The role of neuroeffector mechanisms in cerebral hyperperfusion syndromes

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✓ Cerebral hyperperfusion, a state in which blood flow exceeds the metabolic needs of brain, may complicate a number of neurological and neurosurgical conditions. It may account for the propensity with which hemorrhage, cerebral edema, or seizures follow embolic stroke, carotid endarterectomy, or the excision of large arteriovenous malformations, and for some of the morbidity that accompanies acute severe head injury, prolonged seizures, and acute severe hypertension. Hyperperfusion syndromes have in common acute increases in blood pressure, vasodilatation, breakdown of the blood-brain barrier, and the development of cerebral edema. These common features suggest the possibility that they share the same pathogenic mechanisms. It was believed until recently that reactive hyperemia was caused primarily by the generation of vasoactive metabolites, which induced vasodilatation through relaxation of vascular smooth muscle. However, the authors have recently established that the release of vasoactive neuropeptides from perivascular sensory nerves via axon reflex-like mechanisms has a significant bearing upon a number of hyperperfusion syndromes. In this article, the authors summarize their data and discuss possible therapeutic implications for blockade of these nerves or their constituent neuropeptides.

Article Information

Address for Drs. Wei and Kontos=Division of Cardiology, Department of Medicine, Medical College of Virginia, Richmond, Virginia 23298.Address reprint requests to: Michael A. Moskowitz, M.D., Stroke Research Laboratory, Massachusetts General Hospital, Boston, Massachusetts 02114.

© AANS, except where prohibited by US copyright law.

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Figures

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    Diagram showing trigeminal innervation of the circle of Willis based on retrograde axonal tracing studies, immunohistochemical tracing, and lesioning experiments in cats and rats.90,91,132 The pattern of innervation is conserved across species and would be expected to be the same in man based on clinical observations, if similar tracing studies were possible. The anterior, middle (MCA), and posterior (PCA) cerebral arteries receive nerve fibers from ganglion cells located predominantly within the first trigeminal division (V1). Single ganglion cells send axonal projections that branch extensively and innervate more than a single artery. The proximal two-thirds of the basilar artery and vertebral arteries are innervated by upper cervical dorsal root ganglia. MMA = middle meningeal artery; CNS = central nervous system; ICA = internal carotid artery; SCA = superior cerebellar artery; AICA = anterior inferior cerebellar artery; X = vagus nerve; C1, C2, C3 = cervical segments 1, 2, 3, respectively. (Reproduced from Moskowitz MA: Sensory connections to cephalic blood vessels and their possible importance to vascular headaches, in Rose FC (ed): Advances in Headache Research. London: John Libbey & Co, 1987, pp 81–86, with permission.)

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    Electron micrographs of cat pial artery, a: Section showing a nerve fascicle containing unmyelinated axons possessing multiple clear vesicles (solid arrows) adjacent to one immunopositive axon (open arrow). × 18,000; bar = 1 µm. b=Section showing a substance P-positive axon and an immunonegative axon in close proximity to vascular smooth muscle. Immunonegative axon contains large granular vesicles (g). Synaptic contacts or junctional complexes were not observed between fibers or terminal axons. Sm = smooth muscle: m = mitochondria; v = vesicles within smooth muscles, × 12,045; bar = 1 µm. (Reprinted from Liu-Chen LY, Liszczak TM, King JC, et al: Immunoelectron microscopic study of substance P-containing fibers in feline cerebral arteries. Brain Res 369:12–20, 1986, with permission.)

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    Release of substance P in vitro from nerve endings surrounding bovine pial vessels following superfusion with potassium by calcium-dependent mechanisms. Substance P release was also demonstrable during superfusion with 20 mm potassium or with 1 µM capsaicin. (Reprinted from Moskowitz MA, Brody M, Liu-Chen LY: In vitro release of immunoreactive substance P from putative afferent nerve endings in bovine pia arachnoid. Neuroscience 9:809–814, 1983, with permission.)

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    Graph showing that chronic left trigeminal ganglionectomy attenuates postischemic hyperperfusion in the middle cerebral artery (MCA) cortical gray matter of eight cats by approximately 50% (** = p < 0.01); however, resting cerebral blood flow and flow during postischemic hypoperfusion are not influenced significantly. Global ischemia was induced for 10 minutes by four-vessel occlusion combined with systemic hypotension. Blood flow was measured using radiolabeled microspheres. Only small differences between the intact and denervated hemisphere were seen in the cortical white matter which, although supplied by the same vascular territory, receives a minor trigeminal innervation. (Reprinted from Macfarlane R, Tasdemiroglu E, Moskowitz MA, et al: Chronic trigeminal ganglionectomy or topical capsaicin application to pial vessels attenuates postocclusive hyperemia but does not influence postischemic hypoperfusion. J Cereb Blood Flow Metab 11:261–271, 1991, with permission.)

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    Graph showing that pial cortical arterioles (46 to 175 µm) from seven cats dilate in response to topical acetylcholine (ACh), an endothelium-dependent vasodilator, when applied under resting conditions. However, the same dose elicits a vasoconstrictor response for the first 60 minutes of reperfusion following 10 minutes of global cerebral ischemia, indicating transient loss of endothelium-dependent relaxing factor (EDRF) reaction. Therefore, non-EDRF vasodilators must mediate the neurogenic component of postischemic hyperperfusion. Data represent the mean ± standard deviation.

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