OBJECTIVE: Revascularization is an effective treatment for the ischemic symptom of moyamoya disease. Indirect revascularization is also effective. Magnetic resonance angiography (MRA) has the ability for collateral formation that is equivalent to conventional angiography. This study analyzed the results of indirect revascularization by MRA.0aMETHODS: A total of 25 patients underwent bilateral EDAS for the management of moyamoya disease. All patients underwent MRA after surgery more than 24 months later. The collateral formation was graded as Good, Fair, and Poor. The clinical outcome was assessed as Excellent, Good, Fair, and Poor.0aRESULTS: Good collateral formation was 32 sides of the EDAS, and fair was 18. An excellent clinical outcome was obtained in 15 patients, Good in 8, Fair in 1, and Poor in 1. There was a significant correlation between the preoperative symptom, gender, and the clinical outcome.0aCONCLUSION: In the management of ischemic moyamoya disease, indirect revascularization has been the golden standard with remarkably low morbidity and mortality. Moreover, and MRA can replace conventional angiography in the follow-up of moyamoya patients.ope

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KOR J CEREBROVASCULAR SURGERYSeptember 2OO7 Vol. 9 No 3, page 188-92188IntroductionNatural history of moyamoya disease has been known to beprogressive repeated ischemic symptom of young age andhemorrhagic symptom of adult.2) Revascularization is the maintreatment, with both direct and indirect revascularization.They increase blood flow and perfusion of cerebral cortex anddecrease moyamoya vessels. Finally ischemic symptomdecreases. Its angiogenesis of revascularization has beenstudied, by conventional angiography. However, conventionalangiography needs tolerance of patient and puncture of largeartery, so risk of complication has existed. The quality ofMagnetic Resonance Angiography (MRA) has been improvedand study for angiogenesis of revascularization by MRA hasbeen reported.4) Some studies have been reported regarding thevalue of MRA in diagnosis and follow up of moyamoyadisease.6) But most of them had some limitations, such assmall cases or short term follow-up period. The aim of thisstudy is to show that MRA is useful for evaluation ofpostoperative result of indirect revascularization in moyamoyadisease.Patients and MethodsPatientsFrom January 2002 to January 2005, patients who werediagnosed as moyamoya disease and underwent indirectanastomosis, encephaloduroarteriosynangiosis(EDAS), werereviewed. Preoperative cerebral infarction was excluded forremoval of influence of parenchymal structural changes onLong Term Magnetic Resonance Angiography Follow-up in Moyamoya DiseaseDepartment of Neurosurgery1 and Pediatric Neurosurgery2, Severance Children’s Hospital, Brain Korea 21 project for medical science, Yonsei University College of Medicine, Seoul, KoreaNam Kyu You, MD1∙Kyu Won Shim, MD2∙Young Seok Park, MD2Jung Hee Kim, MD2∙Dong Seok Kim, MD2∙Joong Uhn Choi, MD2ABSTRACTObjective : Revascularization is an effective treatment for the ischemic symptom of moyamoya disease. Indirect revascularization is alsoeffective. Magnetic resonance angiography (MRA) has the ability for collateral formation that is equivalent to conventional angiography.This study analyzed the results of indirect revascularization by MRA. Methods : A total of 25 patients underwent bilateral EDAS for themanagement of moyamoya disease. All patients underwent MRA after surgery more than 24 months later. The collateral formation wasgraded as Good, Fair, and Poor. The clinical outcome was assessed as Excellent, Good, Fair, and Poor. Results : Good collateral formationwas 32 sides of the EDAS, and fair was 18. An excellent clinical outcome was obtained in 15 patients, Good in 8, Fair in 1, and Poor in 1.There was a significant correlation between the preoperative symptom, gender, and the clinical outcome. Conclusion : In the management ofischemic moyamoya disease, indirect revascularization has been the golden standard