Mechanisms of cerebral edema leading to early seizures after traumatic brain injury

Vascular Mechanisms in CNS Trauma

Volumn , Issue , 2014, Pages 29-45

  Iffland, Philip H ^a,b   Grant, Gerald A ^c   Janigro, Damir ^a  

^a Cerebrovascular Research Center   (United States)

^b KENT STATE UNIVERSITY   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84999272488     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4614-8690-9_2     Document Type: Chapter

References (92)

1. Hauser WA (2008) Epidemiology of acute symptomatic seizures. In: Engel G, Pedley TA (eds) Epilepsy: a comprehensive textbook. Lippincott Williams and Wilkins, Philadelphia, PA, pp 71-75
2. Hauser WA, Annegers JF, Kurland LT (1993) Incidence of epilepsy and unprovoked seizures in Rochester, Minnesota: 1935-1984. Epilepsia 34:453-468
3. Marmarou A (2003) Pathophysiology of traumatic brain edema: current concepts. Acta Neurochir Suppl 86:7-10
4. Langendorf FG, Pedley TA, Temkin NR (2008) Posttraumatic seizures. In: Engel G, Pedley TA (eds) Epilepsy: a comprehensive textbook. Lippincott Williams and Wilkins, Philadelphia, PA, pp 2537-2542
5. Salazar AM, Jabbari B, Vance SC, Grafman J, Amin D, Dillon JD (1985) Epilepsy after penetrating head-injury.1. Clinical correlates-a report of the Vietnam Head-Injury Study. Neurology 35:1406-1414
6. Haltiner AM, Temkin NR, Dikmen SS (1997) Risk of seizure recurrence after the first late posttraumatic seizure. Arch Phys Med Rehabil 78:835-840
7. Hesdorffer DC, Benn EK, Cascino GD, Hauser WA (2009) Is a first acute symptomatic seizure epilepsy? Mortality and risk for recurrent seizure. Epilepsia 50:1102-1108
8. Pieracci FM, Moore EE, Beauchamp K, Tebockhorst S, Barnett CC, Bensard DD, Burlew CC, Biffl WL, Stoval RT, Johnson JL (2012) A cost-minimization analysis of phenytoin versus levetiracetam for early seizure pharmacoprophylaxis after traumatic brain injury. J Trauma Acute Care Surg 72:276-281
9. Bullock MR, Povlishock JT (2007) Guidelines for the management of severe traumatic brain injury. Editor's commentary. J Neurotrauma 24(Suppl 1):2
10. Temkin NR, Dikmen SS, Anderson GD, Wilensky AJ, Holmes MD, Cohen W, Newell DW, Nelson P, Awan A, Winn HR (1999) Valproate therapy for prevention of posttraumatic seizures: a randomized trial. J Neurosurg 91:593-600
11. Daneman R (2012) The blood-brain barrier in health and disease. Ann Neurol 72:648-672
12. Cucullo L, Hossain M, Puvenna V, Marchi N, Janigro D (2011) The role of shear stress in blood-brain barrier endothelial physiology. BMC Neurosci 12:40
13. Fung C, Evans E, Shin D, Shin BC, Zhao Y, Sankar R, Chaudhuri G, Devaskar SU (2010) Hypoxic-ischemic brain injury exacerbates neuronal apoptosis and precipitates spontaneous seizures in glucose transporter isoform 3 heterozygous null mice. J Neurosci Res 88:3386-3398
14. Correale J, Villa A (2009) Cellular elements of the blood-brain barrier. Neurochem Res 34:2067-2077
15. Rubin LL, Staddon JM (1999) The cell biology of the blood-brain barrier. Annu Rev Neurosci 22:11-28
16. Janigro D (2012) Are you in or out? Leukocyte, ion, and neurotransmitter permeability across the epileptic blood-brain barrier. Epilepsia 53(Suppl 1):26-34
17. Seiffert E, Dreier JP, Ivens S, Bechmann I, Tomkins O, Heinemann U, Friedman A (2004) Lasting blood-brain barrier disruption induces epileptic focus in the rat somatosensory cortex. J Neurosci 24:7829-7836
18. Janigro D, Gasparini S, D'Ambrosio R, McKhann G, DiFrancesco D (1997) Reduction of K+ uptake in glia prevents long-term depression maintenance and causes epileptiform activity. J Neurosci 17:2813-2824
