CLINICAL PATHOPHYSIOLOGY OF CEREBRAL EDEMA (part 2)
https://doi.org/10.21292/2078-5658-2017-14-4-52-60
Abstract
The article gives the updated understanding of the physiology of cerebral fluid exchange and pathophysiology of cerebral edema. The first part of the article has been devoted to a description of the mechanisms of fluid and electrolyte exchange in health and the second part describes pathophysiological aspects of cerebral edema development, going through certain stages. A cytotoxic edema is the first stage when fluid is redistributed between spaces. It is followed by the sodium deficiency in the interstitium resulting in the development of the second stage - an ionic edema characterized only by functional disorders of hematoencephalic barrier. The consequent anatomic disorder of hematoencephalic barrier results in the development of a vasogenic edema and transfer to the stage of hemorrhagic transformation. Understanding the mechanism of the brain edema development provides new prospectives of the management of this state.
About the Authors
A. A. ZadvornovRussian Federation
Anesthesiologist and Emergency Physician
A. V. Golomidov
Russian Federation
Candidate of Medical Sciences, Head of Anesthesiology and Intensive Care Department for Newborns
E. V. Grigoriev
Russian Federation
Doctor of Medical Sciences, Professor, Deputy Director for Research and Therapy
References
1. Amiry-Moghaddam M., Otsuka T., Hurn P.D., Traystman R.J., Haug F.M., Froehner S.C., Adams M.E., Neely J.D., Agre P., Ottersen O.P., Bhardwaj A. An alpha-syntrophin-dependent pool of AQP4 in astroglial end-feet confers bidirectional water flow between blood and brain. Proc. Natl. Acad. Sci USA, 2003, vol. 100, no. 4, pp. 2106-2111.
2. Bell B.A., Symon L., Branston N.M. CBF and time thresholds for the formation of ischemic cerebral edema, and effect of reperfusion in baboons. J. Neurosurg., 1985, vol. 62, no. 1, pp. 31-41.
3. Castejón O.J. Increased vesicular and vacuolar transendothelial transport in traumatic human brain oedema. A review. Folia Neuropathol., 2013, vol. 51, no. 2, pp. 93-102.
4. Chen H., Luo J., Kintner D.B., Shull G.E., Sun D. Na+-dependent chloride transporter (NKCC1)-null mice exhibit less gray and white matter damage after focal cerebral ischemia. J. Cereb. Blood Flow Metab., 2005, vol. 25, no. 1, pp. 54-66.
5. Chen H., Sun D. The role of Na-K-Cl co-transporter in cerebral ischemia. Neurol Res., 2005, vol. 27, no. 3, pp. 280-286.
6. Crompton E.M., Lubomirova I., Cotlarciuc I., Han T.S., Sharma S.D., Sharma P. Meta-analysis of therapeutic hypothermia for traumatic brain injury in adult and pediatric patients. Crit. Care Med., 2017, vol. 45, no. 4, pp. 575-583.
7. Durward Q.J., Del Maestro R.F., Amacher A.L., Farrar J.K. The influence of systemic arterial pressure and intracranial pressure on the development of cerebral vasogenic edema. J. Neurosurg., 1983, vol. 59, no. 5, pp. 803-809.
8. Elfeber K., Köhler A., Lutzenburg M., Osswald C., Galla H.J., Witte O.W., Koepsell H. Localization of the Na+-D-glucose cotransporter SGLT1 in the blood-brain barrier. Histochem Cell Biol., 2004, vol. 121, no. 3, pp. 201-207.
9. Ferrazzano P., Shi Y., Manhas N., Wang Y., Hutchinson B., Chen X., Chanana V., Gerdts J., Meyerand M.E., Sun D. Inhibiting the Na+/H+ exchanger reduces reperfusion injury: a small animal MRI study. Front Biosci (Elite Ed), 2011, vol. 3, pp. 81-88.
10. Fischer S., Wobben M., Marti H.H., Renz D., Schaper W. Hypoxia-induced hyperpermeability in brain microvessel endothelial cells involves VEGF-mediated changes in the expression of zonula occludens-1. Microvasc. Res., 2002, vol. 63, no. 1, pp. 70-80.
11. Fukuda S., Fini C.A., Mabuchi T., Koziol J.A., Eggleston L.L.Jr., del Zoppo G.J. Focal cerebral ischemia induces active proteases that degrade microvascular matrix. Stroke, 2004, vol. 35, no. 4, pp. 998-1004.
12. Gerzanich V., Woo S.K., Vennekens R., Tsymbalyuk O., Ivanova S., Ivanov A., Geng Z., Chen Z., Nilius B., Flockerzi V., Freichel M., Simard J.M. De novo expression of Trpm4 initiates secondary hemorrhage in spinal cord injury. Nat. Med., 2009, vol. 15, no. 2, pp. 185-191.