with remarkably low morbidity and mortality.Moreover, and MRA can replace conventional angiography in the follow-up of moyamoya patients. (Kor J Cerebrovascular Surgery9(3):188-92, 2007)KEY WORDS : Moyamoya∙MRA∙Revascularization논문접수일 : 2007년 07월 24일심사완료일 : 2007년 08월 16일교신저자 : Dong-Seok Kim, MD, PhD, Department of Neurosurgeryand Pediatric Neurosurger, Severance Children’s Hospital, Yonsei University College of Medicine, 134 Shinchon-dong, Seoeaemun-gu, Seoul, Korea전화 : (02) 2228-2150�전송 : (02) 393-9979E-mail : dskim33@yuhs.accollateral vessel formation. All patients had been followedup at least 24 months. Preoperative Suzuki grade waschecked by conventional angiography and MRA. Techniques of encephaloduroarteriosynangiosis(EDAS)Our modality of indirect revascularization was EDAS.Surgery was performed according to the Suzuki stage andMatsushima grade. If the patient needed bilateralrevascularization, surgery was continued after 4 or 6 weeks.With endotracheal general anesthesia, patients were placed ona table in supine position. Head was rotated to contralateralside to operation side. Superficial temporal artery (STA) waspalpated and hair was shaved along the course of STA withabout 2cm width. Ultrasonic Doppler might be used in somecases. Skin was incised along the STA path, from bifurcationof frontal and temporal branches. For protection of STA, bluntdissection between subcutaneous and galeal layer exposedSTA and its branches. Bleeding control was done with verycareful attention. Using the monopolar coagulator a galeal flapwhich contained STA was made. It was preserved duringcraniotomy. One burr hole was drilled at superior hinge pointof the flap, than a craniotome drill made round shaped boneflap. Dura was incised straightly parallel to the meningealarteries. Dura was split in inner and outer layer. Inner duralayer was excised, and then the galeal flap was sutured toouter dura margin. Bone flap was ground at flap insertionpoints, and fixed on the cranium. Drainage catheter wasplaced on the skull and wound was closed layer by layer.MRI follow up and outcome evaluationAll patients were followed at out-patient clinic. Collateralgrade was assessed according to the collateral vesselformation and visualization; Good: collateral vessels supplied more then two-thirds ofthe MCA territory. Fair: between one-thirds and two-thirds of the MCAterritory. Poor: less than one-third of the MCA territory.Clinical outcome was categorized as follows; Excellent: Patients has been free from symptoms. Good: Decreased frequency of symptoms. Fair: Symptoms were slightly improved or persistent sameas preoperative status. Poor: Symptoms were aggravated. Frequency or intensityincreased. Statistical analysisIndependent T-test and ANOVA test were used forcomparison between preoperative clinical symptom,preoperative angiographic grading, and clinical outcome.Multivariate regression analysis was performed to analyzethe prognostic impact of the following parameters onoutcome grade: age, gender, and preoperative grade. Thelevel of significance was p<0.05.ResultsTotal 25 patients all underwent bilateral EDAS and total50 EDAS were done. Male patients were 11 and female were14. Mean age on operation is 8.5 years old (range from 4 to15 years old). Mean follow up period is 35.8 months afterlast operation (range from 24 to 60 months). Otherpreoperative data was listed in Table 1. There was nosignificant difference in sex, age, preoperative symptom, andpreoperative angiographic grading. Collateral vessels were identified at final MRA(Fig. 1).Good collateral revascularization was observed in 32 casesof EDAS. Fair was 18 cases. There were no poor collaterals. Postoperative outcome was like followings. Excellentoutcome was observed in 15 patients(60%). Eight patientshad bilateral good collaterals and others had mixed grade ofNam Kyu You∙Kyu Won Shim∙Jung Hee Kim∙Young Seok Park∙Dong Seok Kim∙Joong Uhn Choi189Kor J Cerebrovascular Surgery 9(3):188-92, 2007Table 1. Clinical data of 25 patients who underwent bilateralEADS due