revue neurologique 171 (2015) 31–44

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Neurovascular disease

Surgical management of Moyamoya disease and syndrome: Current concepts and personal experience Prise en charge chirurgicale de la maladie et du syndrome de Moyamoya : concepts actuels et expe´rience personnelle L. Thines a,*,g, G. Petyt b,g, P. Aguettaz c,g, M. Bodenant d,g,h, F.-X. Himpens e,g, H. Lenci f,g, H. Henon d,g,h, C. Gauthier e,g, C. Hossein-Foucher b,g, C. Cordonnier d,g,h, J.-P. Lejeune a,g a

Department of neurosurgery, poˆle des neurosciences et de l’appareil locomoteur, universite´ Lille Nord de France, hoˆpital Roger-Salengro, Lille University Hospital, avenue E´mile-Laine, 59037 Lille cedex, France b Department of nuclear medicine, universite´ Lille Nord de France, hoˆpital Roger-Salengro, Lille University Hospital, avenue E´mile-Laine, 59037 Lille cedex, France c Department of neuroradiology, universite´ Lille Nord de France, hoˆpital Roger-Salengro, Lille University Hospital, avenue E´mile-Laine, 59037 Lille cedex, France d Department of neurology, universite´ Lille Nord de France, hoˆpital Roger-Salengro, Lille University Hospital, avenue E´mile-Laine, 59037 Lille cedex, France e Department of neurosonology, universite´ Lille Nord de France, hoˆpital Roger-Salengro, Lille University Hospital, avenue E´mile-Laine, 59037 Lille cedex, France f Department of anaesthesia, universite´ Lille Nord de France, hoˆpital Roger-Salengro, Lille University Hospital, avenue E´mile-Laine, 59037 Lille cedex, France g Universite´ Lille Nord de France, 1, rue Lefe`vre, 59000 Lille, France h ´ Equipe d’accueil EA 1046, de´partement de pharmacologie me´dicale, 1, place de Verdun, 59045 Lille cedex, France

info article

abstract

Article history:

In this focus, we review, in the light of the recent literature, the modalities and indications of

Received 20 November 2013

surgical cerebral revascularization for Moyamoya (MM) disease or syndrome. We also report

Received in revised form

our experience in the surgical management of adult MM. In symptomatic forms, with

5 June 2014

presence of severe disturbances of perfusion or cerebrovascular reactivity on multimodal

Accepted 29 August 2014

imaging work-up, the risks of recurrent ischemic or hemorrhagic stroke is high (respectively

Available online 30 December 2014

10–13%/yr and 2–7%/yr). The objective of treatment is to augment cerebral perfusion (in ischemic forms) or to reduce lenticulo-striate neovessel overload (in hemorrhagic forms), by

Keywords:

initiating the development of a cortical neovascularization and/or by directly increasing

Moyamoya

cerebral blood flow. The risk of immediate postoperative death or stroke is similar between

Surgical treatment

indirect and direct or combined techniques and respectively 0–0.5% and 3–6%, provided a

* Corresponding author. E-mail address: [email protected] (L. Thines). http://dx.doi.org/10.1016/j.neurol.2014.08.007 0035-3787/# 2014 Elsevier Masson SAS. All rights reserved.

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revue neurologique 171 (2015) 31–44

Encephalo-synangiosis

strict perioperative anesthetic management is applied (normocapnia, normoxia and

Extracranial-intracranial bypass

controlled hypertension). Indirect techniques (i.e. encephalo-duro-arterio-myo-periosteo-

Outcome

synangiosis or multiple burr-holes) are technically easy, allow wide cortical revascularization and are very efficient in children: absence of clinical recurrence in more than 95% of

Mots cle´s :

cases and presence of a good neovascularization in 83%. However, their effect is delayed for

Moyamoya

several months, the impact on the hemorrhagic risk is moderate and the global response is

Chirurgie

uncertain in adults. Direct (superficial temporal artery to middle cerebral artery bypass) or

Encephalo-synangiose

combined techniques improve cerebral blood flow immediately and significantly. They are

Pontage extracranien-intracranien

associated with a higher rate of stroke-free survival at 5 years (95% vs 85%). A recent

Pronostic

randomized study has proven that they could reduce the hemorrhagic risk by 2- to 3-fold in comparison with conservative treatment alone. However, their feasibility in children is limited by the very small size of vessels. We present also our results in the surgical management of 12 adult MM patients (mean age 41.3, sex ratio = 1) operated between 2009 and 2014 (14 revascularization procedures: EDAMS 2, multiple burr-holes 1, combined revascularization procedures 11). MM types according to clinical presentation were the following: ischemic 8, hemorrhagic 2, combined 2. All patients were recently symptomatic, with recurrent ischemic/hemorrhagic events (2/3) or crescendo neurological deficit (1/3) in association with severe alterations of cerebral blood flow. Mean clinical and radiological follow-up was 22 months. Postoperative mRS at 6 months was improved or stable in 92%. None of the patients suffered recurring stroke. In conclusion, surgical treatment should be discussed quickly in symptomatic forms of MM (progressive or recurring) because of their poor outcome. Indirect techniques are favored in pediatric patients due to their simplicity and good clinical results. Direct, or preferentially combined techniques would be more effective in adult patients to prevent the recurrence of ischemic or hemorrhagic stroke. # 2014 Elsevier Masson SAS. All rights reserved.

r e´ s u m e´ Dans cette mise au point, nous revoyons, a` la lumie`re de la litte´rature actuelle, les modalite´s et indications du traitement chirurgical par revascularisation ce´re´brale dans la prise en charge de la maladie ou le syndrome de Moyamoya (MM). Nous rapportons e´galement notre expe´rience dans la prise en charge de cette maladie chez l’adulte. En effet, dans les formes symptomatiques, qui comportent en imagerie multimodale la pre´sence d’alte´rations de perfusion ou de la re´serve ce´re´bro-vasculaire, le risque de re´cidive ische´mique ou he´morragique est e´leve´ (respectivement 10–13 %/an et 2–7 %/an). L’objectif du traitement est d’augmenter la perfusion ce´re´brale (formes ische´miques) ou de re´duire la sollicitation des ne´ovaisseaux lenticulo-strie´s (formes he´morragiques), en favorisant le de´veloppement secondaire d’une ne´ovascularisation corticale et/ou en augmentant directement le de´bit dans le re´seau ce´re´bral. Le risque de de´ce`s ou d’AVC lie´ a` la procedure est identique pour les techniques indirectes et directes ou combine´es et respectivement de l’ordre de 0–0,5 % et 3–6 %, pourvu qu’un strict monitorage anesthe´sique pe´riope´ratoire soit applique´ (normocapnie, normoxie, hypertension controˆle´e). Les techniques de revascularisation indirecte (ence´phalo-duro-arte´rio-myo-perioste´o-synangioses, trous de tre´pan multiples) sont techniquement simples, permettent de revasculariser une large surface corticale et sont tre`s efficaces chez l’enfant avec l’absence de re´cidive clinique dans plus de 95 % des cas et le de´veloppement d’une ne´oangiogene`se satisfaisante dans 83 % des cas. Leur be´ne´fice est en revanche retarde´ de plusieurs mois, a peu d’impact sur le risque he´morragique et est plus incertain chez l’adulte. Les techniques de revascularisation directe (anastomose temporo- ou occipito-sylvienne) ou combine´e (directe + indirecte) ame´liorent imme´diatement et de fac¸on importante la perfusion ce´re´brale. Elles ont un meilleur taux de survie sans nouvel AVC a` 5 ans (95 % contre 85 %). Une e´tude randomise´e re´cente a prouve´ qu’elles re´duiraient le risque he´morragique d’un facteur 2 a` 3 en comparaison au traitement me´dical simple. Elles sont en revanche plus difficiles techniquement chez l’enfant (faible calibre arte´riel). Nous pre´sentons e´galement nos re´sultats dans la prise en charge de 12 adultes atteints de MM (aˆge moyen 41,3 ans, sexe ratio = 1) et ope´re´s entre 2009 et 2014 (14 proce´dures de revascularisation : EDAMS 2, trous de tre´pans multiples 1, proce´dures combine´es 11). Les formes de MM e´tait : ische´mique 8, he´morragique 2, combine´ 2. Tous les patients avaient re´cemment pre´sente´ des e´ve´nements re´currents ische´miques/he´morragiques (2/3) ou un de´ficit neurologique crescendo (1/3) en association avec des alte´rations se´ve`res de la perfusion ce´re´brale. Le suivi

revue neurologique 171 (2015) 31–44

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clinique et radiologique moyen e´taient de 22 mois. Le mRS postope´ratoire a` 6 mois e´tait ame´liore´ ou stable dans 92 % des cas. Aucun des patients n’a pre´sente´ de re´cidive d’AVC. En conclusion, un traitement chirurgical doit eˆtre discute´ rapidement dans les formes symptomatiques (progressives ou re´currentes) de MM du fait de leur risque e´volutif. Les techniques indirectes sont privile´gie´es chez l’enfant du fait de leur simplicite´ et de leurs bons re´sultats cliniques. Les techniques directes et surtout combine´es seraient plus efficaces chez l’adulte pour pre´venir le risque de re´currence ische´mique ou he´morragique. # 2014 Elsevier Masson SAS. Tous droits re´serve´s.