19. Misonou H (2010) Homeostatic regulation of neuronal excitability by K(+) channels in normal and diseased brains. Neuroscientist 16:51-64
20. Kofuji P, Newman EA (2004) Potassium buffering in the central nervous system. Neuroscience 129:1045-1056
21. Altamirano AA, Russell JM (1987) Coupled Na/K/Cl efflux. "Reverse" unidirectional fluxes in squid giant axons. J Gen Physiol 89:669-686
22. Sweadner KJ (1979) Two molecular forms of (Na+ + K+)-stimulated ATPase in brain. Separation, and difference in affinity for strophanthidin. J Biol Chem 254:6060-6067
23. Gloor SM (1997) Relevance of Na, K-ATPase to local extracellular potassium homeostasis and modulation of synaptic transmission. FEBS Lett 412:1-4
24. Kahle KT, Simard JM, Staley KJ, Nahed BV, Jones PS, Sun D (2009) Molecular mechanisms of ischemic cerebral edema: role of electroneutral ion transport. Physiology (Bethesda) 24:257-265
25. Pannasch U, Vargova L, Reingruber J, Ezan P, Holcman D, Giaume C, Sykova E, Rouach N (2011) Astroglial networks scale synaptic activity and plasticity. Proc Natl Acad Sci U S A 108:8467-8472
26. Ohno Y, Hibino H, Lossin C, Inanobe A, Kurachi Y (2007) Inhibition of astroglial Kir4.1 channels by selective serotonin reuptake inhibitors. Brain Res 1178:44-51
27. Higashi K, Fujita A, Inanobe A, Tanemoto M, Doi K, Kubo T, Kurachi Y (2001) An inwardly rectifying K(+) channel, Kir4.1, expressed in astrocytes surrounds synapses and blood vessels in brain. Am J Physiol Cell Physiol 281:C922-C931
28. Olsen ML, Sontheimer H (2008) Functional implications for Kir4.1 channels in glial biology:from K+ buffering to cell differentiation. J Neurochem 107:589-601
29. Medici V, Frassoni C, Tassi L, Spreafico R, Garbelli R (2011) Aquaporin 4 expression in control and epileptic human cerebral cortex. Brain Res 1367:330-339
30. Nielsen S, Nagelhus EA, Amiry-Moghaddam M, Bourque C, Agre P, Ottersen OP (1997) Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J Neurosci 17:171-180
31. Rash JE, Yasumura T, Hudson CS, Agre P, Nielsen S (1998) Direct immunogold labeling of aquaporin-4 in square arrays of astrocyte and ependymocyte plasma membranes in rat brain and spinal cord. Proc Natl Acad Sci U S A 95:11981-11986
32. Dietzel I, Heinemann U, Hofmeier G, Lux HD (1980) Transient changes in the size of the extracellular space in the sensorimotor cortex of cats in relation to stimulus-induced changes in potassium concentration. Exp Brain Res 40:432-439
33. Ahn AH, Kunkel LM (1995) Syntrophin binds to an alternatively spliced exon of dystrophin. J Cell Biol 128:363-371
34. Connors NC, Kofuji P (2002) Dystrophin Dp71 is critical for the clustered localization of potassium channels in retinal glial cells. J Neurosci 22:4321-4327
35. O'Kane RL, Martinez-Lopez I, DeJoseph MR, Vina JR, Hawkins RA (1999) Na(+)-dependent glutamate transporters (EAAT1, EAAT2, and EAAT3) of the blood-brain barrier. A mechanism for glutamate removal. J Biol Chem 274:31891-31895
36. Hawkins RA (2009) The blood-brain barrier and glutamate. Am J Clin Nutr 90:867S-874S
37. Tanaka K, Watase K, Manabe T, Yamada K, Watanabe M, Takahashi K, Iwama H, Nishikawa T, Ichihara N, Kikuchi T, Okuyama S, Kawashima N, Hori S, Takimoto M, Wada K (1997) Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276:1699-1702
38. Storck T, Schulte S, Hofmann K, Stoffel W (1992) Structure, expression, and functional analysis of a Na(+)-dependent glutamate/aspartate transporter from rat brain. Proc Natl Acad Sci U S A 89:10955-10959
