Development of post-traumatic epilepsy after controlled cortical impact and lateral fluid-percussion-induced brain injury in the mouse

Journal of Neurotrauma

Volumn 29, Issue 5, 2012, Pages 789-812

  Bolkvadze, Tamuna ^a   Pitkänen, Asla ^a,b  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b KUOPIO UNIVERSITY HOSPITAL   (Finland)

Author keywords

electroencephalogram; epilepsy; post traumatic seizure; traumatic brain injury

Indexed keywords

PENTETRAZOLE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROENCEPHALOGRAPHY; EPILEPTIC DISCHARGE; EPILEPTOGENESIS; HIPPOCAMPUS; HISTOPATHOLOGY; MALE; MORTALITY; MOUSE; NONHUMAN; TRAUMATIC BRAIN INJURY; TRAUMATIC EPILEPSY;

ANIMALS; BRAIN INJURIES; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; EPILEPSY, POST-TRAUMATIC; MALE; MICE; MICE, INBRED C57BL;

EID: 84858419592     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2011.1954     Document Type: Article

References (81)

1. Akasu, T., Muraoka, N., and Hasuo, H. (2002). Hyperexcitability of hippocampal CA1 neurons after fluid percussion injury of the rat cerebral cortex. Neurosci. Lett. 329, 305-308. (Pubitemid 35245348)
2. Andelic, N., Hammergren, N., Bautz-Holter, E., Sveen, U., Brunborg, C., and Røe, C. (2009). Functional outcome and health-related quality of life 10 years after moderate-to-severe traumatic brain injury. Acta Neurol. Scand. 120, 16-23.
3. Anderson, G.D., Temkin, N.R., Dikmen, S.S., Diaz-Arrastia, R., Machamer, J.E., Farhrenbruch, C., Miller, J.W., and Sadrzadeh, S.M. (2009). Haptoglobin phenotype and apolipoprotein E polymorphism: relationship to posttraumatic seizures and neuropsychological functioning after traumatic brain injury. Epilepsy Behav. 16, 501-506.
4. Annegers, J.F., Hauser, W.A., Coan, S.P., and Rocca, W.A. (1998). A population-based study of seizures after traumatic brain injuries. N. Engl. J. Med. 338, 20-24. (Pubitemid 28040171)
5. Asikainen, I., Kaste, M., and Sarna, S. (1999). Early and late posttraumatic seizures in traumatic brain injury rehabilitation patients: brain injury factors causing late seizures and influence of seizures on long-term outcome. Epilepsia 40, 584-589. (Pubitemid 29207322)
6. Atkins, C.M., Truettner, J.S., Lotocki, G., Sanchez-Molano, J., Kang, Y., Alonso, O.F., Sick, T.J., Dietrich W.D., and Bramlett, H.M., (2010). Post-traumatic seizure susceptibility is attenuated by hypothermia therapy. Eur. J. Neurosci. 32, 1912-1920.
7. Bao, Y.H., Bramlett, H.M., Atkins, C.M., Truettner, J.S., Lotocki, G., Alonso, O.F., and Dietrich, W.D. (2011). Post-traumatic seizures exacerbate histopathological damage after fluid-percussion brain injury. J. Neurotrauma 28, 35-42.
8. Blanco, M.M., dos Santos, J.G. Jr., Perez-Mendes, P., Kohek, S.R., Cavarsan, C.F., Hummel, M., Albuquerque, C., and Mello, L.E. (2009). Assessment of seizure susceptibility in pilocarpine epileptic and nonepileptic Wistar rats and of seizure re-induction with pentylenetetrazole and electroshock models. Epilepsia 50, 824-831.
9. Bortel, A., Lévesque, M., Biagini, G., Gotman, J., and Avoli, M. (2010). Convulsive status epilepticus duration as determinant for epileptogenesis and interictal discharge generation in the rat limbic system. Neurobiol. Dis. 40, 478-489.
