First autopsy analysis of a neovascularized arterial network induced by indirect bypass surgery for moyamoya disease: case report

Abstract

abbreviatioNs CBF = cerebral blood flow; CBV = cerebral blood volume; CPP = cerebral perfusion pressure; MMD = moyamoya disease; MTT = mean transit time; OEF = oxygen extraction fraction; STA = superficial temporal artery. The object of this study was to analyze the pathology of collateral vessels newly induced by indirect bypass surgery for moyamoya disease (MMD). An autopsy analysis was conducted on a 39-year-old woman with MMD who had died of a brainstem infarction. The patient had undergone bilateral indirect bypass surgeries 22 years earlier. Sufficient revascularization via bilateral external carotid arterial systems was confirmed by cerebral angiography before her death. Macroscopic observation of the operative areas revealed countless meandering vessels on the internal surface of the dura mater connected with small vessels on the brain surface and in the subpial brain tissue. Notably, microscopic analysis of these vessels revealed the characteristic 3-layer structure of an arterial wall. This autopsy analysis was the first to confirm that indirect bypass surgery had induced the formation of a new arterial network (arteriogenesis) and that this network had been maintained for more than 20 years to compensate for the chronic cerebral ischemia caused by the MMD.

Limits and pitfalls of indirect revascularization in moyamoya disease and syndrome

“…One of the most relevant hypotheses is that functional revascularization requires two fundamental steps: the development of tissues providing vascular beds (angiogenesis) and the shear stress-related stimulus to induce arterious anastomosis (arteriogenesis) [67]. Accordingly, autoptic analysis on patients treated with indirect bypass showed poor revascularization if brain damage had occurred before the surgical procedure, which suggests that a reduced CPP manifests as a prolonged mean transit time (MTT) [68]. CPP influences the effects of indirect bypass surgery since arteriogenesis plays a pivotal role in the formation of the collateral network induced by the surgical procedure [68].…”

“…Accordingly, autoptic analysis on patients treated with indirect bypass showed poor revascularization if brain damage had occurred before the surgical procedure, which suggests that a reduced CPP manifests as a prolonged mean transit time (MTT) [68]. CPP influences the effects of indirect bypass surgery since arteriogenesis plays a pivotal role in the formation of the collateral network induced by the surgical procedure [68]. Once the connection between brain surface and external carotid artery system has been generated thanks to the indirect bypass procedure through scar formation and angiogenesis, arteriogenesis progresses from the external carotid artery system (normal CPP) to the brain surface (extremely decreased CPP) [68].…”

“…CPP influences the effects of indirect bypass surgery since arteriogenesis plays a pivotal role in the formation of the collateral network induced by the surgical procedure [68]. Once the connection between brain surface and external carotid artery system has been generated thanks to the indirect bypass procedure through scar formation and angiogenesis, arteriogenesis progresses from the external carotid artery system (normal CPP) to the brain surface (extremely decreased CPP) [68]. According to this interpretation of the effects of indirect bypass surgery, it is possible to predict the degree of arteriogenesis induced by surgical treatment [68].…”

“…Once the connection between brain surface and external carotid artery system has been generated thanks to the indirect bypass procedure through scar formation and angiogenesis, arteriogenesis progresses from the external carotid artery system (normal CPP) to the brain surface (extremely decreased CPP) [68]. According to this interpretation of the effects of indirect bypass surgery, it is possible to predict the degree of arteriogenesis induced by surgical treatment [68]. Zhao et al compared the revascularization degree on short-term (3-6 months ) and long-term (1 year) follow-up angiography in 25 hemispheres of patients with MMD (13 pediatric and 12 adult) treated with indirect bypass surgery (EDAS) to investigate the differences in the postsurgical neovascularization development in relation to the duration of the follow-up [57].…”

Combined Direct and Indirect Cerebral Revascularization Using Local and Flow-Through Flaps

“…5 The development of collateral vasculature between vascularized tissue and the brain has been repeatedly demonstrated by angiography and autopsy. [6][7][8] Direct and indirect revascularization methods can also be combined for acute revascularization and delayed angiogenesis. 9 In an effort to improve outcomes, we have utilized a multidisciplinary approach with neurosurgery revascularization techniques and plastic surgery flap elevation techniques for combined revascularization procedures.…”