1. Introduction: epidemiology, definition and natural history of the disease Moyamoya (MM) disease is a rare, little known but also probably underdiagnosed vasculopathy in Western countries. Due to the lack of population-based studies of MM disease in Europe, the epidemiology over the continent is not well understood. By comparison, the incidence of the disease (per 100.000 person years) varies considerably between Japan (0.35 to 0.94) and Western countries as the USA (0.05 to 0.17) [1]. In a recent survey of paediatric MM disease in France, the estimated incidence was 0.065 per 100.000 person years [2]. In our own region of ‘‘Nord-pas-de-Calais’’ covering an area of about 4 million people, the recent estimated incidence of adult MM disease during a five-year period (2009–2014) was 0.16 per 100.000 person years. MM phenomenon is the angiographic translation of the incompetency or inability of the circle of Willis to respond to the progressive occlusion of the main arteries at the base of the brain and to compensate for the related haemodynamic deprivation. In reaction to chronic hypoperfusion of the involved hemisphere(s), secondary growth of pre-existing vascular networks or development of supporting collateral neovessels is induced, initially from the lenticulo-striates arteries at the basal ganglia (so-called ‘‘Moyamoya’’ vessels, Japanese equivalent for ‘‘puff of smoke-like’’ diffuse neovascularisation) and then from pial cortico-cortical anastomoses (between anterior, middle, posterior cerebral arteries territories) or leptomeningeal connections (from external carotid artery (ECA) branches of the scalp or meninges) at the brain surface. MM disease is strictly defined by the progressive and idiopathic steno-occlusion of the internal carotid artery (ICA) terminations at the base of the brain. In the typical form, it leads to the occlusion of one (probable MM disease) or both (definite MM disease) ICA but the disease can also frequently extend to the initial segment of the middle (MCA) and/or anterior (ACA) cerebral arteries and rarely to the posterior cerebral artery (PCA). The disease is chronic and progressive, and shifting from a unilateral to a bilateral disease (in one third of cases) and increase in Suzuki’s stage (Table 1) [3] overtime are very common [4–6]. MM-like disease (or pseudoMM disease) is an incomplete form of the disease characterized by the development of MM phenomenon in conjunction with the focal and often unilateral steno-occlusion of the initial segment of the MCA. In the syndromic form (MM syndrome), MM features are seen in association with an identified etiology (i.e. cranial irradiation) or underlying

disease (i.e. atherosclerosis, neurofibromatosis type I, Down’s syndrome, sickle cell disease, homocisteinemia. . .) [7,8]. In many patients, those adaptative mechanisms to chronic hypoperfusion are unfortunately insufficient to prevent the occurrence of progressive neurological deterioration or recurrent ischemic strokes. Furthermore, those fragile neovessels can themselves be responsible for life threatening haemorrhagic complications (intracerebral, intraventricular or subarachnoid haemorrhages) by direct or through pseudoaneurysms rupture [9–11]. Because of the rarity of the disease, data about the natural history of the disease are derived from retrospective and prospective cohorts of small size and should be analyzed cautiously. It should be noted that asymptomatic patients, among whom 30% have silent infarctions or cerebral blood flow disturbances at diagnosis, may also carry a significant risk of developing new deficits with an annual risk of 3.2% per year [12]. Regarding symptomatic MM patients, a high annual risk of recurrent ischemic stroke (about 10–13% per year) is observed and conservatively treated adults face a 5-year risk of recurrence ranging from 40 to 65% in total and of 82% in bilateral forms. This menace is maximal during the first 2 years after diagnosis (roughly 20%), thus pleading for rapid management [9,13–17]. Among patients with haemorrhagic presentation (15–20% of patients in Western countries and 40% in Asia), around 30–60% of them will experience rebleeding with an annual risk of 2 to 7% per year. Because of the conjunction of pre-existent impaired cerebral vascularization with acute intracranial hypertension due to intracranial haemorrhage, the mortality rate is high, about 18% for an inaugural bleeding and then ranging from 30 to 80% for a recurrence [7,9–11,18–20]. Up to now, no targeted medical therapy has been proved efficient for the management of symptomatic patients. However, aspirin used is recommended in non-haemorrhagic subtype hoping to prevent ischemic events due to emboli from

Table 1 – Suzuki and Takaku’s grading system. Grade

Definition

I II III

Narrowing of ICA apex Initiation of Moyamoya collaterals Progressive ICA stenosis with intensification of Moyamoya-associated collaterals Development of ECA collaterals Intensification of ECA collaterals and reduction of Moyamoya-associated vessels Total occlusion of ICA and disappearance of Moyamoya-associated collaterals

IV V VI

ICA: internal carotid artery; ECA: external carotid artery.

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revue neurologique 171 (2015) 31–44

microthrombi formation at sites of arterial stenosis. Calcium channel blockers might also be prescribed in children to reduce the frequency of TIAs or intensity of headaches [21]. Hence, when the disease is clinically aggressive, individualized surgical strategies of revascularization are required to attempt to reverse or, at least, stabilize their course in order to obtain patients’ outcome improvement [7–9]. We present in this article the current surgical techniques available for cerebral revascularization in this context and present our experience in the surgical management of adult MM disease.

2. Preoperative work-up, selection of patients and postoperative follow-up The management of MM disease comes within the competency of a multidisciplinary neurovascular team that will look for the relevant criteria guiding the triage of patients between conservative or surgical treatment. Multimodal imaging work-up is mandatory to exhaustively document the cerebral lesions, the vascular anatomy and the hemodynamic features of the disease [8,9,21,22]. Symptomatic or silent infarctions and haemorrhages are evidenced by the use of cerebral magnetic resonance imaging (MRI). The angioarchitecture of the disease is demonstrated by the use of MR angiography (MRA) and 4 vessels + selective external carotid artery territories digital subtraction angiography (DSA). Hemodynamic features are also very important to take into consideration in the management decision-making process, together with clinical symptoms. Different techniques are nowadays available to assess blood flow in the involved hemisphere(s) as PET, SPECT, MR and CT perfusion or duplex transcranial Doppler (TCD) and could be used in various combinations. The severity of cerebral hypoperfusion can be evaluated during SPECT, MR perfusion, CT perfusion or TCD by measuring the cerebrovascular reactivity (CVR = residual capacity of cerebral arteries to dilate in order to adapt brain perfusion) during a CO2 or acetazolamide challenge. PET scanning is the reference examination to evaluate the importance of cerebral hypoperfusion by the measurement of the oxygen extraction fraction (OEF). Absence of CVR (or decreased CVR = steal phenomenon) or compensatory increased in OEF (absolute value > 0,44) is a marker of ‘‘misery perfusion’’ and is associated with a 7 to 8-fold absolute risk and 17 to 23% annual risk of ipsilateral recurrent stroke in ICA/MCA occlusions [23–25]. Decreased perfusion, maximal vasodilatation and impaired CVR/increased OEF are significantly correlated with the occurrence of ischemic symptoms (stroke + TIAs) in the MM population [26]. Hence, typical patients that could benefit the most from cerebral revascularization are usually symptomatic, with recurrent ischemic/haemorrhagic events, progressive cognitive deterioration (particularly frequent in children) or crescendo neurological deficit in association with severe disturbances of cerebral blood flow on hemodynamical imaging. Similarly to other teams [9,21,27–29], we apply the following criteria in the selection of our adult MM patients for cerebral revascularization:  functional status: patient is able to perform activities of daily living (mRS  3);

