischemic symptoms.

In our opinion, the clinical symptoms, radiological and angiographic findings, and the results of CBF studies should be analyzed and correlated before subjecting the patient to a repeat procedure. In the present series, we obtained excellent results in most of the patients. How-ever, there was 1 death secondary to reperfusion hemor-



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rhage; this occurred in a patient who was having multiple frequent TIAs despite previous EDAS procedures, who had recent infarcts on repeat MR imaging, and received a high-flow vein graft. Since the experience of this adverse outcome after using a saphenous vein interposition graft from the ECA to the M4 artery, we have abandoned the use of higher-flow vein bypasses for patients with moya-moya disease.

Choice of ProceduresVarious authors have described the use of both di-

rect and indirect procedures for reconstruction of an in-adequate indirect procedure.12,24,31,39–41 In our experience, judicious use of either procedure gives good results. As is our policy for initial revascularization in most patients with moyamoya disease, we prefer direct anastomosis with STA-MCA bypass to provide immediate and reli-able augmentation of blood supply to the ischemic hemi-sphere. However, in cases in which the recipient vessels are small or there are multiple adhesions, we use indi-rect procedures, especially EMS, or occasionally omental transpositions, if adequate muscle is not available. The choice of the procedure is tailored to the operative find-ings and availability of donor and recipient vessels.

ConclusionsRepeat revascularization procedures are clinically

effective in preventing future ischemic events, and can be safely performed for patients who are clinically symp-tomatic and have inadequate collateral vessels following indirect procedures, especially EDAS. Although direct procedures are preferred, the choice depends on the op-erative findings and the status of donor and recipient ves-sels.

Disclosure

This work was supported in part by Russell and Elizabeth Siegelman, Bernard and Ronni Lacroute, the William Randolph Hearst Foundation, Stanley and Alexis Shin, and the Huber Family Moyamoya Fund. The authors have no conflict of interest to declare.

Author contributions to the study and manuscript prepara-tion include the following. Conception and design: both authors. Acquisition of data: both authors. Analysis and interpretation of data: both authors. Drafting the article: Pandey. Critically revising the article: both authors. Approved the final version of the paper on behalf of all authors: Steinberg.

Acknowledgments

The authors thank Cindy H. Samos for assistance with the manuscript and Beth Hoyte for help with figure preparation.

References

1. Burke GM, Burke AM, Sherma AK, Hurley MC, Batjer HH, Bendok BR: Moyamoya disease: a summary. Neurosurg Fo-cus 26(4):E11, 2009

2. Cahan LD: Failure of encephalo-duro-arterio-synangiosis procedure in moyamoya disease. Pediatr Neurosci 12:58–62, 1985–1986

3. Chang SD, Steinberg GK: Superficial temporal artery to mid-

dle cerebral artery anastomosis, in Steinberg GK (ed): Tech-niques in Neurosurgery. Philadelphia: Lippincott Williams and Wilkins: Philadelphia, 2000, Vol 6, pp 86–100

4. Czabanka M, Vajkoczy P, Schmiedek P, Horn P: Age-depen-dent revascularization patterns in the treatment of moyamoya disease in a European patient population. Neurosurg Focus 26(4):E9, 2009

5. Fujimura M, Kaneta T, Mugikura S, Shimizu H, Tominaga T: Temporary neurologic deterioration due to cerebral hyperper-fusion after superficial temporal artery-middle cerebral artery anastomosis in patients with adult-onset moyamoya disease. Surg Neurol 67:273–282, 2007

6. Fujimura M, Mugikura S, Kaneta T, Shimizu H, Tominaga T: Incidence and risk factors for symptomatic cerebral hyperper-fusion after superficial temporal artery-middle cerebral artery anastomosis in patients with moyamoya disease. Surg Neurol 71:442–447, 2009

7. Fung LW, Thompson D, Ganesan V: Revascularisation sur-gery for paediatric moyamoya: a review of the literature. Childs Nerv Syst 21:358–364, 2005

8. Golby AJ, Marks MP, Thompson RC, Steinberg GK: Direct and combined revascularization in pediatric moyamoya dis-ease. Neurosurgery 45:50–60, 1999

9. Guzman R, Lee M, Achrol A, Bell-Stephens T, Kelly M, Do HM, et al: Clinical outcome after 450 revascularization pro-cedures for moyamoya disease. Clinical article. J Neurosurg 111:927–935, 2009

10. Guzman R, Steinberg GK: Direct bypass techniques for the treatment of pediatric moyamoya disease. Neurosurg Clin N Am 21:565–573, 2010