10. Calcagni, M.L., Giordano, A., Bruno, I., Parbonetti, G., Di Giuda, D., De Rossi, G., Troncone, L., and Colicchio, G. (2002). Ictal brain SPET during seizures pharmacologically provoked with pentylenetetrazol: a new diagnostic procedure in drug-resistant epileptic patients. Eur. J. Nucl. Med. Mol. Imaging 29, 1298-1306. (Pubitemid 44392209)
11. Carbonell, W.S., Maris, D.O., McCall, T., and Grady, M.S. (1998). Adaptation of the fluid percussion injury model to the mouse. J. Neurotrauma 15, 217-229. (Pubitemid 28113581)
12. Cavazos, J.E., Golarai, G., and Sutula, T.P. (1991). Mossy fiber synaptic reorganization induced by kindling: time course of development, progression, and permanence. J. Neurosci. 11, 2795-2803.
13. Centers for Disease Control and Prevention. (2001). Traumatic brain injury in the United States: A report to Congress. Department of Health and Human Services, Centers for Disease Control and Prevention, Atlanta, Georgia.
14. Coulter, D.A., Rafiq, A., Shumate, M., Gong, Q.Z., DeLorenzo, R.J., and Lyeth, B.G. (1996). Brain injury-induced enhanced limbic epileptogenesis: anatomical and physiological parallels to an animal model of temporal lobe epilepsy. Epilepsy Res. 26, 81-91. (Pubitemid 26420732)
15. Chrzaszcz, M., Venkatesan, C., Dragisic, T., Watterson, D.M., and Wainwright, M.S. (2010). Minozac treatment prevents increased seizure susceptibility in a mouse "two-hit" model of closed skull traumatic brain injury and electroconvulsive shock-induced seizures. J. Neurotrauma 27, 1283-1295.
16. D'Ambrosio, R., Fairbanks, J.P., Fender, J.S., Born, D.E., Doyle, D.L., and Miller, J.W. (2004). Post-traumatic epilepsy following fluid percussion injury in the rat. Brain 127, 304-314. (Pubitemid 38160315)
17. D'Ambrosio, R., Fender, J.S., Fairbanks, J.P., Simon, E.A., Born, D.E., Doyle, D.L., and Miller, J.W. (2005). Progression from frontal-parietal to mesial-temporal epilepsy after fluid percussion injury in the rat. Brain 128, 174-188. (Pubitemid 40070531)
18. Dardiotis, E., Fountas, K.N., Dardioti, M., Xiromerisiou, G., Kapsalaki, E., Tasiou, A., and Hadjigeorgiou, G.M. (2010). Genetic association studies in patients with traumatic brain injury. Neurosurgical Focus 28, 9.
19. Da Silva, A.M., Vaz, A.R., Ribeiro, I., Melo, A.R., Nune, B., and Correia, M. (1990). Controversies in posttraumatic epilepsy. Acta Neurochir. Suppl. 50, 48-51.
20. Diaz-Arrastia, R., Agostini, M.A., Frol, A.B., Mickey, B., Fleck-enstein, J., Bigio, E., and Van Ness, P.C. (2000). Neurophysio-logic and neuroradiologic features of intractable epilepsy after traumatic brain injury in adults. Arch. Neurol. 57, 1611-1616.
21. Diaz-Arrastia, R., Gong, Y., Fair, S., Scott, K.D., Garcia, M.C., Carlile, M.C., Agostini, M.A., and Van Ness, P.C. (2003). Increased risk of late posttraumatic seizures associated with inheritance of APOE epsilon4 allele. Arch Neurol. 60, 818-822. (Pubitemid 36705967)
22. Dudek, F.E. (2009). Commentary: a skeptical view of experimental gene therapy to block epileptogenesis. Neurother-apeutic: NeuroTherapeutics 6, 319-322.
