Prospects of modeling poststroke epileptogenesis

Journal of Neuroscience Research

Volumn 95, Issue 4, 2017, Pages 1000-1016

  Reddy, Doodipala Samba ^a   Bhimani, Aamir ^a   Kuruba, Ramkumar ^a   Park, Min Jung ^a   Sohrabji, Farida ^a  

^a TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

endothelin; epilepsy; epileptogenesis; MCA; poststroke; seizures; stroke

Indexed keywords

ENDOTHELIN 1; LAURIC ACID; SODIUM; ANTICONVULSIVE AGENT;

BRAIN ISCHEMIA; CEREBROVASCULAR ACCIDENT; CORPUS STRIATUM; EPILEPSY; EPILEPTOGENESIS; EXPERIMENTAL STROKE; MIDDLE CEREBRAL ARTERY OCCLUSION; NONHUMAN; PHENOTYPE; POSTSTROKE EPILEPSY; PREVALENCE; PRIORITY JOURNAL; RECURRENT DISEASE; REVIEW; SEX DIFFERENCE; THROMBOSIS; VASOCONSTRICTION; ANIMAL; COMPLICATION; DISEASE MODEL; HUMAN;

ANIMALS; ANTICONVULSANTS; DISEASE MODELS, ANIMAL; EPILEPSY; HUMANS; STROKE;

EID: 84994330137     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23836     Document Type: Review

References (198)

1. Abbott NJ. 2000. Inflammatory mediators and modulation of blood–brain barrier permeability. Cell Mol Neurobiol 20:131–147.
2. Alkayed NJ, Harukuni I, Kimes AS, London ED, Traystman RJ, Hurn PD. 1998. Gender-linked brain injury in experimental stroke. Stroke 29:159–165.
3. Anyanwu EC. 2007. Neurochemical changes in the aging process: implications in medication in the elderly. Sci World J 7:1603–1610.
4. Arboix A, Garcia-Eroles L, Massons JB, Oliveres M, Comes E. 1997. Predictive factors of early seizures after acute cerebrovascular disease. Stroke 28:1590–1594.
5. Arntz R, Rutten-Jacobs L, Maaijwee N, Schoonderwaldt H, Dorresteijn L, van Dijk E, de Leeuw FE. 2013. Post-stroke epilepsy in young adults: a long-term follow-up study. PLoS One 8:e55498.
6. Aronowski J, Strong R, Grotta J. 1997. Reperfusion injury: demonstration of brain damage produced by reperfusion following transient focal ischemia in rats. J Cereb Blood Flow Metab 17:1048–1056.
7. Atochin DN, Murciano JC, Gürsoy-Özdemir Y. 2004. Mouse model of microembolic stroke and reperfusion. Stroke 35:2177–2182.
8. Bake S, Selvaman A, Cherry J, Sohrabji F. 2014. Blood–brain barrier and neuroinflammation are critical targets of IGF-1-mediated neuroprotection in stroke for middle-aged female rats. PLoS One 9:e91427.
9. Balkaya M, Kröber JM, Rex A, Endres M. 2013. Assessing post-stroke behavior in mouse models of focal ischemia. J Cereb Blood Flow Metab 33:330–338.
10. Bederson JB, Pitts LH, Germano SM, Nishimura MC, Davis RL, Bartkowski HM. 1986. Evaluation of 2,3,5-triphenyltetrazolium chloride as a stain for detection and quantification of experimental cerebral infarction in rats. Stroke 17:1304–1308.
11. Beghi E, D'Alessandro R, Beretta S, Consoli D, Crespi V, Delaj L, Gandolfo C, Greco G, La Neve A, Manfredi M, Mattana F, Musolino R, Provinciali L, Santangelo M, Specchio LM, Zaccara G, Epistroke Group. 2011. Incidence and predictors of acute symptomatic seizures after stroke. Neurology 77:1785–1793.
12. Belayev L, Busto R, Zhao W, Fernandez G, Ginsberg MD. 1999. MCA occlusion in the mouse by intraluminal suture coated with poly-l-lysine: neurological and histological validation. Brain Res 833:181–190.
13. Benbir G, Ince B, Bozluolcay M. 2006. The epidemology of post stroke epilepsy according to stroke subtypes. Acta Neurol Scand 114:8–12.
14. Berzin TM, Zipser BD, Rafii MS, Kuo-Leblanc V, Yancopoulos GD, Glass DJ, Fallon JR, Stopa EG. 2000. Agrin and microvascular damage in Alzheimer's disease. Neurobiol Aging 21:349–355.
15. Bladin CF, Alexandrov AV, Bellavance A, Bornstein N, Chambers B, Cote R, Lebrun L, Pirisi A, Norris JW. 2000. Seizures after stroke: a prospective multicenter study. Arch Neurol 57:1617–1622.
16. Bladin CF, Bornstein N. 2009. Post-stroke seizures. Hdbk Clin Neurol 93:613–621.
17. Bliss T, Guzman R, Daadi M, Steinberg GK. 2007. Cell transplantation therapy for stroke. Stroke 38:817–826.
18. Boutin H, LeFeuvre RA, Horai R, Asano M, Iwakura Y, Rothwell NJ. 2001. Role of IL-1alpha and IL-1beta in ischemic brain damage. J Neurosci 21:5528–5534.