13. Haj-Yasein N.N., Vindedal G.F., Eilert-Olsen M., Gundersen G.A., Skare Ø., Laake P., Klungland A., Thorén A.E., Burkhardt J.M., Ottersen O.P., Nagelhus E.A. Glial-conditional deletion of aquaporin-4 (Aqp4) reduces blood-brain water uptake and confers barrier function on perivascular astrocyte endfeet. Proc. Natl. Acad. Sci. USA, 2011, vol. 108, no. 43, pp. 17815-17820.
14. Hamann G.F., del Zoppo G.J., von Kummer R. Hemorrhagic transformation of cerebral infarction-possible mechanisms. Thromb Haemost., 1999, vol. 82, suppl. 1, pp. 92-94.
15. Hansson E., Muyderman H., Leonova J., Allansson L., Sinclair J., Blomstrand F., Thorlin T., Nilsson M., Rönnbäck L. Astroglia and glutamate in physiology and pathology: aspects on glutamate transport, glutamate-induced cell swelling and gap-junction communication. Neurochem. Int., 2000, vol. 37, no. 2-3, pp. 317-329.
16. Hirt L., Price M., Ternon B., Mastour N., Brunet J.F., Badaut J. Early induction of AQP4 contributes the limitation of the edema formation in the brain ischemia. J. Cereb. Blood Flow Metab., 2009, vol. 29, pp. 423-433.
17. Hofmeijer J., Schepers J., Veldhuis W.B., Nicolay K., Kappelle L.J., Bär P.R., van der Worp H.B. Delayed decompressive surgery increases apparent diffusion coefficient and improves peri-infarct perfusion in rats with space-occupying cerebral infarction. Stroke, 2004, vol. 35, no. 6, pp. 1476-1481.
18. Klatzo I. Presidental address. Neuropathological aspects of brain edema. J. Neuropathol. Exp. Neurol., 1967, vol. 26, no. 1, pp. 1-14.
19. Laposata M., Dovnarsky D.K., Shin H.S. Thrombin-induced gap formation in confluent endothelial cell monolayers in vitro. Blood, 1983, vol. 62, no. 3, pp. 549-556.
20. Lu K.T., Huang T.C., Tsai Y.H., Yang Y.L. Transient receptor potential vanilloid type 4 channels mediate Na-K-Cl-co-transporter-induced brain edema after traumatic brain injury. J. Neurochem., 2017, vol. 140, no. 5, pp. 718-727.
21. Monro S.A. Observations on the structure and function of the nervous system. Edinburgh, W Creech, 1783, pp. 2-8.
22. Mori K., Nakao Y., Yamamoto T., Maeda M. Early external decompressive craniectomy with duroplasty improves functional recovery in patients with massive hemispheric embolic infarction: timing and indication of decompressive surgery for malignant cerebral infarction. Surg. Neurol., 2004, vol. 62, no. 5, pp. 420-429.
23. Nag S., Kapadia A., Stewart D.J. Review: molecular pathogenesis of blood-brain barrier breakdown in acute brain injury. Neuropathol Appl. Neurobiol., 2011, vol. 37, no. 1, pp. 3-23.
24. O'Donnell M.E., Tran L., Lam T.I., Liu X.B., Anderson S.E. Bumetanide inhibition of the blood-brain barrier Na-K-Cl cotransporter reduces edema formation in the rat middle cerebral artery occlusion model of stroke. J. Cereb. Blood Flow Metab., 2004, vol. 24, no. 9, pp. 1046-1056.
25. Papadopoulos M. C., Verkman A. S. Aquaporin-4 gene disruption in mice reduces brain swelling and mortality in pneumococcal meningitis. J. Biol. Chem., 2005, vol. 280, no. 14, pp. 13906-13912.
26. Piazza M., Munasinghe J., Murayi R., Edwards N., Montgomery B., Walbridge S., Merrill M., Chittiboina P. Simulating vasogenic brain edema using chronic VEGF infusion. J. Neurosurg., 2017, vol. 6, pp. 1-12.
27. Rao K.V., Reddy P.V., Curtis K.M., Norenberg M.D. Aquaporin-4 expression in cultured astrocytes after fluid percussion injury. J. Neurotrauma, 2011, vol. 28, no. 3, pp. 371-381.
28. Reichardt M. Hirnschwellung. Allg. Z. Psychiatr., 1919, vol. 75, pp. 34-103.
29. Ren Z., Iliff J.J., Yang L., Yang J., Chen X., Chen M.J., Giese R.N., Wang B., Shi X., Nedergaard M. 'Hit & Run' model of closed-skull traumatic brain injury (TBI) reveals complex patterns of post-traumatic AQP4 dysregulation. J. Cereb. Blood Flow Metab., 2013, vol. 33, pp. 834-845.
