Role of Blood Clot Formation on Early Edema Development After Experimental Intracerebral Hemorrhage

Author:

Xi Guohua1,Wagner Kenneth R.1,Keep Richard F.1,Hua Ya1,de Courten-Myers Gabrielle M.1,Broderick Joseph P.1,Brott Thomas G.1,Hoff Julian T.1

Affiliation:

1. From the Department of Surgery (Neurosurgery) (G.X., R.F.K., J.T.H.), University of Michigan, Ann Arbor, Mich; the Departments of Neurology (K.R.W., Y.H., J.P.B., T.G.B.) and Pathology and Laboratory Medicine (G.M. de C.-M.), University of Cincinnati College of Medicine, Cincinnati, Ohio; and the Medical Research Service (K.R.W.), Department of Veterans Affairs Medical Center, Cincinnati, Ohio.

Abstract

Background and Purpose —Blood “toxicity” is hypothesized to induce edema and brain tissue injury following intracerebral hemorrhage (ICH). Lobar ICH in pigs produces rapidly developing, marked perihematomal edema (>10% increase in water content) associated with clot-derived plasma protein accumulation. Coagulation cascade activation and, specifically, thrombin itself contribute to edema development during the first 24 hours after gray matter ICH in rats. In the present study, we sought to determine whether blood clot formation is necessary for edema development by comparing intracerebral infusions of heparinized and unheparinized blood in pig (white matter) and in rat (gray matter). We also examined heparin’s effect on thrombin-induced gray matter edema. Methods —In pigs, we infused autologous blood (with or without heparin) into the cerebral white matter to produce lobar hematomas and froze the brains in situ at 1, 4, or 24 hours after ICH. We determined hematomal and perihematomal edema volumes on coronal sections by computer-assisted morphometry. In rats, we infused either blood or thrombin (with or without heparin) into the basal ganglia and measured water, sodium, and potassium contents at 24 hours after ICH. Results —In pigs, unheparinized blood induced rapid (at 1 hour) and prolonged (24 hours) perihematomal edema (average volume, 1.29±0.20 mL; n=6). No perihematomal edema was present following heparinized blood infusions (n=6). In rats, unheparinized blood produced significantly greater edema than heparinized blood infusions. As with whole blood, thrombin-induced gray matter edema at 24 hours was significantly reduced by coinjection of heparin. Conclusions —After ICH, blood clot formation is required for rapid and prolonged edema development in perihematomal white and gray matter. Thrombin also contributes to prolonged edema in gray matter.

Publisher

Ovid Technologies (Wolters Kluwer Health)

Subject

Advanced and Specialized Nursing,Cardiology and Cardiovascular Medicine,Neurology (clinical)

Reference30 articles.

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3. Suzuki J Ebina T. Sequential changes in tissue surrounding ICH. In: Pia HW Longmaid C Zierski J eds. Spontaneous Intracerebral Hematomas: Advances in Diagnosis and Therapy. Berlin Germany: Springer; 1980:121–128.

4. Experimental intracerebral hemorrhage: effects of a temporary mass lesion

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