19. Broderick JP, Adam HP Jr, Barsan W, Feinberg W, Feldmann E, Grotta J, Kase C, Krieger D, Mayberg M, Tilley B, Zabramski JM, Zuccarello M. 1999. Guidelines for the management of spontaneous intracerebral hemorrhage: a statement for the health care professionals from the special writing group of the Stroke Council, American Heart Association. Stroke 30:905–915.
20. Brodie MJ, Overstall PW, Giorgi L. 1999. Multicentre, double-blind, randomised comparison between lamotrigine and carbamazepine in elderly patients with newly diagnosed epilepsy. The UK Lamotrigine Elderly Study Group. Epilepsy Res 37:81–87.
21. Browne TR, Holmes GL. 2001. Epilepsy. N Engl J Med 344:1145–1151.
22. Burn J, Dennis M, Bamford J, Sandercock P, Wade D, Warlow C. 1997. Epileptic seizures after a first stroke: the Oxfordshire Community Stroke Project. Br Med J 315:1582–1587.
23. Busch E, Kruger K, Allegrini PR, Kerskens CM, Gyngell ML, Hoehn-Berlage M, Hossmann KA. 1998. Reperfusion after thrombolytic therapy of embolic stroke in the rat: magnetic resonance and biochemical imaging. J Cereb Blood Flow Metab 18:407–418.
24. Calloni RIC. 2006. Modelo experimental de isquemia cerebral em ratos por obliteração temporária da artéria cerebral média. Porto Alegre, Brazil: Universidade Federal do Rio Grande do Sul.
25. Camilo O, Goldstein LB. 2004. Seizures and epilepsy after ischemic stroke. Stroke 35:1769–1775.
26. Caplan AI. 2007. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol 213:341–347.
27. Carmichael ST. 2005. Rodent models of focal stroke: size, mechanism, and purpose. NeuroRx 2:396–409.
28. Chiang T, Messing RO, Chou WH. 2011. Mouse model of MCA occlusion. J Vis Exp 48:2761.
29. Couraud PO. 1998. Infiltration of inflammatory cells through brain endothelium. Pathol Biol 46:176–180.
30. Coyle P. 1982. Middle cerebral artery occlusion in the young rat. Stroke 13:855–859.
31. Culmsee C, Zhu C, Landshamer S. 2005. Apoptosis-inducing factor triggered by poly(ADP-ribose) polymerase and Bid mediates neuronal cell death after oxygen-glucose deprivation and focal cerebral ischemia. J Neurossci 25:10262–10272.
32. Davidsson P, Paulson L, Hesse C, Blennow K, Nilsson CL. 2001. Proteome studies of human cerebrospinal fluid and brain tissue using a preparative two-dimensional electrophoresis approach prior to mass spectrometry. Proteomics 1:444–452.
33. De Carolis P, E'Allessandro R, Ferrara R, Andreoli A, Sacquegna T, Lugaresi E. 1984. Late seizures in patient with carotid and middle cerebral artery occlusive disease following ischemic events. J Neurol Neurosurg Psychiatry 47:1345–1347.
34. Del Zoppo GJ. 1998. tPA: a neuron buster, too? Nat Med 4:148–150.
35. Delgado-Escueta AV, Porter R. 1999. Symptomatic lesional epilepsies: introduction. Adv Neurol 79:433–435.
36. DeVries AC, Nelson RJ, Traystman RJ, Hurn PD. 2001. Cognitive and behavioral assessment in experimental stroke research: will it prove useful? Neurosci Biobehav Rev 25:325–342.
37. Dhanuka AK, Misra UK, Kalita J. 2001. Seizures after stroke: a prospective clinical study. Neurol India 49:33–36.
38. Dietrich WD, Watson BD, Busto R, Ginsberg MD, Bethea JR. 1987. Photochemically induced cerebral infarction. I. Early microvascular alterations. Acta Neuropathol 72:315–325.
39. Dietrich WD, Prado R, Watson BD, Nakayama H. 1988. MCA thrombosis: acute blood–brain barrier consequences. J Neuropathol Exp Neurol 47:443–451.
40. 111In-labeled platelet study. Stroke 24:1534–1540.
41. Dietrich WD, Prado R, Halley M, Watson BD. 1993b. Microvascular and neuronal consequences of common carotid artery thrombosis and platelet embolization in rats. J Neuropathol Exp Neurol 52:351–360.
42. Durukan A, Tatlisumak T. 2007. Acute ischemic stroke: overview of major experimental rodent models, pathophysiology, and therapy of focal cerebral ischemia. Pharmacol Biochem Behav 87:179–197.
43. Durukan A, Strbian D, Tatlisumak T. 2008. Rodent models of ischemic stroke: a useful tool for stroke drug development. Curr Pharm Des 14:359–370.
44. Engel J Jr, International League Against Epilepsy (ILAE). 2001. A proposed diagnostic scheme for people with epileptic seizures and with epilepsy: report of the ILAE Task Force on Classification and Terminology. Epilepsia 42:796–803.
45. Engel T, Murphy BM, Schindler CK, Henshall DC. 2007. Elevated p53 and lower MDM2 expression in hippocampus from patients with intractable temporal lobe epilepsy. Epilepsy Res 77:151–156.
46. Faraday N, Rosenfeld BA. 1998. In vitro hypothermia enhances platelet GPIIb–IIIa activation and P-selectin expression. Anesthesiology 88:1579–1585.