30. Saadoun S., Papadopoulos M.C., Watanabe H., Yan D., Manley G.T., Verkman A.S. Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. J. Cell. Sci., 2005, vol. 118, pp. 5691-5698.
31. Simard J.M., Yurovsky V., Tsymbalyuk N., Melnichenko L., Ivanova S., Gerzanich V. Protective effect of delayed treatment with low-dose glibenclamide in three models of ischemic stroke. Stroke, 2009, vol. 40, no. 2, pp. 604-609.
32. Solenov E., Watanabe H., Manley G.T., Verkman A.S. Sevenfold-reduced osmotic water permeability in primary astrocyte cultures from AQP-4-deficient mice, measured by a fluorescence quenching method. Am. J. Physiol. Cell. Physiol., 2004, vol. 286, no. 2, pp. 426-432.
33. Song L., Pachter J.S. Monocyte chemoattractant protein-1 alters expression of tight junction-associated proteins in brain microvascular endothelial cells. Microvasc. Res., 2004, vol. 67, no. 1, pp. 78-89.
34. Stokum J.A., Gerzanich V., Simard J.M. Molecular pathophysiology of cerebral edema. J. Cereb. Blood Flow Metab., 2016, vol. 36, no. 3, pp. 513-538.
35. Stokum J.A., Kurland D.B., Gerzanich V., Simard J.M. Mechanisms of astrocyte-mediated cerebral edema. Neurochem. Res., 2015, vol. 40, no. 2, pp. 317-328.
36. Su G., Kintner D.B., Flagella M., Shull G.E., Sun D. Astrocytes from Na+-K+-Cl- cotransporter-null mice exhibit absence of swelling and decrease in EAA release. Am. J. Physiol. Cell. Physiol., 2002, vol. 282, no. 5, pp. 1147-1160.
37. Suzuki Y., Matsumoto Y., Ikeda Y., Kondo K., Ohashi N., Umemura K. SM-20220, a Na+/H+ exchanger inhibitor: effects on ischemic brain damage through edema and neutrophil accumulation in a rat middle cerebral artery occlusion model. Brain. Res., 2002, vol. 945, no. 2, pp. 242-248.
38. Tao-Cheng J.H., Brightman M.W. Development of membrane interactions between brain endothelial cells and astrocytes in vitro. Int. J. Dev. Neurosci., 1988, vol. 6, no. 1, pp. 25-37.
39. Thrane A.S., Rangroo Thrane V., Nedergaard M. Drowning stars: reassessing the role of astrocytes in brain edema. Trends Neurosci., 2014, vol. 37, no. 11, pp. 620-628.
40. Tourdias T., Mori N., Dragonu I., Cassagno N., Boiziau C., Aussudre J., Brochet B., Moonen C., Petry K.G., Dousset V. Differential aquaporin 4 expression during edema build-up and resolution phases of brain inflammation. J. Neuroinflammation, 2011, vol. 8, pp. 143.
41. Whytt R. Observations on the Dropsy in the brain. Edinburgh, J. Balfour, 1768, pp. 49-95.
42. Xu M., Su W., Xu Q.P. Aquaporin-4 and traumatic brain edema. Clin. J. Traumatol., 2010, vol. 13, no. 2, pp. 103-110.
43. Yamagata K., Tagami M., Takenaga F., Yamori Y., Itoh S. Hypoxia-induced changes in tight junction permeability of brain capillary endothelial cells are associated with IL-1beta and nitric oxide. Neurobiol. Dis., 2004, vol. 17, no. 3, pp. 491-499.
44. Yan Y., Dempsey R.J., Flemmer A., Forbush B., Sun D. Inhibition of Na+-K+-Cl- cotransporter during focal cerebral ischemia decreases edema and neuronal damage. Brain. Res., 2003, vol. 961, no. 1, pp. 22-31.
45. Yang B., Zador Z., Verkman A.S. Glial cell aquaporin-4 overexpression in transgenic mice accelerates cytotoxic brain swelling. J. Biol. Chem., 2008, vol. 283, pp. 15280-15286.
46. Yang Y., Estrada E.Y., Thompson J.F., Liu W., Rosenberg G.A. Matrix metalloproteinase-mediated disruption of tight junction proteins in cerebral vessels is reversed by synthetic matrix metalloproteinase inhibitor in focal ischemia in rat. J. Cereb. Blood Flow Metab., 2007, vol. 27, no. 4, pp. 697-709.
Review
For citations:
Zadvornov A.A., Golomidov A.V., Grigoriev E.V. CLINICAL PATHOPHYSIOLOGY OF CEREBRAL EDEMA (part 2). Messenger of ANESTHESIOLOGY AND RESUSCITATION. 2017;14(4):52-60. (In Russ.) https://doi.org/10.21292/2078-5658-2017-14-4-52-60