23. Echegoyen, J., Armstrong, C., Morgan, R.J., and Soltesz, I. (2009). Single application of a CB1 receptor antagonist rapidly following head injury prevents long-term hyperexcitability in a rat model. Epilepsy Res. 85, 123-127.
24. Erickson, J.C., Clegg, K.E., and Palmiter, R.D. (1996). Sensitivity to leptin and susceptibility to seizures of mice lacking neuro-peptide Y. Nature 381, 415-421.
25. Fisher, R.S., van Emde, B.W., Blume, W., Elger, C., Genton, P., Lee, P., and Engel, J. Jr. (2005). Epileptic seizures and epilepsy: definitions proposed by the International League Against Epilepsy (ILAE) and the International Bureau for Epilepsy (IBE). Epilepsia 46, 470-472. (Pubitemid 40470667)
26. Fox, G.B., LeVasseur, R.A., and Faden, A.I. (1999). Behavioral responses of C57BL/6, FVB/N, and 129/SvEMS mouse strains to traumatic brain injury: implications for gene targeting approaches to neurotrauma. J. Neurotrauma 16, 377-389. (Pubitemid 29264790)
27. Golarai, G., Greenwood, A.C., Feeney, D.M., and Connor, J.A. (2001). Physiological and structural evidence for hippocampal involvement in persistent seizure susceptibility after traumatic brain injury. J. Neurosci. 21, 8523-8537. (Pubitemid 33051451)
28. Goldstein, M. (1990). Traumatic brain injury: a silent epidemic. Ann. Neurol. 27, 327. (Pubitemid 20122385)
29. Guo, D., Zeng, L., Brody, D., and Wong, M. (2010). mTOR inhibition has potential antiepileptogenic effects in a controlled cortical impact model of traumatic brain injury. American Epilepsy Society Annual Meeting. Abstract Number 1.014.
30. Gurkoff, G.G., Giza, C.C., Shin, D., Auvin, S., Sankar, R., and Hovda, D.A. (2009). Acute neuroprotection to pilocarpineinduced seizures is not sustained after traumatic brain injury in the developing rat. Neuroscience 164, 862-876.
31. Haltiner, A.M., Temkin, N.R., and Dikmen, S.S. (1997). Risk of seizure recurrence after the first late posttraumatic seizure. Arch. Phys. Med. Rehabil. 7, 835-840. (Pubitemid 27375089)
32. Hamm, R.J., Pike, B.R., Temple, M.D., O'Dell, D.M., and Lyeth, B.G. (1995). The effect of post injury kindled seizures on cognitive performance of traumatically brain-injured rats. Exp. Neurol. 136, 143-148.
33. Herman, S.T. (2002). Epilepsy after brain insult: targeting epi-leptogenesis. Neurology 59 (Suppl. 5), 21-26.
34. Hudak, A.M., Trivedi, K., Harper, C.R., Booker, K., Caesar, R.R., Agostini, M., Van Ness, P.C, and Diaz-Arrastia, R. (2004). Evaluation of seizure-like episodes in survivors of moderate and severe traumatic brain injury. J. Head Trauma Rehabil. 19, 290-295. (Pubitemid 38938194)
35. Hunt R.F., Scheff, S.W., and Smith, B.N. (2009). Posttraumatic epilepsy after controlled cortical impact injury in mice. Exp. Neurol. 215, 243-252.
36. Hunt, R.F., Scheff, S.W., and Smith, B.N. (2010). Regionally localized recurrent excitation in the dentate gyrus of a cortical contusion model of posttraumatic epilepsy. J. Neurophysiol. 103, 1490-1500.
37. Hanell, A., Clausen, F., Björk, M., Jansson, K., Philipson, O., Nilsson, L.N., Hillered, L., Weinreb, P.H., Lee, D., McIntosh, T.K, Gimbel, D.A., Strittmatter, S.M., and Marklund, N. (2010). Genetic deletion and pharmacological inhibition of Nogo-66 receptor impairs cognitive outcome after traumatic brain injury in mice. J. Neurotrauma 27, 1297-1309.