47. Fisher CM. 1982. Lacunar strokes and infarcts: a review. Neurology 32:871–876.
48. Foerch C, Otto B, Singer OC, Neumann-Haefelin T, Yan B, Berkefeld J. 2004. Serum S100B predicts a malignant course of infarction in patients with acute MCA occlusion. Stroke 35:2160–2164.
49. Forsgren L, Bucht G, Eriksson S, Bergmark L. 1996. Incidence and clinical characterization of unprovoked seizures in adults: a prospective populations-based study. Epilepsia 37:224–229.
50. Fuxe K, Kurosawa N, Cintra A. 1992. Involvement of local ischemia in ET-1 induced lesions of the neostriatum of the anaesthetized rat. Exp Brain Res 88:131–139.
51. Garcia JH, Yoshida Y, Chen H, Li Y, Zhang ZG, Lian J, Chen S, Chopp M. 1993. Progression from ischemic injury to infarct following middle cerebral artery occlusion in the rat. Am J Pathol 142:623–635.
52. Gartshore G, Patterson J, Macrae IM. 1997. Influence of ischemia and reperfusion on the course of brain tissue swelling and blood–brain barrier permeability in a rodent model of transient focal cerebral ischemia. Exp Neurol 147:353–360.
53. George PM, Steinberg GK. 2015. Novel stroke therapeutics: unraveling stroke pathophysiology and its impact on clinical treatments. Neuron 87:297–309.
54. Gerriets T, Li F, Silva MD, Meng X, Brevard M, Sotak CH. 2003. The macrosphere model: evaluation of a new stroke model for permanent MCA occlusion in rats. J Neurosci Methods 122:201–211.
55. Gibson CL. 2013. Cerebral ischemic stroke: is gender important? J Cereb Blood Flow Metab 33:1355–1361.
56. Gibson LM, Hanby MF, Al-Bachari SM, Parkes LM, Allan SM, Emsley HC. 2014. Late-onset epilepsy and occult cerebrovascular disease. J Cereb Blood Flow Metab 34:564–570.
57. Gigante B, Rubattu S, Stanzione R, Lombardi A, Baldi A, Baldi F, Volpe,M., 2003. Contribution of genetic factors to renal lesions in the stroke-prone spontaneously hypertensive rat. Hypertension 42:702–706.
58. Giorgi FS, Galanopoulou AS, Moshe SL. 2014. Sex dimorphism in seizure controlling networks. Neurobiol Dis 72:144–152.
59. Giroud M, Gras P, Fayolle H, Andre N, Soichot P, Dumas R. 1994. Early seizures after acute stroke: a study of 1,640 cases. Epilepsia 35:959–964.
60. Graham NS, Crichton S, Koutroumanidis M, Wolfe CD, Rudd AG. 2013. Incidence and associations of poststroke epilepsy: the prospective South London Stroke Register. Stroke 44:605–611.
61. Guerrini U, Sironi L, Tremoli E, Miller I, Cimino M, Pollo B, Calvio AM, Paoletti R, Asdente M. 2002. New insights into brain damage in stroke-prone rats. A nuclear magnetic imaging study. Stroke 33:825–830.
62. Gupta SR, Naheedy MH, Elias D, Rubino FA. 1988. Postinfarction seizures. A clinical study. Stroke 19:1477–1481.
63. Hallenbeck JM, Dutka A J. 1990. Background review and current concepts of reperfusion injury. Arch Neurol 47:1245–1254.
64. Hartings JA, Williams AJ, Tortella FC. 2003. Occurrence of nonconvulsive seizures, periodic epileptiform discharges, and intermittent delta activity in rat focal ischemia. Exp Neurol 179:139–149.
65. Harvey J, Rasmussen T. 1951. Occlusion of the middle cerebral artery; an experimental study. AMA Arch Neurol Psychiatry 66:20–29.
66. Hauser WA. 1990. Seizure disorders: the changes with age. Epilepsia 33:614.
67. Hauser WA. 1992. Seizure disorders: the changes with age. Epilepsia 33(Suppl 4):S6–S14.
68. Hauser WA, HesdorVer DC. 1990. Epilepsy: frequency, causes, and consequences. New York: Demos.
69. Hauser WA, Annegers JF, Kurland LT. 1991. Prevalence of epilepsy in Rochester, Minnesota:1940–1980. Epilepsia 32:429–445.
70. Hauser WA, Annegers JF, Kurland LT. 1993. Incidence of epilepsy and unprovoked seizures in Rochester, Minnesota: 1935–1984. Epilepsia 34:453–468.
71. Hayakawa T, Waltz AG. 1975. Immediate effects of cerebral ischemia: evolution and resolution of neurological deficits after experimental occlusion of one middle cerebral artery in conscious cats. Stroke 6:321–327.
72. Henshall DC, Butcher SP, Sharkey J. 1999. A rat model of endothelin-3-induced middle cerebral artery occlusion with controlled reperfusion. Brain Res 843:105–111.
73. Heye N, Paetzold C, Steinberg R, Cervos-Navarro J. 1992. The topography of microthrombi in ischemic brain infarct. Acta Neurol Scand 86:450–454.
74. Hoyte LC, Papadakis M, Barber PA, Buchan AM. 2006. Improved regional cerebral blood flow is important for the protection seen in a mouse model of late phase ischemic preconditioning. Brain Res 112:231–237.
