Angiographic Structural Differentiation between Native Arteriogenesis and Therapeutic Synangiosis in Intracranial Arterial Steno-Occlusive Disease

Abstract

Background and purpose: Encephaloduroarteriosynangiosis has been shown to generate collateral vessels from the extracranial-to-intracranial circulation in patients with Moyamoya disease and intracranial arterial steno-occlusive disease. The mechanisms involved are not well-understood. We hypothesized that angiogenesis is the leading mechanism forming collaterals after encephaloduroarteriosynangiosis because there are no pre-existing connections. Angiogenesis-generated collaterals should exhibit higher architectural complexity compared with innate collaterals.

Materials and methods: Pre- and postoperative digital subtraction angiograms were analyzed in patients enrolled in a prospective trial of encephaloduroarteriosynangiosis surgery. Branching angioscore, tortuosity index, and local connected fractal dimension were compared between innate and postoperative collaterals.

Results: One hundred one angiograms (50 preoperative, 51 postoperative) were analyzed from 44 patients (22 with intracranial atherosclerosis and 22 with Moyamoya disease). There was a significantly higher median branching angioscore (13 versus 4, P < .001) and a lower median tortuosity index (1.08 versus 1.76, P < .001) in the encephaloduroarteriosynangiosis collaterals compared with innate collaterals. Higher mean local fractal dimension peaks (1.28 ± 0.1 versus 1.16 ± 0.11, P < .001) were observed in the encephaloduroarteriosynangiosis collaterals compared with innate collaterals for both intracranial atherosclerosis (P < .001) and Moyamoya disease (P < .001) groups. The observed increase in high connectivity was greater in the intracranial atherosclerosis group compared with patients with Moyamoya disease (P = .01).

Conclusions: The higher median branching angioscore and local connected fractal dimension, along with the lower median tortuosity index of encephaloduroarteriosynangiosis collaterals, are consistent with the greater complexity observed in the process of sprouting and splitting associated with angiogenesis.

© 2016 by American Journal of Neuroradiology.

Figures

Fig 1.

Cerebral angiogram anteroposterior views of the left internal carotid artery injection in a patient with intracranial atherosclerosis involving the middle cerebral artery that identify innate deep collaterals and leptomeningeal collaterals. Early arterial phase (A) and late arterial phase (B) show stenosis involving the middle cerebral artery (black arrow), with collaterals arising from the medial lenticulostriate arteries and connecting to the lateral lenticulostriate arteries, corresponding to deep collaterals providing flow to the MCA circulation. In the midarterial phase (C) and late arterial phase (D), normal branches of the anterior cerebral artery (blue arrow) are seen extending beyond the normal watershed territory. There is a delay in filling of the MCA branches (black dotted arrow). Leptomeningeal collaterals (red dotted arrow) are seen between the ACA and MCA branches.

Fig 2.

Cerebral angiogram anteroposterior (A and B) and lateral (C and D) views in a patient with Moyamoya disease with narrowing of the middle cerebral artery, identify innate deep collaterals and leptomeningeal collaterals. Early arterial phase (A) and late arterial phase (B) show normal posterior cerebral artery (white arrow), stenosis involving the middle cerebral artery (black arrow), with deep collaterals arising from the anterior choroidal artery (red arrow), providing collateral flow to the MCA, which fills in a delayed fashion (black dotted arrow). Early arterial phase (C) demonstrates deep collaterals from the anterior choroidal artery (red arrow), providing collateral flow to the MCA, which fills in a delayed fashion (black dotted arrow). Late arterial phase (D) shows leptomeningeal collaterals (red dotted arrows) arising from branches of the anterior choroidal artery (white arrow), providing collateral flow to the distal portion of the pericallosal artery (blue arrow), which fills in a delayed fashion. Also visible are leptomeningeal collaterals (red dotted arrows) arising from posterior cerebral artery (white dotted arrow), supplying the distal portion of the callosomarginal artery (blue dotted arrow).

Fig 3.

Isolation of collaterals by dynamic delineation. Selected vessels are followed through the arterial phase of the digital subtraction angiograms to establish continuity of vessels. Vessels are traced and marked, excluding other overlapping or underlying vessels; then they are converted to a binary black and white image. A, Selective postoperative lateral external carotid artery injection. B, Branches of the superficial temporal artery traced and marked. C, Converted binary image.

Fig 4.

A 10,000-pixel-per-box grid is overlaid on the delineated vessels. The branching angioscore is defined as the total number of branching points within a single box. This is measured in all boxes within the grid containing portions of the delineated vessel, and the box with the highest branching angioscore is selected (highlighted in red). A, Innate collaterals. B, EDAS collaterals.

Fig 5.

The artery tortuosity index is measured by using the longest branch of the delineated vessel between 2 branching points. The artery tortuosity index is calculated by the quotient of the actual vessel length and the straight-line distance (red line) of a delineated vessel between 2 branching points. A, Innate collaterals. B, EDAS collaterals.

Fig 6.

Local connected fractal dimension of delineated vessels. The Fraclac plugin for ImageJ selects seed pixels and measures the total number of connected pixels within a predetermined square area. The process is repeated for increasing concentric areas, and the rate of change of connected pixels is used to calculate the LCFD. The process is repeated for each pixel of the delineated vessel. High connectivity is defined as LCFD ≥ 1.2.