 neurological presentation: patient has recurrent (sensorymotor, speech, visual or gait disturbance) or progressive (crescendo focal deficit or global cognitive decline) neurological deficit(s) due to repeated TIAs, cerebral infarctions, cerebral haemorrhages or severe chronic hypoperfusion. The procedure is delayed for at least 6 weeks after the last cerebral infarction/haemorrhage;  radiological features: the angiographic stage of the disease is Suzuki’s stage II to IV. MRI documents cerebral lesions of different ages in favor of the progressive and recurring nature of the disease;  hemodynamic status: dedicated imaging studies (SPECT and TCD with Diamox1 challenge) show at least significant hypoperfusion of the involve hemisphere or corresponding cortical area. The absence of cerebrovascular reactivity or the presence of a steal phenomenon is a stronger indicator of the severity of the disease, thus reinforcing the need for surgical intervention. Postoperative clinical and radiological follow-up is mandatory. It uses similar radiological imaging techniques to document the surgical (cerebral DSA, MRI) and hemodynamical (PET, SPECT, TCD) results of surgical intervention. Immediate postoperative assessment will look essentially for surgical complications (brain CT or MR) and bypass patency (if indicated) with TCD, CTA or DSA [30]. Delayed follow-up will be performed at 6 and 12 months with MRI, DSA, TCD to seek for silent stroke recurrence, development of collateral vessels or graft patency. Hemodynamic imaging techniques will be associated to study the evolution of cerebral blood flow, the improvement of CVR being usually a positive prognostic factor against stroke recurrence in those patients [31]. Because of the progressiveness of the disease, retreatment might be necessary after 10% of procedures because of the development or continuation of symptomatic hypoperfusion in certain cortical areas [32]. Hence, long-term yearly neurological follow-up is recommended and radiological assessment should give the priority to non-invasive and non-irradiating imaging techniques if the clinical course is uneventful.

3. General considerations about surgical revascularization The main objective of the treatment is to increase the cerebral blood flow in the revascularized territory in order to reduce the risk of subsequent ischemic events, which is the most frequent mode of presentation in children (2/3) but that is also relatively frequent in adults (> 1/3). Although, it has never been proven in a randomized trial, regarding the rarity of the disease, the benefice of surgery in this indication has been repeatedly supported by several prospective cases series [33–35]. Furthermore, the improvement of cerebral perfusion has been proven to also have an impact on the haemorrhagic risk related to the disease with reduction of haemorrhagic recurrences by 3 fold in relation with the decrease in hemodynamic overload on the leptomeningeal and deep anastomotic vessels by the rarefaction of MM neovascularization, induced by the optimization of brain perfusion [10,18,36–40].

revue neurologique 171 (2015) 31–44

The improvement of cerebral blood flow could be obtained immediately by connecting an artery (usually the superficial temporal artery (STA) of the scalp, a branch of the ECA) on a cortical branch of the MCA. This technique is identified as direct revascularization or extracranial-intracranial bypass. Cerebral perfusion could also be improved more slowly by using different techniques of indirect revascularization all acting by the delayed development of a cortical neovascularization (encephalo-synangiosis) [8,41]. Careful analysis of preoperative cerebral angiography (ECA, ICA, vertebro-basilar arteries) should help the neurosurgeon to detect pre-existing leptomeningeal anastomoses and to avoid interrupting them while opening the scalp or the dura-matter, therefore depriving the patient of natural pre-existing additional blood flow. All these techniques have a relatively low rate of morbi/ mortality, provided a strict perioperative anaesthetic management is applied. At the induction of anaesthesia, important variations of capnia (kept between 35 and 40 mmHg) or drop in blood pressure (mild controlled hypertension with mean arterial blood pressure around 80–90 mmHg) should be avoided, because both could be very harmful in those patients suffering of severe underlying perturbations of cerebral perfusion [21,42,43]. Patients undergoing direct revascularization procedures are operated under 75 mg of aspirin daily to reduce the risk of bypass early or delayed thrombosis. During cross clamping of the recipient cortical artery, barbiturateinduced burst suppression (reducing the cerebral metabolism of oxygen consumption) and additional moderate peroperative anticoagulation (2000 to 3000 units of non-fractioned heparin) are routinely used to minimize the risk of ischemic stroke in the bypassed territory. In older and more recent series, reporting a majority of conventional indirect procedures, namely encephalo-duro-arterio-synangiosis (EDAS), encephalo-duro-arterio-myo-synangiosis (EDAMS) and others (encephalo-galeo-periosteo-synangiosis: EGPS), perioperative (30 days) risks of death or stroke were respectively 0–0.5% and roughly 7–10% [13,14,43] with a 3–6.5% perioperative stroke risk for regular EDAS, EDAMS or EDAS + EGPS [14,16,44,45]. In recent series, reporting a majority of direct (extracranialintracranial bypass) or combined procedures (direct + indirect), perioperative (30 days) risks of death or stroke were respectively between 0–0.4% and 3.5–5.9% [28,46–48]. Surgical risk would be higher in syndromic MM patients, which would carry a perioperative stroke risk of 8.7% [28].

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extracranial pedicular grafts, as omentum majus graft [54], most of those techniques are nowadays using vascularized tissues harvested directly from the the head coverings: cranial periosteum, galea aponeurotica for the galeo- or periosteosynangiosis, temporal muscle for the encephalo-myo-synangiosis or EMS [55], superficial temporal artery with its surrounding connective cuff and dura-matter for the EDAS [56,57]. The denomination of the technique and the associated acronym depend on the combination of those tissues, the most complete being the EDAMS [58] and the encephalo-duroarterio-myo-periosteo-synangiosis or EDAMPS [53]. These techniques of synangiosis can be applied as a focal unilateral treatment by making a wide craniotomy over a large area of the parasylvian region, therefore aiming at revascularizing most of the MCA territory, or as a unilateral bifocal treatment by adding a parasagittal craniotomy and a periosteal shred (frontal encephalo-duro-arterio-(myo)-galeo or periosteo-synangiosis) over the internal surface of the hemisphere, therefore aiming at revascularizing at the same time the ACA territory. This last technique is called ribbon-EDAMS, ribbon-EDAS, EDAGS or EDAMPS [53,59,60]. Indirect method can also be applied as a multifocal bilateral treatment (one procedure) by the mean of multiple burr-holes (or multicraniostomies) through which the dura and arachnoid can be opened and a small periosteal or muscular flap introduced. These are used to revascularize both hemispheric convexities, usually in paediatric patients, with bilateral typical MM disease or syndrome [61–64].

4.2.

Technique [53,58]

4.

Indirect surgical revascularization options

The classical EDAMS procedure (Fig. 1) starts by harvesting an artery of the scalp (usually the STA). Once the artery is freed from the scalp, the temporal muscle is vertically cut, scrapped from the bone and then retracted to allow the craniotomy to be performed. The dura is opened in a leaf-like manner, paying attention not to damage the pre-existing arterial meningeal supplies, and the dural flaps are inverted onto the cortex (duro-synangiosis). Time is spent to open extensively the arachnoid over the sulci (often thick in MM patients) in order to improve the contact between the apposed tissues (temporal muscle, STA or periosteum) and the pial surface of the brain. The bone flap is fenestrated to allow the intracranial course of the pedicular grafts and eventually fixed with titanium rivets or plates before skin closure. The angiographic result that could be obtained with such a technique is demonstrated in Fig. 2. The multiple burr-holes technique is also described in Fig. 3.

4.1.

Principles [9,49–53]

4.3.

