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The pathophysiology of brain swelling associated with subdural hemorrhage: the role of the trigeminovascular system

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Abstract

Introduction

This paper reviews the evidence in support of the hypothesis that the trigeminal system mediates brain swelling associated with subdural bleeding. The trigeminovascular system has been extensively studied in migraine; it may play an important but under-recognized role in the response to head trauma. Nerve fibers originating in trigeminal ganglion cells are the primary sensors of head trauma and, through their collateral innervation of the intracranial and dural blood vessels, are capable of inciting a cascade of vascular responses and brain swelling. The extensive trigeminal representation in the brainstem initiates and augments autonomic responses. Blood and tissue injury in the dura incite neurogenic inflammatory responses capable of sensitizing dural nerves and potentiating the response to trauma.

Discussion

The trigeminal system may provide the anatomo-physiological link between small-volume, thin subdural bleeds and swelling of the underlying brain. This physiology may help to explain the poorly understood phenomena of “second-impact syndrome,” the infant response to subdural bleeding (the “big black brain”), as well as post-traumatic subdural effusions. Considerable age-specific differences in the density of dural innervation exist; age-specific responses of this innervation may explain differences in the brain's response to trauma in the young. An understanding of this pathophysiology is crucial to the development of intervention and treatment of these conditions. Antagonists to specific neuropeptides of the trigeminal system modify brain swelling after trauma and should be further explored as potential therapy in brain trauma and subdural bleeding.

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Acknowledgments

We wish to thank those families who gave us consent to study the brains of their babies in order to undertake this work. We thank Mrs. Carolyn Sloan and Joseph Davidson for staining the dural sections and Martha Hansell for drawing Fig. 4. We acknowledge our colleagues, particularly Professor Margaret Esiri and Dr. Monika Hofer, whose comments were most helpful in the preparation of the manuscript.

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  1. Neuropathology, John Radcliffe Hospital, Oxford, UK

    Waney Squier

  2. Department of Radiology, Penn State Hershey Medical Center, Hershey, PA, USA

    Julie Mack

  3. Nuffield Department of Surgical Sciences and Department of Clinical Neurology, John Radcliffe Hospital, Oxford, UK

    Alex Green & Tipu Aziz

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  1. Waney Squier
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Correspondence to Waney Squier.

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Squier, W., Mack, J., Green, A. et al. The pathophysiology of brain swelling associated with subdural hemorrhage: the role of the trigeminovascular system. Childs Nerv Syst 28, 2005–2015 (2012). https://doi.org/10.1007/s00381-012-1870-1

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