38. Kazemi, M., Silva, M.D., Li, F., Fisher, M., and Sotak, C.H. (2004). Investigation of techniques to quantify in vivo lesion volume based on comparison of water apparent diffusion coefficient (ADC) maps with histology in focal cerebral ischemia of rats. Magn. Reson. Imaging. 22, 653-659. (Pubitemid 38692625)
39. Kraus, J. Tagliaferri, F., Compagnone, C., Korsic, M., and Serva-dei, F., (2006). Brain injury epidemiology in Europe: a systematic review from recent data. Acta Neurochir. 148, 255-268.
40. Kharatishvili, I., and Pitkänen, A. (2010). Association of the severity of cortical damage with the occurrence of spontaneous seizures and hyperexcitability in an animal model of post-traumatic epilepsy. Epilepsy Res. 90, 47-59.
41. Kharatishvili, I., Immonen, R., Gröhn, O., and Pitkänen, A. (2007).Quantitative diffusion MRI of hippocampus as a surrogate marker for post-traumatic epileptogenesis. Brain 130, 3155-3168. (Pubitemid 350209080)
42. Kharatishvili, I., Nissinen, J.P., McIntosh, T.K, and Pitkänen, A. (2006). A model of posttraumatic epilepsy induced by lateral fluid-percussion brain injury in rats. Neuroscience 140, 685-697.
43. Lowenstein, D.H. (2009). Epilepsy after head injury: an overview. Epilepsia 50 (Suppl. 2), 4-9.
44. Lowenstein, D.H., Thomas, M.J., Smith, D.H., and McIntosh, T.K. (1992). Selective vulnerability of dentate hilar neurons following traumatic brain injury: a potential mechanistic link between head trauma and disorders of the hippocampus. J. Neurosci. 12, 4846-4853.
45. Löscher, W., and Nolting, B. (1991). The role of technical, biological and pharmacological factors in the laboratory evaluation of anticonvulsant drugs. IV. Protective indices. Epilepsy Res. 9, 1-10.
46. Marklund, N., and Hillered, L. (2010). Animal modeling of traumatic brain injury in pre-clinical drug development-Where do we go from here? Br. J. Pharmacology. Dec 22. doi: 10.1111/j.1476-5381.2010.01163.x. Epub ahead of print
47. Marklund, N., Clausen, F., Lewen, A., Hovda, D.A., Olsson, Y., and Hillered, L., (2001). A-phenyl-tert-N-butyl nitrone (PBN) improves functional and morphological outcome after cortical contusion injury in the rat. Acta Neurochir. 143, 73-81.
48. Mathern, G.W., Pretorius, J.K., and Babb, T.L. (1995). Influence of the type of initial precipitating injury and at what age it occurs on course and outcome in patients with temporal lobe seizures. J. Neurosurg. 82, 220-227.
49. Morales, D.M., Marklund, N., Lebold, D., Thompson, H.J., Pit-kanen, A., Maxwell, W.L., Longhi, L., Laurer, H., Maegele, M., Neugebauer, E., Graham, D.I., Stocchetti, N., and McIntosh, T.K. (2005). Experimental models of traumatic brain injury: do we really need to build a better mousetrap? Neuroscience 136, 971-989. (Pubitemid 41790514)
50. Navarro Mora, G., Bramanti, P., Osculati, F., Chakir, A., Nico-lato, E., Marzola, P., Sbarbati, A., and Fabene, P.F. (2009). Does pilocarpine-induced epilepsy in adult rats require status epi-lepticus? PloS One 4, 5759.
51. Ng, T., Graham, D.I., Adams, J.H., and Ford, I. (1989). Changes in the hippocampus and the cerebellum resulting from hyp-oxic insults: frequency and distribution. Acta Neuropathol. 78, 438-443. (Pubitemid 19200594)