The underlying principle of this type of revascularization is easy: to apply an autologous vascularized graft on the hypoperfused cortical surface through an opening of the head coverings to induce adherences, to promote delayed leptomeningeal neovascularization and to enhance blood delivery to the brain. Those procedures are also known under the generic appellation of encephalo-synangiosis, a term covering a wide spectrum of techniques that differ by the type and variety of tissues used. If in the past, some have used

Advantages, drawbacks and results

The main advantage of those techniques is their relative simplicity and rapidity. This makes them applicable by most of the neurosurgical teams provided the knowledge about the natural history of the disease and principles/pitfalls of its treatment are mastered. The technique is always feasible and very appealing in children in whom the small size of cortical and cutaneous vessels frequently precludes the possibility of a direct bypass. Moreover, they allow the revascularization of large areas of the affected hemisphere that covers at least the

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Fig. 1 – Illustrative case no. 1: EDAMS technique. This 51-year-old man was followed at our institution because of 3 episodes of left lenticulo-striate haemorrhages of which he made a good clinical recovery. Brain imaging disclosed a left Moyamoyalike disease with the development of abnormal deep lenticulo-striate neovessels. SPECT only showed a left parietal hypoperfusion without cerebrovascular impairment. Because of the recurrence of haemorrhagic events and of the small size of the superficial temporal artery, we opted for an indirect revascularization procedure with encephalo-duro-arteriomyo-synangiosis (EDAMS, successive steps G-N). At 3 years follow-up, the patient did not experience any rebleeding or ischaemic stroke. A. Cerebral CT scan showing a deep left lenticulo-striate haemorrhage. B. Cerebral MRA disclosing the occlusion of the left middle cerebral artery (MCA) in M1 (white arrow-head). C, D. FLAIR and gradient echo T2* weighted cerebral MRI showing the parenchymal sequelae. E. Cerebral SPECT at rest evidencing a left parietal hypoperfusion (without cerebrovascular reactivity impairment: image not displayed). F. Left internal carotid artery angiography confirming the proximal occlusion of the left MCA and the presence of lenticulo-striate Moyamoya vessels (white arrow-head). G. Skin incision under microscope magnification and along the course of the superficial temporal artery (STA). H. Harvesting of the STA, where continuity is preserved. I. Craniotomy fashioning, bone flap = B, donor STA = A and temporal muscle graft = M. J. Arachnoid opening. K. The temporal muscle graft is apposed onto the cortex underneath a strip of dura including the preserved parietal branch of the middle meningeal artery. L. The edges of the temporal muscle and of the STA conjunctive cuff are sutured to those of the dural flaps which extremities have been fold in the subdural space. M. The bone flap is replaced and secured by titanium rivets (note the two fenestrations on the bone flap to allow the intracranial course of the STA). N. Skin closure with absorbable suture.

revue neurologique 171 (2015) 31–44

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Fig. 2 – Illustrative case no. 2. Example of a very good angiographic result after encephalo-duro-arterio-synangiosis in an adult patient with definite Moyamoya disease. A, B. Preoperative lateral and anterior views of left internal carotid artery angiography showing no filling of the left middle cerebral artery (white arrow-head) territory together with the dense development lenticulo-striate Moyamoya collaterals (black arrow-head). C, D. Preoperative lateral and anterior views of left external carotid artery angiography evidencing noticeable leptomeningeal collaterals coming from the parietal branch (white arrow-head) of the middle meningeal artery (STA) and from the occipital artery (black arrow-head) with an important parieto-occipital blush. E, F. Postoperative lateral and anterior views of selective left external carotid artery angiography showing diffuse neovascularization (white arrow-heads) arising from the site of craniotomy and from the frontal branch of the superficial temporal artery (black arrow-head) used for the synangiosis.

MCA territory but could also reach less accessible territories (ACA and/or PCA) with ribbon-EDAMS or multiple burr-holes technique. Finally, several indirect procedures can be performed on the same hemisphere over time if there is interval progression of the disease to new vascular territories. The main disadvantage is that the clinical and angiographic effects are usually obtained 3 to 4 months after the procedure due to the time necessary for development of collateral vessels [8,40]. In children, EMS (indirect technique) could led to good revascularization (> 1/3 of the MCA territory) in 75% of patients among whom was noted a reduction of the lenticulo-striates

and choroidal neovessels, respectively in 90% and 60% of the cases, which could have the potential to also prevent future haemorrhagic complications [37]. Better results were then obtained in young patients (< 21 years old) using EDAS with pial synangiosis (suturing of the donor artery to the brain surface, therefore improving their direct contact) that offered a longterm control of the disease: 94% and 96% of patients were free of stroke or TIAs, respectively at 1 and 5 years [44]. Refinement of the EDAS technique with frontal galeal (periosteal)-synangiosis (EDAGS) led to even better results in terms of global SPECT changes (62% vs 36%) and in terms of revascularization of the ACA territory with improvement of related symptoms (81% vs

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Fig. 3 – Illustrative case no. 3. This 15-year-old boy was followed for a definite Moyamoya disease revealed by an acute confusional state following influenza B infection. Before this episode, he was complaining of attention and concentration disturbances, alternating paresthesia and severe holocranial chronic headaches. Imaging work-up disclosed bilateral Moyamoya disease with severe hypoperfusion of both hemispheres and recent infarction in the right frontal lobe. We opted for an indirect revascularization with multiple burr-holes technique. A. Diffusion sequence of cerebral MRI disclosing recent ischemic lesions in the right frontal lobe. B. MRA found bilateral steno-occlusion of distal internal carotid arteries. C. CTA showing the deep Moyamoya vessels bilaterally (arrow). D. MR perfusion and CVR maps with CO2 challenge evidenced severe hypoperfusion of fronto-temporo-parietal regions bilaterally (only posterior cerebral arteries territories are evidenced)–by courtesy of Pr Krainik and Dr Tahon, Grenoble University Hospital. E. The superficial temporal artery course (arrow-head) is preoperatively marked using a micro-doppler to allow appropriate skin incision (along the shaved area) to avoid vascular sacrifice. F. The scalp is peeled off with a knife, leaving the vascularised periosteum on the cranial surface. G. Cranial convexities are exposed and the burr-holes site are marked. H. Triangular periosteal flaps are incised and scraped from the skull close to the burr-holes sites in which they will be inserted. I. After dural and arachnoid opening, a temporal muscle flap is inserted in a burr hole. J. Twelve burr-holes per hemisphere were performed in the same manner in association with either periosteal or muscular flaps.

40%), better extent of frontal neoangiogenesis (79% vs 16%) and increase in blood flow on SPECT (70% vs 52%). However, in this study, it did not translate in significantly decreased rates of new infarctions or neurological improvement than EDAS alone [65]. Some authors have advocated the use of multiple indirect procedures in the same patient, which would result in the

optimization of collaterals formation and clinical improvement in 94% of patients versus 76% with EDAS alone [66]. If those techniques have high rates of success in children, probably because of the strong potential of neoangiogenesis in this age group, it seems that results are less easily reproducible and predictable in adults since some studies have reported far

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lower rates of good responders to these indirect treatments alone [8,9,67,68]. Nevertheless, in other series, the overall 5year risk of perioperative and subsequent ipsilateral stroke or death ranged from 15 to 30% in the adult population treated predominantly with an indirect technique (> 85%) versus 40– 65% after initial symptoms without treatment [13,14,28]. More recent series using EDAS in combination with multiple burrholes also demonstrated the resolution of ischemic or haemorrhagic manifestations in more than 95% of patients, among whom a majority were adults (> 80%) [63]. However, the positive effect of this surgical protocol on stroke recurrence (around 90% of patients being stroke-free postoperatively) failed to translate into a significant improvement of clinical outcomes (mRS) at follow-up [13,32].

5.

Direct surgical revascularization

5.1.

Principles [8,9,50–52]

The objective of this technique is to create by the mean of a microvascular anastomosis a direct connection between an artery of the scalp (a collateral branch of the ECA) and a cortical branch (M4) of the MCA. This will constitute an extracranial-intracranial bypass which role is to immediately increase the cerebral perfusion in the MCA territory and redistribute blood flow in other vascular territories. Due to the small size of their distal branches, particularly in MM patients, and to their deep location at the medial side of the hemisphere, the anterior and posterior cerebral arteries territories are not easily accessible to direct revascularization. This explains why combined techniques are nowadays advised to enlarge the surface of revascularization in association to direct bypass.

5.2.