39. Juge O (1982) Physiopathology of brain edema. Schweiz Med Wochenschr 112:956-959
40. Nag S, Manias JL, Stewart DJ (2009) Pathology and new players in the pathogenesis of brain edema. Acta Neuropathol 118:197-217
41. Donkin JJ, Vink R (2010) Mechanisms of cerebral edema in traumatic brain injury: therapeutic developments. Curr Opin Neurol 23:293-299
42. Unterberg AW, Stover J, Kress B, Kiening KL (2004) Edema and brain trauma. Neuroscience 129:1021-1029
43. Fishman RA (1992) Physiology of the cerebrospinal fluid. In: Mills LM (ed) Cerebrospinal fluid in diseases of the nervous system. W.B. Sauners Company, Philadelphia, pp 23-42
44. Asahi M, Wang X, Mori T, Sumii T, Jung JC, Moskowitz MA, Fini ME, Lo EH (2001) Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J Neurosci 21:7724-7732
45. Liu W, Hendren J, Qin XJ, Shen J, Liu KJ (2009) Normobaric hyperoxia attenuates early blood-brain barrier disruption by inhibiting MMP-9-mediated occludin degradation in focal cerebral ischemia. J Neurochem 108:811-820
46. Liu J, Jin X, Liu KJ, Liu W (2012) Matrix metalloproteinase-2-mediated occludin degradation and caveolin-1-mediated claudin-5 redistribution contribute to blood-brain barrier damage in early ischemic stroke stage. J Neurosci 32:3044-3057
47. Shigemori Y, Katayama Y, Mori T, Maeda T, Kawamata T (2006) Matrix metalloproteinase-9 is associated with blood-brain barrier opening and brain edema formation after cortical contusion in rats. Acta Neurochir Suppl 96:130-133
48. Plesnila N, Schulz J, Stoffel M, Eriskat J, Pruneau D, Baethmann A (2001) Role of bradykinin B2 receptors in the formation of vasogenic brain edema in rats. J Neurotrauma 18:1049-1058
49. Geppetti P, Bertrand C, Ricciardolo FL, Nadel JA (1995) New aspects on the role of kinins in neurogenic inflammation. Can J Physiol Pharmacol 73:843-847
50. Trabold R, Eros C, Zweckberger K, Relton J, Beck H, Nussberger J, Muller-Esterl W, Bader M, Whalley E, Plesnila N (2010) The role of bradykinin B(1) and B(2) receptors for secondary brain damage after traumatic brain injury in mice. J Cereb Blood Flow Metab 30:130-139
51. Zweckberger K, Plesnila N (2009) Anatibant, a selective non-peptide bradykinin B2 receptor antagonist, reduces intracranial hypertension and histopathological damage after experimental traumatic brain injury. Neurosci Lett 454:115-117
52. Shakur H, Andrews P, Asser T, Balica L, Boeriu C, Quintero JD, Dewan Y, Druwe P, Fletcher O, Frost C, Hartzenberg B, Mantilla JM, Murillo-Cabezas F, Pachl J, Ravi RR, Ratsep I, Sampaio C, Singh M, Svoboda P, Roberts I (2009) The BRAIN TRIAL: a randomised, placebo controlled trial of a Bradykinin B2 receptor antagonist (Anatibant) in patients with traumatic brain injury. Trials 10:109
53. Donkin JJ, Nimmo AJ, Cernak I, Blumbergs PC, Vink R (2009) Substance P is associated with the development of brain edema and functional deficits after traumatic brain injury. J Cereb Blood Flow Metab 29:1388-1398
54. Zacest AC, Vink R, Manavis J, Sarvestani GT, Blumbergs PC (2010) Substance P immunoreactivity increases following human traumatic brain injury. Acta Neurochir Suppl 106:211-216
55. Brain SD, Williams TJ (1985) Inflammatory oedema induced by synergism between calcitonin gene-related peptide (CGRP) and mediators of increased vascular permeability. Br J Pharmacol 86:855-860
56. Figaji AA, Zwane E, Fieggen AG, Argent AC, Le Roux PD, Siesjo P, Peter JC (2009) Pressure autoregulation, intracranial pressure, and brain tissue oxygenation in children with severe traumatic brain injury. J Neurosurg Pediatr 4:420-428