52. Nissinen, J., Halonen, T., Koivisto, E., and Pitkä nen, A. (2000). A new model of chronic temporal lobe epilepsy induced by electrical stimulation of the amygdala in rat. Epilepsy Res. 38, 177-205.
53. Nissinen, J., Lukasiuk, K., and Pitkänen, A. (2001). Is mossy fiber sprouting present at the time of the first spontaneous seizures in rat experimental temporal lobe epilepsy? Hippocampus 11, 299-310. (Pubitemid 32655288)
54. Pitkänen, A., and McIntosh, T.K. (2006). Animal models of post-traumatic epilepsy. J. Neurotrauma 23, 241-261.
55. Pitkänen, A., Bolkvadze, T., and Immonen, R. (2011). Anti-epileptogenesis in rodent post-traumatic epilepsy models. Neurosci. Lett. Mar 21. Epub ahead of print.
56. Racine, R.J. (1972). Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32, 281-294.
57. Rattka, M., Brandt, C., Bankstahl, M., Bröer, S., and Löscher, W. (2011). Enhanced susceptibility to the GABA antagonist pen-tylenetetrazole during the latent period following a pilocar-pine-induced status epilepticus in rats. Neuropharmacology 60, 505-512.
58. Reeves, T.M., Lyeth, B.G., Phillips, L.L., Hamm, R.J., and Povlishock, J.T. (1997). The effects of traumatic brain injury on inhibition in the hippocampus and dentate gyrus. Brain Res. 757, 119-132. (Pubitemid 27244628)
59. Salazar, A.M., Jabbari, B., Vance, S.C., Grafman, J., Amin, D., and Dillon, J.D. (1985). Epilepsy after penetrating head injury. I. Clinical correlates: a report of the Vietnam Head Injury Study. Neurology 35, 1406-1414. (Pubitemid 15242412)
60. Santhakumar, V., Bender, R., Frotscher, M., Ross, S.T., Hollrigel, G.S., Toth, Z., and Soltesz, I. (2000). Granule cell hyperexcitability in the early post-traumatic rat dentate gyrus: the "irritable mossy cell" hypothesis. J. Physiol. 524, 117-134. (Pubitemid 30195309)
61. Santhakumar, V., Ratzliff, A.D., Jeng, J., Toth, Z., and Soltesz, I. (2001). Long-term hyperexcitability in the hippocampus after experimental head trauma. Ann. Neurol. 50, 708-717. (Pubitemid 33116130)
62. Schauwecker, P.E., and Steward, O. (1997). Genetic determinants of susceptibility to excitotoxic cell death: implications for gene targeting approaches. Proc. Natl. Acad. Sci. USA 94, 4103-4108. (Pubitemid 27180506)
63. Schauwecker, P.E. (2002). Complications associated with genetic background effects in models of experimental epilepsy. Prog. Brain Res. 135, 139-148. (Pubitemid 35461013)
64. Scheid, R., and von Cramon, D.Y. (2010). Clinical findings in the chronic phase of traumatic brain injury: data from 12 years' experience in the Cognitive Neurology Outpatient Clinic at the University of Leipzig. Dtsch. Arztebl. Int. 107, 199-205.
65. Schwartzkroin, P.A., Wenzel, H.J., Lyeth, B.G, Poon, C.C., De-lance, A., Van, K.C., Campos, L., and Nguyen, D.V. (2010). Does ketogenic diet alter seizure sensitivity and cell loss following fluid percussion injury? Epilepsy Res. 92, 74-84.
66. Sloviter, R.S. (1982). A simplified Timm stain procedure compatible with formaldehyde fixation and routine paraffin embedding of rat brain. Brain Res. Bull. 8, 771-774. (Pubitemid 13240618)