11. Havlik RJ, Fried I, Chyatte D, Modlin IM: Encephalo-omental synangiosis in the management of moyamoya disease. Sur-gery 111:156–162, 1992

12. Hayashi T, Shirane R, Tominaga T: Additional surgery for postoperative ischemic symptoms in patients with moyamoya disease: the effectiveness of occipital artery-posterior cere-bral artery bypass with an indirect procedure: technical case report. Neurosurgery 64:E195–E196, 2009

13. Houkin K, Kuroda S, Ishikawa T, Abe H: Neovascularization (angiogenesis) after revascularization in moyamoya disease. Which technique is most useful for moyamoya disease? Acta Neurochir (Wien) 142:269–276, 2000

14. Irikura K, Miyasaka Y, Kurata A, Tanaka R, Yamada M, Kan S, et al: The effect of encephalo-myo-synangiosis on abnor-mal collateral vessels in childhood moyamoya disease. Neu-rol Res 22:341–346, 2000

15. Ishikawa T, Kamiyama H, Kuroda S, Yasuda H, Nakayama N, Takizawa K: Simultaneous superficial temporal artery to middle cerebral or anterior cerebral artery bypass with pan-synangiosis for Moyamoya disease covering both anterior and middle cerebral artery territories. Neurol Med Chir (Tokyo) 46:462–468, 2006

16. Isono M, Ishii K, Kamida T, Inoue R, Fujiki M, Kobayashi H: Long-term outcomes of pediatric moyamoya disease treated by encephalo-duro-arterio-synangiosis. Pediatr Neurosurg 36:14–21, 2002

17. Karasawa J, Kikuchi H, Furuse S, Sakaki T, Yoshida Y: A sur-gical treatment of “moyamoya” disease “encephalo-myo syn-angiosis”. Neurol Med Chir (Tokyo) 17:29–37, 1977

18. Karasawa J, Touho H, Ohnishi H, Miyamoto S, Kikuchi H: Cerebral revascularization using omental transplantation for childhood moyamoya disease. J Neurosurg 79:192–196, 1993

19. Khan N, Schuknecht B, Boltshauser E, Capone A, Buck A, Im-hof HG, et al: Moyamoya disease and Moyamoya syndrome: experience in Europe; choice of revascularisation procedures. Acta Neurochir (Wien) 145:1061–1071, 2003

20. Kim DS, Kang SG, Yoo DS, Huh PW, Cho KS, Park CK: Surgical results in pediatric moyamoya disease: angiographic revascularization and the clinical results. Clin Neurol Neuro-surg 109:125–131, 2007



21. Kim JE, Oh CW, Kwon OK, Park SQ, Kim SE, Kim YK: Tran-sient hyperperfusion after superficial temporal artery/middle cerebral artery bypass surgery as a possible cause of postop-erative transient neurological deterioration. Cerebrovasc Dis 25:580–586, 2008

22. Kim SK, Wang KC, Kim IO, Lee DS, Cho BK: Combined en-cephaloduroarteriosynangiosis and bifrontal encephalo galeo (peri osteal)synangiosis in pediatric moyamoya disease. Neu-rosurgery 50:88–96, 2002

23. Komotar RJ, Starke RM, Otten ML, Merkow MB, Garrett MC, Marshall RS, et al: The role of indirect extracranial-in-tracranial bypass in the treatment of symptomatic intracranial atheroocclusive disease. Clinical article. J Neurosurg 110: 896–904, 2009

24. Matsushima T, Fujiwara S, Nagata S, Fujii K, Fukui M, Hasuo K: Reoperation for moyamoya disease refractory to enceph-alo-duro-arterio-synangiosis. Acta Neurochir (Wien) 107: 129–132, 1990

25. Matsushima T, Fujiwara S, Nagata S, Fujii K, Fukui M, Kita-mura K, et al: Surgical treatment for paediatric patients with moyamoya disease by indirect revascularization procedures (EDAS, EMS, EMAS). Acta Neurochir (Wien) 98:135–140, 1989

26. Matsushima T, Inoue T, Ikezaki K, Matsukado K, Natori Y, Inamura T, et al: Multiple combined indirect procedure for the surgical treatment of children with moyamoya disease. A comparison with single indirect anastomosis and direct anas-tomosis. Neurosurg Focus 5(5):e4, 1998

27. Matsushima Y: Failure of encephalo-duro-arterio-synangiosis procedure in moyamoya disease. Pediatr Neurosci 12:326–327, 1985–1986