Technique [9,53,69,70]

The donor artery is most of the time the parietal (or frontal) branch of the STA and, less frequently, the retro-auricular or the occipital artery. It is preoperatively selected according to its angiographic characteristics: appropriate course (projecting above the MCA cortical network), sufficient calibre and absence of large leptomeningeal distal cortical supply. A transcutaneous mini-doppler is used to map its course before it is harvested under operative microscope magnification (Fig. 4) by coagulating or clipping and dividing its small and large collaterals. Once the artery is freed from the scalp, the temporal muscle, cranial, dural and arachnoid openings are performed in the same manner as in the indirect technique. An accessible cortical recipient artery of similar calibre is prepared. Conjunctive and adventitial layers are removed at the donor artery extremity in order to ensure vessels congruence and proper suturing. Under temporary cross clamping, an arteriotomy is performed on the recipient vessel followed by microsurgical anastomosis with 10.0 interrupted or running sutures. After the cortical vessel flow is restored and the water-tightness at the anastomosis site is confirmed, the STA clamp can be removed. Immediate patency of the bypass can be assessed intraoperatively with the aid of a micro-doppler, a debimeter or microscope-integrated

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videoangiography [71]. When direct revascularization is used alone, the dura is closed leaving a large inferior durotomy for the STA graft. If a combined procedure (STA-MCA bypass + EDAMS) is performed, associated grafts (dura-matter, temporal muscle, periosteum) are applied onto the cortex. The bone flap is fenestrated so as to prevent compression or kinking of the STA donor vessel. The temporal muscle is partially reapproximated and the skin is closed. Postoperatively, 300 mg/d aspirin is administrated for one week, and then 75 mg daily.

5.3.

Advantages, drawbacks and results

This technique has the advantage of offering an immediate increase in cerebral blood flow, which is of paramount importance in patients with close recurrent events or crescendo symptoms due to chronic or worsening cerebral hypoperfusion. Applied alone, ECIC bypass might be considered to some extent as a ‘‘focal’’ solution since it theoretically only revascularizes the MCA territory. Nevertheless, the redistribution of flow provided by the bypass could also improve the filling of other vascular territories. Moreover, it is always possible, and even advised, to add to the direct procedure an indirect one in order to increase the chance of treatment success by blending the advantages of both techniques [72,73]. Those direct revascularization procedures are in most of the cases hardly applicable in children because of technical limits represented by the small size of cutaneous and cortical arteries, and the vasospastic character of cerebral arteries in this population. If the anaesthetic risk is globally similar to the indirect technique (mainly related to the risk of drop in blood pressure during anaesthesia), the duration of the procedure is longer because it adds the time of the microsurgical anastomosis to that of the EDAMS. This technique might also be associated with specific, although rare, complications including focal deficit due to ischemia or haemorrhage in the territory of the bypassed artery [28,74]. If early (1 week) new postoperative neurological symptoms might occur in about 10 to 30% of patients (mainly adults), those are in their vast majority transient (resolving completely in 1 or 2 weeks) and are not related to ischemic or haemorrhagic damages to the brain (normal MRI). A hyperaemic phenomenon has been suspected by some authors [75,76] but, as hyperperfusion could only be radiologically demonstrated in one third of patients [77], those temporary symptoms might also be related to transitory competing flows between natural collaterals and the bypass [68]. Extracranial-intracranial bypass patency rates are usually reported to be high > 90% [28,32]. Some authors even managed to perform combined procedures in children with high rate of clinical success, more than 90% of patients being free of TIA or ischemic events postoperatively [66,78–82], which compares favourably with paediatric series reporting indirect procedures (EDAS) alone or with similar adult series. Overall, combined procedures seems very effective in preventing stroke recurrence in children and adults with an annual risk of stroke that could be decreased respectively to 0% and 0.4% [46]. In recent occidental series, the overall 5-year risk of perioperative stroke, subsequent stroke or death has been reported to be around 5.5%, with improvement of mRS by 1–

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Fig. 4 – Illustrative case 4. This 47-year-old woman suffered of crescendo right hemiparesis without speech disturbance when she was admitted at our institution. MRI disclosed ancient left middle cerebral artery (MCA) infarctions. Hemodynamic studies showed a marked left fronto-parietal hypoperfusion with absent cerebrovascular reactivity during acetazolamide challenge. MRA and cerebral angiography disclosed a left Moyamoya-like disease with occlusion of the left MCA at its origin. We opted for a combined revascularization procedure with superficial temporal artery (STA) to MCA bypass. The patient made an immediate recovery of her motor deficit but presented the onset of aphasia 48 hours after the surgery without evidence of hyperperfusion or new ischemia in the left hemisphere. Speech disturbance spontaneously recoverd in two weeks. A. Cerebral MRI FLAIR weighted sequence showing previous ischemic lesions in the left MCA territory. B, C. Anterior view of left internal carotid artery (ICA) conventional (B) and 3D (C) angiography disclosing occlusion of the left MCA at the ICA bifurcation with development of Moyamoya collaterals (arrow-head). D. Preoperative SPECT finding severe hypoperfusion of rolandic region consistent with the clinical presentation (arrow-head). E. Postoperative SPECT showing normalisation of cerebral blood flow. F. Postoperative lateral view of selective angiography of the left superficial temporal artery (STA: arrow-head) confirming bypass patency and a good filling of the MCA territory (arrow). G. Postoperative doppler follow-up finding good flow in the bypass (85 cc/min). H. The course of the frontal and parietal branch of the STA are marked using a micro-doppler. I. The parietal branch of the STA is harvested. J. The craniotomy is performed. K. The arachnoid is extensively opened. L. The recipient vessel is freed from its arachnoidal adherences. M. The recipient

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2 points in roughly 70% of patients, more than 90% of patients being free of stroke or TIAs at 1 year or later [28,47]. As in the paediatric population treated with an indirect technique, bypass alone technique or combined procedures would lead to the rarefaction of MM vessels in 25 to 67% of adult patients [83,84]. In some cases, this would make peripheral lenticulo-striate pseudo-aneurysms (known to be responsible for deep haemorrhages) disappear [38,85]. All this effects would translate in a reduction of the rebleeding rate from 30–40% to roughly 13–20% in patients initially presenting with haemorrhage [10,18,83,84] and by comparison with either conservative or indirect EDAS treatments [36,67].

6. Personal experience in the surgical management of adult MM disease Between 2009 and 2014, 12 adult patients underwent 14 revascularization procedures for MM disease in our department (1 young patient was referred from Grenoble University Centre): mean age 41.3 (range 15–60,6 yrs, SD = 14.6), sex ratio = 1. Two patients had a syndromic MM: 1 deficit in BRCC3 gene, 1 dimorphism without confirmed genetic diagnosis. MM forms were the following: definite 5, probable 1, MM-like 6. MM types according to clinical presentation were the following: ischemic 8, hemorrhagic 2, combined 2. All patients followed a strict preoperative work-up as previously detailed using MRI, 6 vessels DSA, SPECT and TCD with acetazolamide challenge. All patients were recently symptomatic, with recurrent ischemic/haemorrhagic events (2/3) or crescendo neurological deficit (1/3) in association with severe alterations of cerebral blood flow on hemodynamical imaging. Indirect procedures alone were performed in 3 cases (EDAMS 2, multiple burr-holes 1) because no appropriate donor or recipient vessels were preor intraoperatively identified. After indirect procedures, significant, moderate and limited neoangiogenesis were seen respectively in 1 case each. Eleven combined revascularization procedures, namely direct + indirect (EDAMS), were performed in 9 patients: one had bilateral treatment for bilaterally symptomatic MM disease and an other received the association of a STA-MCA bypass with a delayed occipito-MCA bypass for recurring symptoms secondary to the stenosis of the STA graft. After combined procedures, peroperative, immediate and delayed bypass patency rates were respectively: 100%, 91% and 91% (1 early occlusion). One patient, with an aggressive definite MM syndrome (recurrent left sylvian and border zone infarctions with hemiparesis and aphasia, 29 years after inaugural contralateral infarction), died after surgery (bypass thrombosis and rapidly extensive postoperative MCA infarction). Postoperative ischemia occurred after 3 procedures: one was border zone and contralateral (bilateral MM) with confusion that resolved in few weeks, 1 was homolateral (temporooccipital territory) but at distance of bypass site with incomplete

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hemianopsia and seizure (MM syndrome with associated severe cardiac insufficiency), 1 was in the bypassed frontal territory but very focal with only transitory speech disturbance. One patient had to be reoperated for delayed wound disunion without evidence of infection. Mean clinical and radiological follow-up was 22 months. Postoperative mRS at discharge and at 6 months were respectively improved or stable in 71% and 92% of cases compared with preoperative status. All patients were free of recurring vascular events at last clinical and radiological follow-up.

