Occlusive hyperemia: a theory for the hemodynamic complications following resection of intracerebral arteriovenous malformations

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✓ An alternative theory is proposed to explain the brain edema and hemorrhage that may occur after resection of high-flow intracerebral arteriovenous malformations (AVM's). This theory, termed “occlusive hyperemia,” is based on a retrospective analysis of operative dictations along with postoperative imaging studies (191 angiograms and 273 computerized tomography scans) in 295 cases of intracerebral AVM's operated on at the Mayo Clinic between 1970 and 1990. In this series, 34 cases (12%) of postoperative deterioration were documented, of which 15 were due to incomplete resection of the AVM. Of the remaining 19 cases, six had brain edema alone and 13 had hemorrhage with edema, despite complete excision of the AVM. In these 19 cases, the AVM's were greater than 6 cm in diameter in 10 patients, between 3 and 6 cm in six, and less than 3 cm in three. Obstruction of the venous drainage system was observed in 14 (74%) of the 19 cases. Ten of these 14 were due to obstruction of the primary venous drainage of the brain parenchyma immediately surrounding the lesions, while four were due to obstruction of other venous structures. In no case was a rapid circulation identified on postoperative angiograms. The flow pattern was slow or stagnant in former AVM feeders and their parenchymal branches. It is proposed that postoperative intracranial hemorrhage and/or brain edema in AVM patients may be due to: 1) obstruction of the venous outflow system of brain adjacent to the AVM, with subsequent passive hyperemia and engorgement; and 2) stagnant arterial flow in former AVM feeders and their parenchymal branches, with subsequent worsening of the existing hypoperfusion, ischemia, and hemorrhage or edema into these areas. Supportive hemodynamic evidence for this theory was derived from the literature.

Article Information

Address reprint requests to: Nayef R. F. Al-Rodhan, M.D., Ph.D., Department of Neurosurgery, Mayo Clinic, 200 First Street SW, Rochester, Minnesota 55905.

© AANS, except where prohibited by US copyright law.

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Figures

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    Diagrammatic summary of cases that deteriorated postoperatively despite complete arteriovenous malformation (AVM) resection and the relative frequency of venous obstruction in those cases.

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    Case I. Preoperative right common carotid angiograms, anteroposterior (left) and lateral (right) views, demonstrating a large right midposterior temporal arteriovenous malformation and a 7-mm middle cerebral artery aneurysm. Note the large draining cortical vein in the posterior temporo-occipital region (arrow).

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    Case 1. Left: Nonenhanced postoperative computerized tomography scan, obtained after evacuation of the hematoma, showing thrombus in the right posterior temporo-occipital draining cortical vein (arrow) depicted in Fig. 2. Note the surrounding edema/venous infarction and mild mass effect. Center: Postoperative right common carotid angiogram demonstrating no residual arteriovenous malformation (AVM). Right: Postoperative left vertebral angiogram demonstrating stagnant arterial flow and no residual AVM. Note retrograde filling of the angular branch of the middle cerebral artery (arrowhead).

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    Case 2. Preoperative left vertebral angiograms demonstrating a left posterior cerebral artery fistula in the left posterior temporo-occipital region. There are multiple draining veins in the left occipito-inferior parietal lobes and over the left cerebral convexity. Note the enlarged left posterior cerebral artery.

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    Case 2. Left: Postoperative computerized tomography (CT) scan demonstrating enhancement in the draining veins consistent with stagnant flow and/or thrombosis and low attenuation changes in the parietal lobe consistent with edema/venous infarction. Multiple areas of calcification were present on the preoperative CT (not shown). The low attenuation resolved over a period of several weeks. Right: Postoperative left vertebral angiogram demonstrating successful clipping of the left posterior cerebral artery arteriovenous fistula. Stagnant flow was noted in the left posterior cerebral circulation proximal to the clip.

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    Diagrammatic representation of the proposed theory of occlusive hyperemia over three stages: preoperative (A), intraoperative (B), and postoperative (C).

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