75. Huang Y H, Chi NF, Kuan YC, Chan CJ, Hu HY, Chien LN. 2015. Efficacy of phenytoin, valproic acid, carbamazepine and new antiepileptic drugs on control of late-onset post-stroke epilepsy in Taiwan. Eur J Neurol 22:1459–1468.
76. Huber JD, Egleton RD, Davis TP. 2001. Molecular physiology and patho-physiology of tight junctions in the blood–brain barrier. Trends Neurosci 24:719–725.
77. Hughes PM, Anthony DC, Ruddin M. 2003. Focal lesions in the rat central nervous system induced by ET-1. J Neuropathol Exp Neurol 62:1276–1286.
78. Jamrozik K, Broadhurst RJ, Lai N, Hankey GJ, Burvill PW, Anderson CS. 1999. Trends in the incidence, severity, and short-term outcome of stroke in Perth, Western Australia. Stroke 30:2105–2111.
79. Johnston TD, Chen Y, Reed RL. 1994. Functional equivalence of hypothermia to specific clotting factor deficiencies. J Trauma 37:413–417.
80. Joseph R, Tsering C, Grunfeld S, Welch KM. 1991. Platelet secretory products may contribute to neuronal injury. Stroke 22:1448–1451.
81. Jungehulsing GJ, Heuschmann PU, Holtkamp M, Schwab S, Kolominsky-Rabas PL. 2013. Incidence and predictors of post-stroke epilepsy. Acta Neurol Scand 127:427–430.
82. Jutila L, Ylinen A, Partanen K, Mervaala E, Partanen J, Vapalahti M, Vainio P, Pitkanen A. 2002. Neurobiology of epileptogenesis in the temporal lobe. Adv Techn Stand Neurosurg 27:5–22.
83. Kalpatrick CJ, Davis SM, Tress BM. 1990. Epileptic seizures in acute stroke. Arch Neurol 47:157–160.
84. Kammersgaard LP, Olsen TS. 2005. Poststroke epilepsy in the Copenhagen Stroke Study: incidence and predictors. J Stroke Cerebrovasc Dis 14:210–214.
85. Kappelle LJ, Gijn JV. 1986. Lacunar infarcts. Clin Neurol Neurosurg 88:3–17.
86. Kappos L, Moeri D, Radue EW, Schoetzau A, Schweikert K, Barkhof F, Miller D, Guttmann CR, Weiner HL, Gasperini C, Filippi M. 1999. Predictive value of gadolinium-enhanced magnetic resonance imaging for relapse rate and changes in disability or impairment in multiple sclerosis: a meta-analysis. Gadolinium MRI Meta-Analysis Group. Lancet 353:964–969.
87. Karhunen H, Pitkänen A, Virtanen T, Gureviciene I, Pussinen R, Ylinen A, Sivenius J, Nissinen J, Jolkkonen J. 2003. Long-term functional consequences of transient occlusion of the middle cerebral artery in rats: a 1-year follow-up of the development of epileptogenesis and memory impairment in relation to sensorimotor deficits. Epilepsy Res 54:1–10.
88. Karhunen HJ, Nissinen J, Sivenius J, Jolkkonen J, Pitkanen A. 2006. A long-term video-EEG and behavioral follow-up after endothelin-1 induced middle cerebral artery occlusion in rats. Epilepsy Res 72:25–38.
89. Karhunen H, Bezvenyuk Z, Nissinen J, Sivenius J, Jolkkonen J, Pitkanen A. 2007. Epileptogenesis after cortical photothrombotic brain lesion in rats. Neuroscience 148:314–324.
90. Kelly KM. 2002. Post-stroke seizures and epilepsy: clinical studies and animal models. Epilepsy Curr 2:173–177.
91. Kelly KM. 2006. Stroke. In: Pitkänen A, Schwartzkroin PA, Moshe SL, editors. Models of seizures and epilepsy. London: Elsevier Academic Press. p 501–526.
92. Kelly KM. 2007. Animal modeling of post-stroke seizures and epilepsy: 5-year update. Epilepsy Curr 7:159–162.
93. Kelly KM, Kharlamov A, Hentosz TM, Kharlamova EA, Williamson JM, Bertram EH, Kapur J, Armstrong DM. 2001. Photothrombotic brain infarction results in seizure activity in aging Fischer 344 and Sprague Dawley rats. Epilepsy Res 47:189–203.
94. Kelly KM, Jukkola PI, Kharlamov EA, Downey KL, McBride JW, Strong R, Aronowski J. 2006. Long-term video-EEG recordings following transient unilateral middle cerebral and common carotid artery occlusion in Long-Evans rats. Exp Neurol 201:495–506.
95. Kessler KR, Schnitzler A, Classen J, Benecke R. 2002. Reduced inhibition within primary motor cortex in patients with post stroke focal motor seizures. Neurology 59:1028–1033.
96. Kharlamov EA, Jukkola PI, Schmitt KL, Kelly KM. 2003. Electrobehavioral characteristics of epileptic rats following photothrombotic brain infarction. Epilepsy Res 56:185–203.
97. Kharlamov EA, Kharlamov A, Kelly KM. 2007. Changes in neuropeptide Y protein expression following photothrombotic and epileptogenesis. Brain Res 1127:151–162.