7.

Conclusion

MM disease/syndrom is a complex and unpredictable entity that requires multidisciplinary clinical and radiological expertise. In symptomatic patients, it is accompanied by an important annual risk of recurrence of ischemic and haemorrhagic strokes, respectively about 10–13% and 2–7%. This menace is higher during the first 2 years, but there is also a life long threat of subsequent delayed events, particularly as regards intracerebral haemorrhages, which are associated with a high mortality rate. Furthermore, other important clinical aspects have been largely under-reported or evaluated by many studies, as the delayed impact of chronic hypoperfusion and the cumulative effect of recurrent vascular insults to the brain that could be responsible for progressive cognitive decline and social handicap, in children but also in adults [8,78,80,86–89]. Probably because of the good results of surgical revascularization, the rarity and variability of the disease together with the variety of available surgical treatments, no randomized trial has been organized so far to attempt to confirm the beneficial effect of surgical revascularization in ischaemic MM disease. However, on the basis of the previous studies described in this article, there is growing evidence that surgical revascularization would be effective at improving cerebral haemodynamic and at reducing the risk of recurrent stroke both in paediatric and adult patients. Therefore, there is a global consensus to offer this kind of treatment when severity criteria are gathered: symptomatic disease with crescendo/progressive neurological/cognitive deficit or recurrent ischemic/haemorrhagic strokes associated with pronounced alterations of cerebral perfusion on haemodynamic imaging. Because the disease is active mainly after its clinical onset, early treatment is recommended, particularly in symptomatic children, to avoid irreversible cerebral lesions [21,90]. There are lots of discrepancies between studies comparing indirect with direct/combined procedures and two recent reviews failed to demonstrate the superiority of one technique over another, at least in children [35,91]. Nevertheless, some remarkable characteristics make those strategies more suitable to a population rather than another. Indirect procedures

cortical artery is exposed. N. Good congruence between donor and recipient vessel is confirmed. O. The distal end of the STA is prepared then flushed with heparinized serum. P. The recipient cortical vessel is temporarily occluded to allow the anastomosis. Q. An arteriotomy is performed. R, S. The STA is sutured to the recipient vessel with two 10.0 prolene running sutures. T. Final bypass. U, V. Peroperative indocyanine green videoangiography confirming the patency of the bypass and the fast filling of donor and recipient vessels (coloured in red on the semi-quantitative flow map).

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are widely used in children because they are easily feasible and effective regarding the usual small size of cerebral/ cutaneous vessels and the strong angiogenic potential at this age. Techniques covering the largest surface of the hemisphere(s) with as many grafting tissues as possible like EDAMPS (encephalo-duro-arterio-myo-periosteo-synangiosis) or multiple burr-holes should be favoured in order to enhance pial neovascularization. Despite a slightly higher rate of perioperative complications and lower clinical/radiological efficacies in adults, an indirect procedure is a second choice but acceptable option in this age group if an extracranial-intracranial bypass is not technically feasible because of the patient’s vascular anatomy or neurosurgeon inexperience. In other adult cases, particularly those with crescendo deficit, there is a general consensus to encourage the use of combined procedures that cumulate the advantages of both techniques: rapid improvement of blood flow (immediate reversion of hypoperfusion related neurological deficits), large coverage of brain surface and higher reduction of 5-year recurrent stroke rate (5% vs 15%). Concerning patients with haemorrhagic presentation, surgical revascularization has been proven to induce reduction in MM deep collaterals or pseudo-aneurysms, thus decreasing the risk of subsequent haemorrhages by 2 to 3-fold. The recent of the Japanese multicentered, prospective, randomized, controlled trial, designed to evaluate the efficacy of direct revascularization versus medical management alone in preventing recurrent haemorrhages in adult MM patients, has confirmed this preventive effect of direct bypass surgery with significant differences in favor of the surgical group and similar reduction of the rate of rebleeding at 5-years follow-up [92]. This important result is the best scientific evidence to date supporting the interest of direct (or combined) revascularization in adult MM patients with haemorrhagic presentation and should be considered in clinical practice.

Disclosure of interest The authors declare that they have no conflicts of interest concerning this article.

references

[1] Kleinloog R, Regli L, Rinkel GJ, Klijn CJ. Regional differences in incidence and patient characteristics of moyamoya disease: a systematic review. J Neurol Neurosurg Psychiatry 2012;83:531–6. [2] Kossorotoff M, Herve D, Toulgoat F, Renaud C, Presles E, Chabriat H, et al. Paediatric moyamoya in mainland France: a comprehensive survey of academic neuropaediatric centres. Cerebrovasc Dis 2012;33:76–9. [3] Suzuki J, Takaku A. Cerebrovascular ‘‘moyamoya’’ disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 1969;20:288–99. [4] Smith ER, Scott RM. Progression of disease in unilateral moyamoya syndrome. Neurosurg Focus 2008;24:E17. [5] Kuroda S, Ishikawa T, Houkin K, Nanba R, Hokari M, Iwasaki Y. Incidence and clinical features of disease progression in adult moyamoya disease. Stroke 2005;36:2148–53.

[6] Kelly ME, Bell-Stephens TE, Marks MP, Do HM, Steinberg GK. Progression of unilateral moyamoya disease: a clinical series. Cerebrovasc Dis 2006;22:109–15. [7] Scott RM, Smith ER. Moyamoya disease and moyamoya syndrome. N Engl J Med 2009;360:1226–37. [8] Kuroda S, Houkin K. Moyamoya disease: current concepts and future perspectives. Lancet Neurol 2008;7:1056–66. [9] Zipfel GJ, Fox Jr DJ, Rivet DJ. Moyamoya disease in adults: the role of cerebral revascularization. Skull Base 2005;15:27–41. [10] Yoshida Y, Yoshimoto T, Shirane R, Sakurai Y. Clinical course, surgical management, and long-term outcome of moyamoya patients with rebleeding after an episode of intracerebral hemorrhage: an extensive follow-up study. Stroke 1999;30:2272–6. [11] Morioka M, Hamada J, Todaka T, Yano S, Kai Y, Ushio Y. High-risk age for rebleeding in patients with hemorrhagic moyamoya disease: long-term follow-up study. Neurosurgery 2003;52:1049–54. [12] Kuroda S, Hashimoto N, Yoshimoto T, Iwasaki Y. Radiological findings, clinical course, and outcome in asymptomatic moyamoya disease: results of multicenter survey in Japan. Stroke 2007;38:1430–5. [13] Hallemeier CL, Rich KM, Grubb Jr RL, Chicoine MR, Moran CJ, Cross 3rd DT, et al. Clinical features and outcome in North American adults with moyamoya phenomenon. Stroke 2006;37:1490–6. [14] Chiu D, Shedden P, Bratina P, Grotta JC. Clinical features of moyamoya disease in the United States. Stroke 1998;29:1347–51. [15] Kraemer M, Heienbrok W, Berlit P. Moyamoya disease in Europeans. Stroke 2008;39:3193–200. [16] Starke RM, Komotar RJ, Hickman ZL, Paz YE, Pugliese AG, Otten ML, et al. Clinical features, surgical treatment, and long-term outcome in adult patients with moyamoya disease. Clinical article. J Neurosurg 2009;111:936–42. [17] Gross BA, Du R. The natural history of moyamoya in a North American adult cohort. J Clin Neurosci 2013;20:44–8. [18] Fujii K, Ikezaki K, Irikura K, Miyasaka Y, Fukui M. The efficacy of bypass surgery for the patients with hemorrhagic moyamoya disease. Clin Neurol Neurosurg 1997;99(Suppl. 2):S194–5. [19] Kobayashi E, Saeki N, Oishi H, Hirai S, Yamaura A. Longterm natural history of hemorrhagic moyamoya disease in 42 patients. J Neurosurg 2000;93:976–80. [20] Gross BA, Du R. Adult moyamoya after revascularization. Acta Neurochir (Wien) 2013;155:247–54. [21] Smith ER, Scott RM. Surgical management of moyamoya syndrome. Skull Base 2005;15:15–26. [22] Czabanka M, Pena-Tapia P, Schubert GA, Heppner FL, Martus P, Horn P, et al. Proposal for a new grading of Moyamoya disease in adult patients. Cerebrovasc Dis 2011;32:41–50. [23] Zipfel GJ, Sagar J, Miller JP, Videen TO, Grubb Jr RL, Dacey Jr RG, et al. Cerebral hemodynamics as a predictor of stroke in adult patients with moyamoya disease: a prospective observational study. Neurosurg Focus 2009;26:E6. [24] Ogasawara K, Ogawa A, Yoshimoto T. Cerebrovascular reactivity to acetazolamide and outcome in patients with symptomatic internal carotid or middle cerebral artery occlusion: a xenon-133 single-photon emission computed tomography study. Stroke 2002;33:1857–62. [25] Kuroda S, Houkin K, Kamiyama H, Mitsumori K, Iwasaki Y, Abe H. Long-term prognosis of medically treated patients with internal carotid or middle cerebral artery occlusion: can acetazolamide test predict it? Stroke 2001;32:2110–6. [26] Nariai T, Matsushima Y, Imae S, Tanaka Y, Ishii K, Senda M, et al. Severe haemodynamic stress in selected subtypes of patients with moyamoya disease: a positron emission