28. Matsushima Y, Fukai N, Tanaka K, Tsuruoka S, Inaba Y, Aoy-agi M, et al: A new surgical treatment of moyamoya disease in children: a preliminary report. Surg Neurol 15:313–320, 1981

29. Matsushima Y, Suzuki R, Ohno K, Masaoka H, Wakabayashi S, Maehara T: Angiographic revascularization of the brain after encephaloduroarteriosynangiosis: a case report. Neuro-surgery 21:928–934, 1987

30. Mesiwala AH, Sviri G, Fatemi N, Britz GW, Newell DW: Long-term outcome of superficial temporal artery-middle ce-rebral artery bypass for patients with moyamoya disease in the US. Neurosurg Focus 24(2):E15, 2008

31. Miyamoto S, Kikuchi H, Karasawa J, Nagata I, Yamazoe N, Akiyama Y: Pitfalls in the surgical treatment of moyamoya disease. Operative techniques for refractory cases. J Neuro-surg 68:537–543, 1988

32. Mizoi K, Kayama T, Yoshimoto T, Nagamine Y: Indirect re-vascularization for moyamoya disease: is there a beneficial ef-fect for adult patients? Surg Neurol 45:541–549, 1996

33. Ross IB, Shevell MI, Montes JL, Rosenblatt B, Watters GV, Farmer JP, et al: Encephaloduroarteriosynangiosis (EDAS)

for the treatment of childhood moyamoya disease. Pediatr Neurol 10:199–204, 1994

34. Sainte-Rose C, Oliveira R, Puget S, Beni-Adani L, Boddaert N, Thorne J, et al: Multiple bur hole surgery for the treatment of moyamoya disease in children. J Neurosurg 105 (6 Sup-pl):437–443, 2006

35. Scott RM, Smith JL, Robertson RL, Madsen JR, Soriano SG, Rockoff MA: Long-term outcome in children with moyamoya syndrome after cranial revascularization by pial synangiosis. J Neurosurg 100 (2 Suppl Pediatrics):142–149, 2004

36. Starke RM, Komotar RJ, Connolly ES: Optimal surgical treat-ment for moyamoya disease in adults: direct versus indirect bypass. Neurosurg Focus 26(4):E8, 2009

37. Suzuki J, Kodama N: Moyamoya disease—a review. Stroke 14:104–109, 1983

38. Suzuki Y, Negoro M, Shibuya M, Yoshida J, Negoro T, Wata-nabe K: Surgical treatment for pediatric moyamoya disease: use of the superficial temporal artery for both areas supplied by the anterior and middle cerebral arteries. Neurosurgery 40:324–330, 1997

39. Touho H, Iseda T: [Strategy for vascular reconstruction for failed indirect anastomosis in adult Moyamoya disease—a case report]. No Shinkei Geka 31:997–1001, 2003 (Jpn)

40. Touho H, Karasawa J, Ohnishi H, Yamada K, Shibamoto K: Surgical reconstruction of failed indirect anastomosis in childhood Moyamoya disease. Neurosurgery 32:935–940, 1993

41. Touho H, Karasawa J, Tenjin H, Ueda S: Omental transplanta-tion using a superficial temporal artery previously used for encephaloduroarteriosynangiosis. Surg Neurol 45:550–559, 1996

42. Tu YK, Liu HM, Kuo MF, Wang PJ, Hung CC: Combined en-cephalo-arterio-synangiosis and encephalo-myo-synangiosis in the treatment of moyamoya disease. Clin Neurol Neuro-surg 99 (Suppl 2):S118–S122, 1997

43. Veeravagu A, Guzman R, Patil CG, Hou LC, Lee M, Stein-berg GK: Moyamoya disease in pediatric patients: outcomes of neurosurgical interventions. Neurosurg Focus 24(2):E16, 2008

44. Zipfel GJ, Fox DJ Jr, Rivet DJ: Moyamoya disease in adults: the role of cerebral revascularization. Skull Base 15:27–41, 2005

Manuscript submitted November 16, 2010.Accepted March 21, 2011Please include this information when citing this paper: published

online April 29, 2011; DOI: 10.3171/2011.3.JNS101908.Address correspondence to: Gary K. Steinberg, M.D., Ph.D.,

R281, Department of Neurosurgery, Stanford University School of Medicine, 300 Pasteur Drive, Stanford, California 94305-5327. email: [email protected].

outcome of repeat revascularization surgery for moyamoya...

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