98. Kilpatrick CJ, Davis SM, Tress BM, Rossiter SC, Hopper JL, Vandendriesen ML. 1990. Epileptic seizures in acute stroke. Arch Neurol 47:157–160.
99. Koppel BS, Harden CL. 2014. Gender issues in the neurobiology of epilepsy: a clinical perspective. Neurobiol Dis 72B:193–197.
100. Kotila M, Waltimo O. 1992. Epilepsy after stroke. Epilepsia 33:495–498.
101. Kudo M, Aoyama A, Ichimori S, Fukunaga N. 1982. An animal model of cerebral infarction. Homologous blood clot emboli in rats. Stroke 13:505–508.
102. Kumada T, Ishihara M, Ogawa H, Abiko Y. 1980. Experimental model of venous thrombosis in rats and effect of some agents. Thromb Res 18:189–203.
103. Lambraksis CC, Lancman ME. 1998. The phenomenology of seizures and epilepsy after stroke. J Epilepsy 11:233–240.
104. Lamy C, Domigo V, Semah F, Arquizan C, Trystram D, Coste J, Mas JL. 2003. Patent Foramen Ovale and Atrial Septal Aneurysm Study Group. Early and late seizures after cryptogenic ischemic stroke in young adults. Neurology 60:400–404.
105. Lancman ME, Golimstok A, Norscini J, Granillo R. 1993. Risk factors for developing seizures after a stroke. Epilepsia 34:141–143.
106. Li F, Omae T, Fisher M. 1999. Spontaneous hyperthermia and its mechanism in the intraluminal suture MCA occlusion model of rats. Stroke 30:2464–2470.
107. Li J, Zeng Z, Viollet B, Ronnett GV, McCullough LD. 2007. Neuroprotective effects of adenosine monophosphateactivated protein kinase inhibition and gene deletion in stroke. Stroke 38:2992–2999.
108. Liebeskind DS. 2005. Collaterals in acute stroke: beyond the clot. Neuroimag Clin 15:553–473.
109. Liu F, McCullough LD. 2011. MCA occlusion model in rodents: methods and potential pitfalls. J Biomed Biotechnol 2011:464–701.
110. Liu F, Schafer DP, McCullough LD. 2009a. TTC, Fluoro-Jade B and NeuN staining confirm evolving phases of infarction induced by MCA occlusion. J Neurosci Methods 179:1–8.
111. Liu F, Yuan R, Benashski SE, McCullough LD. 2009b. Changes in experimental stroke outcome across the life span. J Cereb Blood Flow Metab 29:792–802.
112. Liu J, Schmitt KL, Kharlamov EA, Stolarski CJ, Grayson DR, Kelly KM. 2002. Quantitative reverse transcription-polymerase chain reaction of GABA-A alpha1, beta1 and gamma2S subunits in epileptic rats following photothrombotic infarction of neocortex. Epilepsy Res 52:85–95.
113. Longa EZ, Weinstein PR, Carlson S, Cummins R. 1989. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20:84–91.
114. Löscher W, Brandt C. 2010. Prevention or modification of epileptogenesis after brain insults: experimental approaches and translational research. Pharmacol Rev 62:668–700.
115. Lossius MI, Ronning OM, Mowinckel P, Gjerstad L. 2002. Incidence and predictors for post-stroke epilepsy. A prospective controlled trial. The Akershus Stroke Study. Eur J Neurol 9:365–368.
116. Lossius MI, Ronning OM, Slapo GD, Mowinckel P, Gjerstadt L. 2005. Poststroke epilepsy: occurrence and predictors—a long-term prospective controlled study (Akershus Stroke Study). Epilepsia 46:1246–1251.
117. Lozano JD, Abulafia DP, Danton GH, Watson BD, Dietrich WD. 2007. Characterization of a thromboembolic photochemical model of repeated stroke in mice. J Neurosci Methods 162:244–254.
118. Lu XCM, Williams AJ, Tortella FC. 2001. Quantitative electroencephalography spectral analysis and topographic mapping in a rat model of middle cerebral artery occlusion. Neuropathol Appl Neurol 27:481–495.
119. Luhdorf K, Jensen LK, Plesner AM. 1986. Etiology of seizures in the elderly. Epilepsia 27:458–463.
120. Lyden P, Brott T, Tilley B, Welch KM, Mascha EJ, Levine S, Haley EC, Grotta J, Marler J. 1994. Improved reliability of the NIH Stroke Scale using video training. NINDS TPA Stroke Study Group. Stroke 25:2220–2226.
121. Manwani B, Liu F, Xu Y, Persky R, Li J, McCullough LD. 2011. Functional recovery in aging mice after experimental stroke. Brain Behav Immun 25:1689–1700.
122. Markgraf CG, Green EJ, Watson B, McCabe PM, Schneiderman N, Dietrich WD, Ginsberg MD. 1994. Recovery of sensorimotor function after distal middle cerebral artery photothrombotic occlusion in rats. Stroke 25:153–159.
123. Mathern GW, Babb TL, Pretorius JK, Melendez M, Lévesque MF. 1995. The pathophysiologic relationships between lesion pathology, intracranial ictal EEG onsets, and hippocampal neuron losses in temporal lobe epilepsy. Epilepsy Res 21:133–147.
124. Mathern GW, Adelson PD, Cahan LD, Leite JP. 2002. Hippocampal neuron damage in human epilepsy: Meyer's hypothesis revised. Prog Brain Res 135:237–251.