to moyamoya diseaseAge at operation 8.52 (4~15) years oldGenderMale 11Female 14Clinical SymptomsTIAa 06Frequent TIA 19Angiographic gradingbII 07III 34IV 09a TIA : Transient ischemic attackb Angiographic stage was evaluated according to the methodof Suzuki and Kodama.17) Grade I, V and VI were not detected inthis study good and fair collaterals. Good outcome patients were8(32%). Bilateral good collateral were 2, and bilateral faircollateral were 2. Others had that one side was good andother side was fair. There was 1 fair grade patients who hadright side good collateral and left side fair collateral(4%).Only one patient had poor outcome, whose collaterals werebilateral fair grades(4%)(Table 2). Collateral formation wasassessed with preoperative angiographic grades and clinicalsymptoms(Table 3). There was no statistical significance ineach grade.Statistically analysis showed significant correlationbetween preoperative symptom and postoperative outcome(Table 4). Other factors did not show significance, but sexand collateral grades had significance(p<0.05). Femalepatients showed more favorable clinical outcome.DiscussionIndirect revascularization is one of effective methods fortreatment of ischemic symptom of Moyamoya disease.5)12)Indirect revascularization is easier and simpler procedure thandirect anastomosis which is more appropriate if possible.11) InLong Term Magnetic Resonance Angiography Follow-up in Moyamoya Disease190 Kor J Cerebrovascular Surgery 9(3):188-92, 2007Fig. 1. Collateral grading on MRA. (A) Good collateral formation (B) Fair collateral (C) Poor collateral.Table 2. Clinical outcome of 25 patients and collateral vesselformation grading by MRAClinical outcome N MRA collaterals GradeExcellent 15Good 23Fair 7Good 8Good 8Fair 8Fiar 1Good 1Fair 1Poor 1Good 0Fair 2Total 25 50Table 3. Collateral grade and preoperative Suzuki grade andpreoperative clinical symptomsCollateral gradeGood Fair PoorSuzuki GradeII 04 03 0III 23 11 0IV 06 03 0Clinical SymptomsTIA 11 01 0Frequent TIA 22 16 0Table 4. Multivariate regression analysis for outcome grade in patients who underwent EDASVariables Regression coefficient Standard error PSex 0.539 0.249 *0.006*Age 0.021 0.187 0.575Matsushima grade 0.171 0.038 0.494Suzuki grade -0.299- 0.178 0.101Collateral grade 0.621 0.202 *0.003** statistically significant (p<0.05).our study, improvement of symptom was observed in 92% ofpatients. This result is same or superior to previous reportedstudies about result of indirect or direct revascularization ofMoyamoya disease.8)13) It also has less complicationcompared with direct one. Mild headache and nauseaoccurred in some cases, but it disappeared soon. There wasno morbidity and mortality in our study. Postoperative image study is essential to evaluate theresult and outcome of moyamoya surgery. MRA has becomethe choice of study for follow up and to check the result ofrevascularization. In this study, collateral vessel formationon postoperative MRA showed statistically significantcorrelation with clinical outcome. Development of collateralhad been resulted in blood flow increase, and finallyperfusion of cerebral hemisphere increased. Other factors didnot have any statistical significance except gender. Femalepatients had more favorable outcome than male. No studyabout gender which was affecting the disease progressionand severity of moyamoya disease was found. Further studymay be needed. About other prognostic factor, recently astudy reported that postoperative blood flow on SPECT isstatistically prediction factor of clinical outcome.16)MRA has ability to evaluate the collateral formation. In thepast, MR study had been considered as an additional andsupportive tool to angiography.1)14)18) Conventional angiographyhas been used as a golden tool of evaluation of cerebralvascular structure in moyamoya disease. But, patients wereexposed to radiation and had to bear the pain duringexamination. Technology has improved and MR imagebecame more detailed. MRA have many advantages overconventional angiography. There