67. Smith, D.H., Soares, H.D., Pierce, J.S., Perlman, K.G., Saatman, K.E., Meaney, D.F., Dixon, C.E., and McIntosh, T.K. (1995). A model of parasagittal controlled cortical impact in the mouse: cognitive and histopathologic effects. J. Neurotrauma 12, 169-178.
68. Specht, C.G, and Schoepfer, R. (2004). Deletion of multimerin-1 in alpha-synuclein-deficient mice. Genomics 83, 1176-1178.
69. Specht, C.G., and Schoepfer, R. (2001). Deletion of the alpha-synuclein locus in a subpopulation of C57BL/6J inbred mice. BMC Neurosci. 2, 11.
70. Statler, K.D., Scheerlinck, P., Pouliot, W., Hamilton, M., White, H.S., and Dudek, F.E. (2009). A potential model of pediatric posttraumatic epilepsy. Epilepsy Res. 86, 221-223.
71. Statler, K.D., Swank, S., Abildskov, T., Bigler, E.D., and White, H.S. (2008). Traumatic brain injury during development reduces minimal clonic seizure thresholds at maturity. Epilepsy Res. 80, 163-170.
72. Swartz, B.E., Houser, C.R., Tomiyasu, U., Walsh, G.O., DeSalles, A., Rich, J.R., and Delgado-Escueta, A. (2006). Hippocampal cell loss in posttraumatic human epilepsy. Epilepsia 47, 1373-1382. (Pubitemid 44200419)
73. Toth, Z., Hollrigel, G.S., Gorcs, T., and Soltesz, I. (1997). Instantaneous perturbation of dentate interneuronal networks by a pressure wave-transient delivered to the neocortex. J. Neuroscience 17, 8106-8117. (Pubitemid 27461035)
74. Tran, L.D., Lifshitz, J., Witgen, B.M., Schwarzbach, E., Cohen, A.S., and Grady, M.S. (2006). Response of the contralateral hippocampus to lateral fluid percussion brain injury. J. Neu-rotrauma 23, 1330-1342. (Pubitemid 46489619)
75. Vaishnavi, S., Rao, V., and Fann, J.R. (2009). Neuropsychiatric problems after traumatic brain injury: unraveling the silent epidemic. Psychosomatics 50, 198-205.
76. Vezzani, A., Speciale, C., Della Vedova, F., Tamburin, M., and Benatti, L. (1995). Alternative splicing at the C-terminal but not at the N-terminal domain of the NMDA receptor NR1 is altered in the kindled hippocampus. Eur. J. Neurosci. 7, 2513-2517.
77. Wieser, H.G., Bancaud, J., Talairach, J., Bonis, A., and Szikla, G. (1979). Comparative value of spontaneous and chemically and electrically induced seizures in establishing the lateralization of temporal lobe seizures. Epilepsia 20, 47-59. (Pubitemid 9126969)
78. Witgen, B.M., Lifshitz, J., Smith, M.L., Schwarzbach, E., Liang, S.L., Grady, M.S., and Cohen, A.S. (2005). Regional hippo-campal alteration associated with cognitive deficit following experimental brain injury: a systems, network and cellular evaluation. Neuroscience 133, 1-15. (Pubitemid 40694154)
79. Wotjak, C.T. (2003). C57BLack/BOX? The importance of exact mouse strain nomenclature. Trends Genet. 19, 183-184. (Pubitemid 36398418)
80. Yang, L., Afroz, S., Michelson, H.B., Goodman, J.H., Valsamis, H.A., and Ling, D.S. (2010). Spontaneous epileptiform activity in rat neocortex after controlled cortical impact injury. J. Neurotrauma 27, 1541-1548.
81. Yonekawa, W.D., Kupferberg, H.J., and Woodbury, D.M. (1980). Relationship between pentylenetetrazol-induced seizures and brain pentylenetetrazol levels in mice. J. Pharmacol. Exp. Ther. 214, 589-593. (Pubitemid 10061405)