125. McColl BW, Carswell HV, McCulloch J, Horsburgh K. 2004. Extension of cerebral hypoperfusion and ischaemic pathology beyond MCA territory after intraluminal filament occlusion in C57Bl/6J mice. Brain Res 997:15–23.
126. McCullough LD, Zeng Z, Li H, Landree LE, McFadden J, Ronnett GV. 2005. Pharmacological inhibition of AMPactivated protein kinase provides neuroprotection in stroke. J Biol Chem 280:20493–20502.
127. McLarnon JG, Wang X, Bae JH, Kim SU. 1999. Endothelin-induced changes in intracellular calcium in human microglia. Neurosci Lett 263:9–12.
128. Mendez-Otero R, Giraldi-Guimarães A, Pimentel-Coelho PM, Freitas GR. 2009. Terapia celular no acidente vascular cerebral. Rev Brasil Hematol Hemoter 31:99–103.
129. Merkler AE, Dunn LE, et al. 2016. International Stroke Conference Oral Abstracts, Session Title: Clinical rehabilitation and recovery oral abstracts II: the long-term risk of seizures After Stroke. Abstract 109:
130. Meyer JS, Charney JZ, Rivera VM. 1971. Cerebral embolization: prospective clinical analysis of 42 cases. Stroke 2:541–554.
131. Miller ER, Kharlamov EA, Ynugadhati V, Kelly KM. 2013. Revisiting arterial occlusion as an animal model of poststroke epilepsy. American Epilepsy Society Annual Meeting, Abstract 1.041.
132. Mima T, Yanagisawa M, Shigeno T. 1989. Endothelin acts in feline and canine cerebral arteries from the adventitial side. Stroke 20:1553–1556.
133. Mohr JP, Caplan LR, Melski JW. 1978. The Harvard Cooperative Stroke Registry: a prospective registry. Neurology 28:754–762.
134. Mohr JP, Gautier JC, Hier D, Stein RW. 1986. Middle cerebral artery. In: Barnett HJM, Stein BM, Mohr JP, Yatsu FM, editors. Stroke, vol. 1. Pathophysiology, diagnosis and management. Churchill Livingstone, New York: p 377–450.
135. Murciano JC, Harshaw D, Neschis DG, Koniaris L, Bdeir K, Medinilla S, Fisher AB, Golden MA, Cines DB, Nakada MT, Muzykantov VR. 2002. Platelets inhibit the lysis of pulmonary microemboli. Am J Physiol 282:L529–L539.
136. Myint PK, Staufenberg EF, Sabanathan K. 2006. Post-stroke seizure and post-stroke epilepsy. Postgrad Med J 82:568–572.
137. Okamoto K, Yamori Y, Nagaoka A. 1974. Establishment of the stroke-prone spontaneously hypertensive rats (SHR). Circ Res 33/34:I143–I153.
138. Olsen TS. 2001. Post-stroke epilepsy. Curr Atheroscler Rep 3:340–344.
139. Oppenheim C, Samson Y, Manaï R, Lalam T, Vandamme X, Crozier S, Srour A, Cornu P, Dormont D, Rancurel G, Marsault C. 2000. Prediction of malignant middle cerebral artery infarction by diffusion-weighted imaging. Stroke 31:2175–2181.
140. Overgaard K, Sereghy T, Pedersen H, Boysen G. 1994. Effect of delayed thrombolysis with rt-PA in a rat embolic stroke medel. J Cereb Blood Flow Metab 14:472–477.
141. Park MJ, Kuruba R, Sohrabji F, and Reddy DS. 2016. Long-term epileptic seizure monitoring in MCAO model of stroke in female rats. American Epilepsy Society Annual Meeting, Abstract 194305.
142. Pitkänen A, Schwartzkroin PA, Moshé SL, editors. 2005. Models of seizures and epilepsy, chapter 40. New York: Academic Press.
143. Pitkänen A, Kharatishvili I, Karhunen H, Lukasiuk K, Immonen R, Nairismägi J, Gröhn O, Nissinen J. 2007. Epileptogenesis in experimental models. Epilepsia 48(Suppl 2):13–20.
144. Qureshi A, Tuhrim S, Broderick J. 2001. Spontaneous intracerebral haemorrhage. N Engl J Med 344:1450–1460.
145. Racine RJ, 1972. Modicication of seizure activity by electrical stimulation. II. Motor seizure. Electrocephalogr Clin Neurophysiol 32:281–294.
146. Rao MV, Hattiangady B, Reddy DS, Shetty AK. 2006. Hippocampal neurodegeneration, spontaneous seizures and mossy fiber sprouting in F344 rat model of temporal lobe epilepsy. J Neurosci Res 83:1088–1105.
147. Reddy DS. 2010. Clinical pharmacokinetic interactions between antiepileptic drugs and hormonal contraceptives. Expert Rev Clin Pharmacol 3:183–192.
148. Reddy DS. 2013. Role of hormones and neurosteroids in epileptogenesis. Front Cell Neuroscience 7:1–20.
149. Reddy DS. 2014. Clinical pharmacology of current antiepileptic drugs. Int J Pharm Sci Nanotech 7:2305–2319.
150. Reddy DS, Kuruba R. 2013. Experimental models of status epilepticus and neuronal injury for evaluation of therapeutic interventions. Int J Mol Sci 14:18284–18318.