57. Soares HD, Hicks RR, Smith D, McIntosh TK (1995) Inflammatory leukocytic recruitment and diffuse neuronal degeneration are separate pathological processes resulting from traumatic brain injury. J Neurosci 15:8223-8233
58. Marchi N, Bazarian JJ, Puvenna V, Janigro M, Ghosh C, Zhong J, Zhu T, Blackman E, Stewart D, Ellis J, Butler R, Janigro D (2013) Consequences of repeated blood-brain barrier disruption in football players. PLoS One 8(3):e56805
59. Campbell M, Hanrahan F, Gobbo OL, Kelly ME, Kiang AS, Humphries MM, Nguyen AT, Ozaki E, Keaney J, Blau CW, Kerskens CM, Cahalan SD, Callanan JJ, Wallace E, Grant GA, Doherty CP, Humphries P (2012) Targeted suppression of claudin-5 decreases cerebral oedema and improves cognitive outcome following traumatic brain injury. Nat Commun 3:849
60. Garcia JH, Liu KF, Yoshida Y, Chen S, Lian J (1994) Brain microvessels: factors altering their patency after the occlusion of a middle cerebral artery (Wistar rat). Am J Pathol 145:728-740
61. Liang D, Bhatta S, Gerzanich V, Simard JM (2007) Cytotoxic edema: mechanisms of pathological cell swelling. Neurosurg Focus 22:E2
62. Simard JM, Kent TA, Chen M, Tarasov KV, Gerzanich V (2007) Brain oedema in focal ischaemia: molecular pathophysiology and theoretical implications. Lancet Neurol 6:258-268
63. Rumpel H, Nedelcu J, Aguzzi A, Martin E (1997) Late glial swelling after acute cerebral hypoxia-ischemia in the neonatal rat: a combined magnetic resonance and histochemical study. Pediatr Res 42:54-59
64. Su G, Kintner DB, Flagella M, Shull GE, Sun D (2002) Astrocytes from Na(+)-K(+)-Cl(_) cotransporter-null mice exhibit absence of swelling and decrease in EAA release. Am J Physiol Cell Physiol 282:C1147-C1160
65. Rao VL, Baskaya MK, Dogan A, Rothstein JD, Dempsey RJ (1998) Traumatic brain injury down-regulates glial glutamate transporter (GLT-1 and GLAST) proteins in rat brain. J Neurochem 70:2020-2027
66. Neusch C, Weishaupt JH, Bahr M (2003) Kir channels in the CNS: emerging new roles and implications for neurological diseases. Cell Tissue Res 311:131-138
67. Obrenovitch TP, Urenjak J (1997) Is high extracellular glutamate the key to excitotoxicity in traumatic brain injury? J Neurotrauma 14:677-698
68. Kristian T, Siesjo BK (1998) Calcium in ischemic cell death. Stroke 29:705-718
69. Kauppinen RA, Enkvist K, Holopainen I, Akerman KE (1988) Glucose deprivation depolarizes plasma membrane of cultured astrocytes and collapses transmembrane potassium and glutamate gradients. Neuroscience 26:283-289
70. Manley GT, Fujimura M, Ma T, Noshita N, Filiz F, Bollen AW, Chan P, Verkman AS (2000) Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat Med 6:159-163
71. Baraban SC, Schwartzkroin PA (1998) Effects of hyposmolar solutions on membrane currents of hippocampal interneurons and mossy cells in vitro. J Neurophysiol 79:1108-1112
72. Fazio V, Bhudia SK, Marchi N, Aumayr B, Janigro D (2004) Peripheral detection of S100beta during cardiothoracic surgery: what are we really measuring? Ann Thorac Surg 78:46-52
73. Kanner AA, Marchi N, Fazio V, Mayberg MR, Koltz MT, Siomin V, Stevens GH, Masaryk T, Ayumar B, Vogelbaum MA, Barnett GH, Janigro D (2003) Serum S100beta: a noninvasive marker of blood-brain barrier function and brain lesions. Cancer 97:2806-2813
74. Vogelbaum MA, Masaryk T, Mazzone P, Mekhail T, Fazio V, McCartney S, Marchi N, Kanner A, Janigro D (2005) S100beta as a predictor of brain metastases: brain versus cerebrovascular damage. Cancer 104:817-824