revue neurologique 171 (2015) 31–44

[27]

[28]

[29]

[30]

[31]

[32]

[33]

[34]

[35]

[36]

[37]

[38]

[39]

[40]

[41]

[42]

[43]

tomography study. J Neurol Neurosurg Psychiatry 2005;76:663–9. Ganesan V. Moyamoya: to cut or not to cut is not the only question. A paediatric neurologist’s perspective. Dev Med Child Neurol 2010;52(1):10–3. Guzman R, Lee M, Achrol A, Bell-Stephens T, Kelly M, Do HM, et al. Clinical outcome after 450 revascularization procedures for moyamoya disease. Clinical article. J Neurosurg 2009;111:927–35. Kim SH, Choi JU, Yang KH, Kim TG, Kim DS. Risk factors for postoperative ischemic complications in patients with moyamoya disease. J Neurosurg 2005;103:433–8. Thines L, Agid R, Dehdashti AR, da Costa L, Wallace MC, Terbrugge KG, et al. Assessment of extracranial-intracranial bypass patency with 64-slice multidetector computerized tomography angiography. Neuroradiology 2009;51:505–15. So Y, Lee HY, Kim SK, Lee JS, Wang KC, Cho BK, et al. Prediction of the clinical outcome of pediatric moyamoya disease with postoperative basal/acetazolamide stress brain perfusion SPECT after revascularization surgery. Stroke 2005;36:1485–9. Abla AA, Gandhoke G, Clark JC, Oppenlander ME, Velat GJ, Zabramski JM, et al. Surgical outcomes for moyamoya angiopathy at Barrow Neurological Institute with comparison of adult indirect encephaloduroarteriosynangiosis bypass, adult direct superficial temporal artery-to-middle cerebral artery bypass, and pediatric bypass: 154 revascularization surgeries in 140 affected hemispheres. Neurosurgery 2013;73:430–9. 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 2002;36:14–21. Choi JU, Kim DS, Kim EY, Lee KC. Natural history of moyamoya disease: comparison of activity of daily living in surgery and non surgery groups. Clin Neurol Neurosurg 1997;99(Suppl. 2):S11–8. Fung LW, Thompson D, Ganesan V. Revascularisation surgery for paediatric moyamoya: a review of the literature. Childs Nerv Syst 2005;21:358–64. Kawaguchi S, Okuno S, Sakaki T. Effect of direct arterial bypass on the prevention of future stroke in patients with the hemorrhagic variety of moyamoya disease. J Neurosurg 2000;93:397–401. Irikura K, Miyasaka Y, Kurata A, Tanaka R, Yamada M, Kan S, et al. The effect of encephalo-myo-synangiosis on abnormal collateral vessels in childhood moyamoya disease. Neurol Res 2000;22:341–6. Kuroda S, Houkin K, Kamiyama H, Abe H. Effects of surgical revascularization on peripheral artery aneurysms in moyamoya disease: report of three cases. Neurosurgery 2001;49:463–7. Liu X, Zhang D, Shuo W, Zhao Y, Wang R, Zhao J. Long-term outcome after conservative and surgical treatment of haemorrhagic moyamoya disease. J Neurol Neurosurg Psychiatry 2013;84:258–65. Houkin K, Nakayama N, Kuroda S, Ishikawa T, Nonaka T. How does angiogenesis develop in pediatric moyamoya disease after surgery? A prospective study with MR angiography. Childs Nerv Syst 2004;20:734–41. Burke GM, Burke AM, Sherma AK, Hurley MC, Batjer HH, Bendok BR. Moyamoya disease: a summary. Neurosurg Focus 2009;26:E11. Parray T, Martin TW, Siddiqui S. Moyamoya disease: a review of the disease and anesthetic management. J Neurosurg Anesthesiol 2011;23:100–9. Hyun SJ, Kim JS, Hong SC. Prognostic factors associated with perioperative ischemic complications in adult-onset moyamoya disease. Acta Neurochir (Wien) 2010;152:1181–8.

43

[44] 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 2004;100:142–9. [45] Kim SK, Cho BK, Phi JH, Lee JY, Chae JH, Kim KJ, et al. Pediatric Moyamoya disease: an analysis of 410 consecutive cases. Ann Neurol 2010;68:92–101. [46] Kuroda S, Houkin K, Ishikawa T, Nakayama N, Iwasaki Y. Novel bypass surgery for moyamoya disease using pericranial flap: its impacts on cerebral hemodynamics and long-term outcome. Neurosurgery 2010;66:1093–101. [47] Mallory GW, Bower RS, Nwojo ME, Taussky P, Wetjen NM, Varzoni TC, et al. Surgical outcomes and predictors of stroke in a North American white and African American moyamoya population. Neurosurgery 2013;73:984–91. [48] Fujimura M, Kaneta T, Tominaga T. Efficacy of superficial temporal artery-middle cerebral artery anastomosis with routine postoperative cerebral blood flow measurement during the acute stage in childhood moyamoya disease. Childs Nerv Syst 2008;24:827–32. [49] Matsushima T, Inoue T, Katsuta T, Natori Y, Suzuki S, Ikezaki K, et al. An indirect revascularization method in the surgical treatment of moyamoya disease–various kinds of indirect procedures and a multiple combined indirect procedure. Neurol Med Chir (Tokyo) 1998;38(Suppl.): 297–302. [50] Baaj AA, Agazzi S, Sayed ZA, Toledo M, Spetzler RF, van Loveren H. Surgical management of moyamoya disease: a review. Neurosurg Focus 2009;26:E7. [51] Smith JL. Understanding and treating moyamoya disease in children. Neurosurg Focus 2009;26:E4. [52] Starke RM, Komotar RJ, Connolly ES. Optimal surgical treatment for moyamoya disease in adults: direct versus indirect bypass. Neurosurg Focus 2009;26:E8. [53] Kuroda S, Houkin K. Bypass surgery for moyamoya disease: concept and essence of sugical techniques. Neurol Med Chir (Tokyo) 2012;52:287–94. [54] Karasawa J, Kikuchi H, Kawamura J, Sakai T. Intracranial transplantation of the omentum for cerebrovascular moyamoya disease: a two-year follow-up study. Surg Neurol 1980;14:444–9. [55] Karasawa J, Kikuchi H, Furuse S, Sakaki T, Yoshida Y. A surgical treatment of ‘‘moyamoya’’ disease ‘‘encephalo-myo synangiosis’’. Neurol Med Chir (Tokyo) 1977;17:29–37. [56] Matsushima Y, Fukai N, Tanaka K, Tsuruoka S, Inaba Y, Aoyagi M, et al. A new surgical treatment of moyamoya disease in children: a preliminary report. Surg Neurol 1981;15:313–20. [57] Adelson PD, Scott RM. Pial synangiosis for moyamoya syndrome in children. Pediatr Neurosurg 1995;23:26–33. [58] Kinugasa K, Mandai S, Kamata I, Sugiu K, Ohmoto T. Surgical treatment of moyamoya disease: operative technique for encephalo-duro-arterio-myo-synangiosis, its follow-up, clinical results, and angiograms. Neurosurgery 1993;32:527–31. [59] Kinugasa K, Mandai S, Tokunaga K, Kamata I, Sugiu K, Handa A, et al. Ribbon enchephalo-duro-arterio-myosynangiosis for moyamoya disease. Surg Neurol 1994;41:455–61. [60] Kim CY, Wang KC, Kim SK, Chung YN, Kim HS, Cho BK. Encephaloduroarteriosynangiosis with bifrontal encephalogaleo(periosteal)synangiosis in the pediatric moyamoya disease: the surgical technique and its outcomes. Childs Nerv Syst 2003;19:316–24. [61] McLaughlin N, Martin NA. Effectiveness of burr holes for indirect revascularization in patients with Moyamoya disease-a review of the literature. World Neurosurg 2014;81(1):91–8.