is no radiation exposureand pain. MR study is possible to evaluate brain parenchymaand vascular structures at the same time. Younger patientsmay need sedation or general anesthesia during angiography.Repeated anesthesia might increase risk of ischemic attackand cerebral infarction in moyamoya disease.9) Usefulness ofMRA that was compared with conventional angiography hadbeen proved by several authors.3)7)15) Fine moyamoya vesselscould be visualized at the high resolution MR image, andalso collateral vessels from implanted STA. MR Perfusionimage has been available and it may substitute theconventional SPECT images.10)The limitation of this study is retrospective and relativelysmall patients group. With more cases, the correlationbetween development of collateral vessels and symptomimprovement will be studied.ConclusionsIn the management of ischemic moyamoya disease,indirect revascularization has been a golden standard withremarkably low morbidity and mortality. However thepatient has been followed with conventional angiographywith comparable risk. Fortunately the techniques of MRAhave been remarkably improved to see fine collateralvessels. Therefore we suggest that the MRA can replace theconventional angiography in follow-up of moyamoyapatient.REFERENCES01) Aoki T, Matsuzawa H, Houkin K, Kamiyama H, Abe H,Miyasaka K, and Saito H, Usefulness and limitation of MRimaging and MR angiography in diagnosis of juvenilemoyamoya disease. No Shinkei Geka, 1993. 21(4):p.305-1102) Choi JU, Kim DS, Kim EY, and Lee KC, Natural history ofmoyamoya disease: comparison of activity of daily living insurgery and non surgery groups. Clin Neurol Neurosurg,1997. 99 Suppl 2:p.S11-803) Christopoulos G, Ziegler V, Coblenz G, Wedell E, GriewingB, and Schmitt R, [Clinical symptoms and diagnostic imagingin moyamoya disease]. Rontgenpraxis, 2003. 55(1):p.39-4504) Houkin K, Nakayama N, Kuroda S, Ishikawa T, and NonakaT, How does angiogenesis develop in pediatric moyamoyadisease after surgery? A prospective study with MRangiography. Childs Nerv Syst, 2004. 20(10):p.734-4105) Isono M, Ishii K, Kamida T, Inoue R, Fujiki M, and KobayashiH, Long-term outcomes of pediatric moyamoya disease treatedby encephalo-duro-arterio-synangiosis. Pediatr Neurosurg,2002. 36(1):p.14-2106) Kagawa R, Okada Y, Moritake K, and Takamura M, Magneticresonance angiography demonstrating adult moyamoyadisease progressing from unilateral to bilateral involvement--case report. Neurol Med Chir (Tokyo), 2004. 44(4):p.183-607) Kikuchi M, Hayakawa H, Takahashi I, Nagao K, Hoshino H,Kudo S, and Ito K, Moyamoya disease in three siblings--follow-up study with magnetic resonance angiography (MRA).Neuropediatrics, 1995. 26(1):p.33-608) Kim DS, Kang SG, Yoo DS, Huh PW, Cho KS, and Park CK,Surgical results in pediatric moyamoya disease: angiographicrevascularization and the clinical results. 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Neurosurgery, 1992. 31(3):p.401-512) Nakashima H, Meguro T, Kawada S, Hirotsune N, andOhmoto T, Long-term results of surgically treated moyamoyadisease. Clin Neurol Neurosurg, 1997. 99 Suppl 2:p.S156-6113) Park JH, Yang SY, Chung YN, Kim JE, Kim SK, Han DH, andCho BK, Modified encephaloduroarteriosynangiosis withbifrontal encephalogaleoperiosteal synangiosis for thetreatment of pediatric moyamoya disease. Technical note. JNeurosurg, 2007. 106(3 Suppl):p.237-4214) Pereira PL, Farnsworth CT, Duda SH, Rose M, Reinbold WD,and Claussen CD, Pediatric moyamoya syndrome: follow-upstudy with MR angiography. AJR Am J Roentgenol, 1996.167(2):p.526-815) Saeki N, Silva MN, Kubota M, Takanashi J, Sugita K, NakazakiS, and Yamaura A, Comparative performance of magneticresonance angiography and conventional angiography inmoyamoya disease. 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Long term magnetic Resonance Angiography follow-up in moyamoya disease

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Long term magnetic Resonance Angiography follow-up in moyamoya disease

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