151. Reddy DS, Mohan A. 2011. Development and persistence of limbic epileptogenesis are impaired in mice lacking progesterone receptors. J Neurosci 31:650–658.
152. Reglodi D, Somogyvari-Vigh A, Maderdrut JL, Vigh S, Arimura A. 2000. Postischemic spontaneous hyperthermia and its effects in MCA occlusion in the rat. Exp Neurol 163:399–407.
153. Robinson MJ, Macrae IM, Todd M, Reid JL, McCulloch J. 1991. Reduction in local cerebral blood flow induced by ET-1 applied topically to the MCA in the rat. J Cardiovasc Pharmacol 17:S354–S357.
154. Rojas JI, Zurr ' u MC, Romano M, Patrucco L, Cristiano E. 2007. Acute ischemic stroke and transient ischemic attack in the very old—risk factor profile and stroke subtype between patients older than 80 years and patients aged less than 80 years. Eur J Neurol 14:895–899.
155. Rosenblum WI, El-Sabban F. 1977. Platelet aggregation in the cerebral microcirculation: effect of aspirin and other agents. Circ Res 40:320–328.
156. Rossmeisl JH Jr, Rohleder JJ, Pickett JP, Duncan R, Herring IP. 2007. Presumed and confirmed striatocapsular brain infarctions in 6 dogs. Vet Ophthalmol 10:23–36.
157. Rubanyi GM, Polokoff MA. 1994. Endothelins: Molecular biology, biochemistry, pharmacology, physiology, and pathophysiology. Pharmacol Rev 46:325–415.
158. Ryglewicz D, Baranska-Gieruszczak M, Niedzielska K, Kryst-Widzgowska T. 1990. EEG and CT findings in poststroke epilepsy. Acta Neurol Scand 81:488–490.
159. Sacquegna T, De Carolis P, Andreoli A, Ferrara R, Limoni P, Testa C, Lugaresi E. 1984. Long term prognosis after occlusion of middle cerebral artery. Br Med J Clin Res E 288:1490–1491.
160. Saver JL, Johnston KC, Homer D, Wityk R, Koroshetz W, Truskowski LL. 1999. Infarct volume as a surrogate or auxiliary outcome measure in ischemic stroke clinical trials. The RANTTAS Investigators. Stroke 30:293–298.
161. Schroeter M, Franke C, Stoll G, Hoehn M. 2001. Dynamic changes of magnetic resonance imaging abnormalities in relation to inflammation and glial responses after photothrombotic cerebral infarction in the rat brain. Acta Neuropathol 101:114–122.
162. Selvamani A, Sohrabji F. 2010a. The neurotoxic effects of estrogen on ischemic stroke in older female rats is associated with age-dependent loss of insulin-like growth factor-1. J Neurosci 30:6852–6861.
163. Selvamani A, Sohrabji F. 2010b. Reproductive age modulates the impact of focal ischemia on the forebrain as well as the effects of estrogen treatment in female rats. Neurobiol Aging 31:1618–1628.
164. Sharkey J, Butcher SP. 1995. Characterization of an experimental model of stroke produced by intracerebral microinjection of endothelin-1 adjacent to the rat middle cerebral artery. J Neurosci Methods 60:125–131.
165. Sharkey J, Ritchie IM, Kelly PA. 1993. Perivascular microapplication of endothelin-1: a new model of focal cerebral ischemia in the rat. J Cereb Blood Flow Metab 13:865–871.
166. Silverman IE, Restrepo L, Mathews GC. 2002. Poststroke seizures. Arch Neurol 59:195–201.
167. Sironi L, Tremoli E, Miller I, Guerrini U, Calvio AM, Eberini I, Gemeiner M, Asdente M, Paoletti R, Gianazza E. 2001. Acute phase proteins before cerebral ischemia in stroke-prone rats: identification by proteomics. Stroke 32:753–760.
168. Sironi L, Tremoli E, Calvio AM, Bellosta S, Lodetti B, Guerrini U, Monetti M, Tremoli E, Mussoni L. 2003. Endogenous proteolytic activity in a rat model of spontaneous cerebral stroke. Brain Res 974:184–192.
169. Sironi L, Guerrini U, Tremoli E, Miller I, Gelosa P, Lascialfari A, Zucca I, Eberini I, Gemeiner M, Paoletti R, Gianazza E. 2004. Analysis of pathological events at the onset of brain damage in stroke-prone rats: a proteomics and magnetic resonance imaging approach. J Neurosci Res 78:115–122.
170. Slapo GD, Lossius MI, Gjerstad L. 2006. Poststroke epilepsy: occurrence, predictors and treatment. Expert Rev Neurother 6:1801–1809.
171. Sohrabji F, Welsh CJ, Reddy DS. 2015. Sex differences in neurological diseases. In: Shansky E, editor. Sex differences in the central nervous system. New York: Elsevier. p 1–28.
172. Stefan H, Theodore WH. 2012a. Epilepsy. Part I, basic principles and diagnosis. Hndbk Clin Neurol vol 107. Amsterdam: Elsevier. Online resource (xiii, p 482).
173. Stefan H, Theodore WH. 2012b. Epilepsy. Part II, treatment. Hndbk Clin Neurol. Amsterdam: Elsevier. Online resource (xiii, p 485–1004).
