Moyamoya disease (MMD) is a progressive cerebrovascular disease with unknown etiology, characterized by bilateral stenoocclusive changes at the terminal portion of the internal carotid artery and an abnormal vascular network formation at the base of the brain. MMD has an intrinsic nature to convert the vascular supply for the brain from internal carotid (IC) system to the external carotid (EC) system, as indicated by Suzuki’s angiographic staging. Insufficiency of this ‘IC-EC conversion system’ could result not only in cerebral ischemia, but also in intracranial hemorrhage from inadequate collateral anastomosis, both of which represent the clinical manifestation of MMD. Surgical revascularization prevents cerebral ischemic attack by improving cerebral blood flow, and recent evidence further suggests that extracranial-intracranial bypass could powerfully reduce the risk of re-bleeding in MMD patients with posterior hemorrhage, who were known to have extremely high re-bleeding risk. Although the exact mechanism underlying the hemorrhagic presentation in MMD is undetermined, most recent angiographic analysis revealed the characteristic angio-architecture related to high re-bleeding risk, such as the extension and dilatation of choroidal collaterals and posterior cerebral artery involvement. We sought to update the current management strategy for hemorrhagic MMD, including the outcome of surgical revascularization for hemorrhagic MMD in our institute. Further investigations will clarify the optimal surgical strategy to prevent hemorrhagic manifestation in patients with MMD.
Moyamoya disease (MMD) is a progressive cerebrovascular disease with unknown etiology, characterized by bilateral steno-occlusive changes at the terminal portion of the internal carotid artery (ICA) and an abnormal vascular network formation at the base of the brain [
In light of this dynamic pathology of MMD, EC-IC bypass such as superficial temporal artery-middle cerebral artery (STA-MCA) bypass potentially has a perfect concept to compliment this ‘IC-EC conversion system’ and thus prevents cerebral ischemia and/or hemorrhage [
Original diagnostic criteria of definitive MMD included steno-occlusive change at ICA bilaterally, which is associated with abnormal vascular network formation at the base of the brain [
Definitive diagnosis of MMD is not always easy, especially in patients with early stage of Suzuki’s angiographic grading [
Concept of surgical revascularization for MMD includes both microsurgical reconstruction by STA-MCA bypass and the consolidation for future vasculogenesis by indirect pial synangiosis such as encephalo-duro-myo-synangiosis (EDMS) and encephalo-duro-arterio-synangiosis [
Direct revascularization surgery such as STA-MCA bypass is established as an effective procedure for the MMD patients with ischemic symptoms, providing long-term favorable outcomes [
Based on the JAM criteria, we attempted revascularization surgery for the hemorrhagic MMD patients since 2014, in principal for the affected hemispheres with posterior hemorrhage. Surgical indication for hemorrhagic MMD in our institute is specified in
Since the first supplemental study of JAM trial indicated the extremely high annual re-bleeding rates in MMD patients with posterior hemorrhage [
Before JAM trial, it has been reported that dilatation and/or extension of choroidal artery could be one of the characteristic angiographic findings of hemorrhagic MMD. Irikura et al. [
Surgical complications of MMD include peri-operative cerebral ischemia and cerebral hyperperfusion syndrome [
Besides peri-operative cerebral ischemia, rapid focal increase in CBF at the site of the anastomosis could result in focal hyperemia associated with vasogenic edema and/or hemorrhagic conversion in MMD [
Concept of the peri-operative management for MMD is to afford favorable ‘IC-EC conversion’ without causing deleterious impact to the affected hemisphere [
Recent evidence suggests that surgical revascularization such as STA-MCA bypass could powerfully reduce the risk of re-bleeding in MMD patients with posterior hemorrhage, who potentially have extremely high annual re-bleeding rate (17% per year). Outcome of surgical revascularization for hemorrhagic MMD is favorable, while prompt perioperative management is essential to avoid surgical complications including cerebral hyperperfusion syndrome.
No potential conflict of interest relevant to this article was reported.
This type of study does not require informed consent.
A : Representative finding of T2*-weighted magnetic resonance (MR) imaging of a 45-year old woman with hemorrhagic MMD. Among the multiple hemorrhages, posterior hemorrhage was evident on the left hemisphere (arrows). B : MR angiography demonstrating terminal internal carotid artery stenosis and abnormal vascular network formation bilaterally.
Intra-operative view of microsurgical revascularization. Surgical view before (A), during (B), and after left superficial temporal artery-middle cerebral artery bypass (C and D). Indocyanine green video-angiography demonstrated apparently patent bypass with favorable distribution of bypass flow (D).
A : Postoperative MR angiography demonstrating STA-MCA bypass as thick high signal intensity (arrow). B : N-isopropyl-p-[123I] iodpamphetamine single-photon emission computed tomography seven days after left STA-MCA bypass demonstrating marked improvement in cerebral blood flow on the hemisphere operated on (dotted circles). STA-MCA : superficial temporal artery-middle cerebral artery.
Surgical indication for hemorrhagic Moyamoya disease
1. Adult (16 to 65 years old) |
2. Within 1 year after hemorrhage (1–12 months) |
3. Independent ADL (mRS 0–2) |
4. Absence of major brain damage |
5. Posterior hemorrhage |
ADL : activity of daily living, mRS : modified Rankin Scale
Angiographic characteristics associated with hemorrhage in Moyamoya disease
1. Hemorrhagic presentation |
1) Development of thalamic and/or choroidal collaterals |
2) Higher Suzuki’s angiographic staging |
2. Posterior hemorrhage |
1) Development of choroidal collateral |
2) Posterior cerebral artery involvement |
ADL : activity of daily living, mRS : modified Rankin Scale