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revue neurologique 171 (2015) 31–44

[62] Kawaguchi T, Fujita S, Hosoda K, Shose Y, Hamano S, Iwakura M, et al. Multiple burr-hole operation for adult moyamoya disease. J Neurosurg 1996;84:468–76. [63] Dusick JR, Gonzalez NR, Martin NA. Clinical and angiographic outcomes from indirect revascularization surgery for Moyamoya disease in adults and children: a review of 63 procedures. Neurosurgery 2011;68:34–43. [64] 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 2006;105:437–43. [65] Kim SK, Wang KC, Kim IO, Lee DS, Cho BK. Combined encephaloduroarteriosynangiosis and bifrontal encephalogaleo(periosteal)synangiosis in pediatric moyamoya disease. Neurosurgery 2002;50:88–96. [66] Matsushima T, Inoue TK, Suzuki SO, Inoue T, Ikezaki K, Fukui M, et al. Surgical techniques and the results of a fronto-temporo-parietal combined indirect bypass procedure for children with moyamoya disease: a comparison with the results of encephalo-duro-arteriosynangiosis alone. Clin Neurol Neurosurg 1997;99(Suppl. 2): S123–7. [67] Houkin K, Kamiyama H, Abe H, Takahashi A, Kuroda S. Surgical therapy for adult moyamoya disease. Can surgical revascularization prevent the recurrence of intracerebral hemorrhage? Stroke 1996;27:1342–6. [68] Pandey P, Steinberg GK. Neurosurgical advances in the treatment of moyamoya disease. Stroke 2011;42: 3304–10. [69] Wanebo JE, Zabramski JM, Spetzler RF. Superficial temporal artery-to-middle cerebral artery bypass grafting for cerebral revascularization. Neurosurgery 2004;55:395–8. [70] Newell DW, Vilela MD. Superficial temporal artery to middle cerebral artery bypass. Neurosurgery 2004;54: 1441–8. [71] Woitzik J, Horn P, Vajkoczy P, Schmiedek P. Intraoperative control of extracranial-intracranial bypass patency by near-infrared indocyanine green videoangiography. J Neurosurg 2005;102:692–8. [72] Kim DS, Yoo DS, Huh PW, Kang SG, Cho KS, Kim MC. Combined direct anastomosis and encephaloduroarteriogaleosynangiosis using inverted superficial temporal artery-galeal flap and superficial temporal artery-galeal pedicle in adult moyamoya disease. Surg Neurol 2006;66:389–94. [73] Amin-Hanjani S, Singh A, Rifai H, Thulborn KR, Alaraj A, Aletich V, et al. Combined direct and indirect bypass for Moyamoya: quantitative assessment of direct bypass flow over time. Neurosurgery 2013;73(6):962–7. [74] Fujimura M, Shimizu H, Mugikura S, Tominaga T. Delayed intracerebral hemorrhage after superficial temporal arterymiddle cerebral artery anastomosis in a patient with moyamoya disease: possible involvement of cerebral hyperperfusion and increased vascular permeability. Surg Neurol 2009;71:223–7. [75] Fujimura M, Mugikura S, Kaneta T, Shimizu H, Tominaga T. Incidence and risk factors for symptomatic cerebral hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in patients with moyamoya disease. Surg Neurol 2009;71:442–7. [76] Kim JE, Oh CW, Kwon OK, Park SQ, Kim SE, Kim YK. Transient hyperperfusion after superficial temporal artery/ middle cerebral artery bypass surgery as a possible cause of postoperative transient neurological deterioration. Cerebrovasc Dis 2008;25:580–6.

[77] Ohue S, Kumon Y, Kohno K, Watanabe H, Iwata S, Ohnishi T. Postoperative temporary neurological deficits in adults with moyamoya disease. Surg Neurol 2008;69:281–6. [78] Funaki T, Takahashi JC, Takagi Y, Yoshida K, Araki Y, Kikuchi T, et al. Impact of posterior cerebral artery involvement on long-term clinical and social outcome of pediatric moyamoya disease. J Neurosurg Pediatr 2013;12(6):626–32. [79] Takahashi A, Kamiyama H, Houkin K, Abe H. Surgical treatment of childhood moyamoya disease–comparison of reconstructive surgery centered on the frontal region and the parietal region. Neurol Med Chir (Tokyo) 1995;35:231–7. [80] Ishikawa T, Houkin K, Kamiyama H, Abe H. Effects of surgical revascularization on outcome of patients with pediatric moyamoya disease. Stroke 1997;28:1170–3. [81] Suzuki Y, Negoro M, Shibuya M, Yoshida J, Negoro T, Watanabe 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 1997;40:324–9. [82] Golby AJ, Marks MP, Thompson RC, Steinberg GK. Direct and combined revascularization in pediatric moyamoya disease. Neurosurgery 1999;45:50–8. [83] Iwama T, Morimoto M, Hashimoto N, Goto Y, Todaka T, Sawada M. Mechanism of intracranial rebleeding in moyamoya disease. Clin Neurol Neurosurg 1997;99(Suppl. 2):S187–90. [84] Okada Y, Shima T, Nishida M, Yamane K, Yamada T, Yamanaka C. Effectiveness of superficial temporal arterymiddle cerebral artery anastomosis in adult moyamoya disease: cerebral hemodynamics and clinical course in ischemic and hemorrhagic varieties. Stroke 1998;29:625–30. [85] Peltier J, Vinchon M, Soto-Ares G, Dhellemmes P. Disappearance of a middle cerebral artery aneurysm associated with Moyamoya syndrome after revascularization in a child: case report. Childs Nerv Syst 2008;24:1483–7. [86] Lee JY, Phi JH, Wang KC, Cho BK, Shin MS, Kim SK. Neurocognitive profiles of children with moyamoya disease before and after surgical intervention. Cerebrovasc Dis 2011;31:230–7. [87] Calviere L, Catalaa I, Frugier CG, Viguier A, Albucher JF, Delisle MB, et al. [Clinical course and outcome in French adults with Moyamoya disease]. Rev Neurol (Paris) 2009;165:709–17. [88] Matsushima Y, Aoyagi M, Nariai T, Takada Y, Hirakawa K. Long-term intelligence outcome of post-encephalo-duroarterio-synangiosis childhood moyamoya patients. Clin Neurol Neurosurg 1997;99(Suppl. 2):S147–50. [89] Karzmark P, Zeifert PD, Tan S, Dorfman LJ, Bell-Stephens TE, Steinberg GK. Effect of moyamoya disease on neuropsychological functioning in adults. Neurosurgery 2008;62:1048–51. [90] Kim SK, Seol HJ, Cho BK, Hwang YS, Lee DS, Wang KC. Moyamoya disease among young patients: its aggressive clinical course and the role of active surgical treatment. Neurosurgery 2004;54:840–4. [91] Veeravagu A, Guzman R, Patil CG, Hou LC, Lee M, Steinberg GK. Moyamoya disease in pediatric patients: outcomes of neurosurgical interventions. Neurosurg Focus 2008;24:E16. [92] Miyamoto S, Yoshimoto T, Hashimoto N, Okada Y, Tsuji I, Tominaga T, et al. Effects of extracranial-intracranial bypass for patients with hemorrhagic moyamoya disease: results of the Japan Adult Moyamoya Trial. Stroke 2014;45:1415–21.