174. Suman S, Das P. 2003. Management of epilepsy in the elderly. Geriatr Med 33:61–67.
175. Sun DA, Sombati S, DeLorenzo RJ. 2001. Glutamate injury induced epileptogenesis in hippocampal neurons. An in vitro model of stroke-induced “epilepsy.” Stroke 32:2344–2350.
176. Sun DA, Sombati S, Blair RE, DeLorenzo RJ. 2002. Calcium-dependent epileptogenesis in an in vitro model of stroke-induced “epilepsy.” Epilepsia 43:1296–1305.
177. Sun YY, Yang D, Kuan CY. 2012. Mannitol-facilitated perfusion staining with 2,3,5-triphenyltetrazolium chloride (TTC) for detection of experimental cerebral infarction and biochemical analysis. J Neurosci Methods 203:122–129.
178. Toshima Y, Satoh S, Ikegaki I, Asano T. 2000. A new model of cerebral microthrombosis in rats and the neuroprotective effect of a Rho-kinase inhibitor. Stroke 31:2245–2250.
179. Türeyen K, Vemuganti R, Sailor KA, Dempsey RJ. 2004. Infarct volume quantification in mouse focal cerebral ischemia: a comparison of triphenyltetrazolium chloride and cresyl violet staining techniques. J Neurosci Methods 139:203–207.
180. Tyson GW, Teasdale GM, Graham DI, McCulloch J. 1982. Cerebrovascular permeability following MCA occlusion in the rat. The effect of halothane-induced hypotension. J Neurosurg 57:186–196.
181. Valeri CR, Feingold H, Cassidy G, Ragno G, Khuri S, Altschule MD. 1987. Hypothermia-induced reversible platelet dysfunction. Ann Surg 205:175–181.
182. Venance L, Premont J, Glowinski J, Giaume C. 1998. Gap junctional communication and pharmacological heterogeneity in astrocytes cultured from the rat striatum. J Physiol 510:429–440.
183. Volpe M, Russo R, Vecchione C, Savoia C, Piras O, Gigante B, Lind-Paintner K, Rubattu S. 1998. Endothelial dysfunction and genetic pre-disposition to stroke in spontaneously hypertensive rats. J Hypertens 16:S31–S35.
184. Wang CX, Todd KG, Yang Y, Gordon T, Shuaib A. 2001a. Patency of cerebral microvessels after focal embolic stroke in the rat. J Cereb Blood Flow Metab 21:413–421.
185. Wang CX, Yang T, Shuaib A. 2001b. An improved version of embolic model of brain ischemic injury in the rat. J Neurosci Methods 109:147–151.
186. Watson BD, Dietrich WD, Busto R, Wachtel MS, Ginsberg MD. 1985. Induction of reproducible brain infarction by photochemically initiated thrombosis. Ann Neurol 17:497–504.
187. Watson BD, Dietrich WD, Prado R, Ginsberg MD. 1987. Argon laser-induced arterial photothrombosis. Characterization and possible application to therapy of arteriovenous malformations. J Neurosurg 66:748–754.
188. Watson BD, Prado R, Veloso A, Brunshwig JP, Dietrich WD. 2002. Cerebral blood flow restoration and reperfusion injury after ultraviolet laser-facilitated MCA recanalization in rat thrombotic stroke. Stroke 33:428–434.
189. Wester P, Dietrich WD, Prado R, Watson BD, Globus MY. 1992. Serotonin release into plasma during common carotid artery thrombosis in rats. Stroke 23:870–875.
190. Williams AJ, Tortella FC, Lu XM, Moreton JE, Hartings JA. 2004. Antiepileptic drug treatment of nonconvulsive seizures induced by experimental focal brain ischemia. J Pharmacol Exp Ther 311:220–227.
191. Wolberg AS, Meng ZH, Monroe III DM, Hoffman M. 2004. A systematic evaluation of the effect of temperature on coagulation enzyme activity and platelet function. J Trauma 56:1221–1228.
192. Yamashita K, Busch E, Wiessner C, Hossmann KA. 1997. Thread occlusion but not electrocoagulation of the MCA causes hypothalamic damage with subsequent hyperthermia. Neurol Med Chir 37:723–727.
193. Yamori Y, Horie R, Tanase H, Fujiwara K, Nara Y, Lovenberg W. 1984. Possible role of nutritional factors in the incidence of cerebral lesions in stroke-prone spontaneously hypertensive rats. Hypertension 6:49–53.
194. Yanagisawa M, Kurihara H, Kimura S. 1988. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 332:411–415.
195. Yanamoto H, Nagata I, Niitsu Y, Zhang Z, Xue JH, Sakai N. 2001. Prolonged mild hypothermia therapy protects the brain against permanent focal ischemia. Stroke 32:232–239.
196. Yoshimine T, Yanagihara T. 1983. Regional cerebral ischemia by occlusion of the posterior communicating artery and the middle cerebral artery in gerbils. J Neurosurg 58:362–367.
197. Zhang RL, Chopp M, Zhang ZG, Jiang Q, Ewing JR. 1997. A rat model of focal embolic cerebral ischemia. Brain Res 766:83–92.
198. Zhang Z, Zhang RL, Jiang Q, Raman SB, Cantwell L, Chopp M. 1997. A new rat model of thrombotic focal cerebral ischemia. J Cereb Blood Flow Metab 17:123–135.