75. Kapural M, Krizanac-Bengez L, Barnett G, Perl J, Masaryk T, apollo D, Rasmussen P, Mayberg MR, Janigro D (2002) Serum S-100beta as a possible marker of blood-brain barrier disruption. Brain Res 940:102-104
76. Begaz T, Kyriacou DN, Segal J, Bazarian JJ (2006) Serum biochemical markers for postconcussion syndrome in patients with mild traumatic brain injury. J Neurotrauma 23:1201-1210
77. Blyth B, Farahvar A, He H, Nayak A, Yang C, Shaw G, Bazarian JJ (2011) Elevated serum ubiquitin carboxy-terminal hydrolase L1 is associated with abnormal blood brain barrier function after traumatic brain injury. J Neurotrauma 28:2453-2462
78. Blyth BJ, Farhavar A, Gee C, Hawthorn B, He H, Nayak A, Stocklein V, Bazarian JJ (2009) Validation of serum markers for blood-brain barrier disruption in traumatic brain injury. J Neurotrauma 26:1497-1507
79. Biberthaler P, Mussack T, Wiedemann E, Kanz KG, Koelsch M, Gippner-Steppert C, Jochum M (2001) Evaluation of S-100b as a specific marker for neuronal damage due to minor head trauma. World J Surg 25:93-97
80. Bechmann I, Galea I, Perry VH (2007) What is the blood-brain barrier (not)? Trends Immunol 28:5-11
81. Galea I, Bechmann I, Perry VH (2007) What is immune privilege (not)? Trends Immunol 28:12-18
82. Chang GC, Young LH (2011) Sympathetic ophthalmia. Semin Ophthalmol 26:316-320
83. Gold M, Pul R, Bach JP, Stangel M, Dodel R (2012) Pathogenic and physiological autoantibodies in the central nervous system. Immunol Rev 248:68-86
84. Popovich PG, Stokes BT, Whitacre CC (1996) Concept of autoimmunity following spinal cord injury: possible roles for T lymphocytes in the traumatized central nervous system. J Neurosci Res 45:349-363
85. Fujinami RS, Oldstone MB (1985) Amino acid homology between the encephalitogenic site of myelin basic protein and virus: mechanism for autoimmunity. Science 230:1043-1045
86. Lang HL, Jacobsen H, Ikemizu S, Andersson C, Harlos K, Madsen L, Hjorth P, Sondergaard L, Svejgaard A, Wucherpfennig K, Stuart DI, Bell JI, Jones EY, Fugger L (2002) A functional and structural basis for TCR cross-reactivity in multiple sclerosis. Nat Immunol 3:940-943
87. Prochazka M, Voltnerova M, Stefan J (1971) Studies of immunologic reactions after brain injury. II. Antibodies against brain tissue lipids after blunt head injury in man. Int Surg 55:322-326
88. Lopez-Escribano H, Minambres E, Labrador M, Bartolome MJ, Lopez-Hoyos M (2002) Induction of cell death by sera from patients with acute brain injury as a mechanism of production of autoantibodies. Arthritis Rheum 46:3290-3300
89. Skoda D, Kranda K, Bojar M, Glosova L, Baurle J, Kenney J, Romportl D, Pelichovska M, Cvachovec K (2006) Antibody formation against beta-tubulin class III in response to brain trauma. Brain Res Bull 68:213-216
90. Granata T, Gobbi G, Spreafico R, Vigevano F, Capovilla G, Ragona F, Freri E, Chiapparini L, Bernasconi P, Giordano L, Bertani G, Casazza M, Dalla BB, Fusco L (2003) Rasmussen's encephalitis: early characteristics allow diagnosis. Neurology 60:422-425
91. Michalak Z, Lebrun A, Di Miceli M, Rousset MC, Crespel A, Coubes P, Henshall DC, Lerner-Natoli M, Rigau V (2012) IgG leakage may contribute to neuronal dysfunction in drug-refractory epilepsies with blood-brain barrier disruption. J Neuropathol Exp Neurol 71:826-838
92. Bargestock E, Puvenna V, Iffland P, Falcone T, Hossain M, Vetter S, Man S, Dickstein L, Carvalho-Tavares J, Marchi N, Janigro D (2013) Is peripheral immunity regulated by blood-brain barrier permeability changes? BMC Neurosci