Modulation of antioxidant enzymatic activities by certain antiepileptic drugs (valproic acid, oxcarbazepine, and topiramate): Evidence in humans and experimental models

Oxidative Medicine and Cellular Longevity

Volumn , Issue , 2013, Pages

  Cárdenas Rodríguez, Noemí ^a   Coballase Urrutia, Elvia ^a   Rivera Espinosa, Liliana ^a   Romero Toledo, Arantxa ^a   Sampieri, Aristides Iii ^b   Ortega Cuellar, Daniel ^a   Montesinos Correa, Hortencia ^a   Floriano Sánchez, Esaú ^c   Carmona Aparicio, Liliana ^a  

^a INSTITUTO NACIONAL DE PEDIATRÍA   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

ANTICONVULSIVE AGENT; ANTIOXIDANT; CARBAMAZEPINE; DRUG DERIVATIVE; ENZYME; FRUCTOSE; OXCARBAZEPINE; TOPIRAMATE; VALPROIC ACID;

ANIMAL; CHEMISTRY; DISEASE MODEL; DRUG EFFECT; HUMAN; METABOLISM; OXIDATIVE STRESS; REVIEW;

ANIMALS; ANTICONVULSANTS; ANTIOXIDANTS; CARBAMAZEPINE; DISEASE MODELS, ANIMAL; ENZYMES; FRUCTOSE; HUMANS; OXIDATIVE STRESS; VALPROIC ACID;

EID: 84893874304     PISSN: 19420900     EISSN: 19420994     Source Type: Journal    
DOI: 10.1155/2013/598493     Document Type: Review

References (77)

1. Lara T., Análisis Clínico-epidemiológico de la Epilepsia en la hospitalización psiquiátrica del Instituto Nacional de Neurología y Neurocirugía "Manuel Velasco Suárez" Una revisión de cuatro años. Revista Argentina De Neurología, Psiquiatría Y Neurocirugía 2002 35 4 177 182
2. Engel J. Jr., Concepts of epilepsy. Epilepsia 1995 36 1 S23 S29 2-s2.0-0029064451
3. Lara T. H., Ramírez R. L., Epidemiología de la Epilepsia en México. Un análisis interinstitucional de veinticinco años. Revista Neurologia, Neurocirugia Psiquiatria 1993 33 11 20
4. Jacobs M. P., Fischbach G. D., Davis M. R., Dichter M. A., Dingledine R., Lowenstein D. H., Morrell M. J., Noebels J. L., Rogawski M. A., Spencer S. S., Theodor (Pubitemid 33055465)
5. Auvin S., Pineda E., Shin D., Gressens P., Mazarati A., Novel animal models of pediatric epilepsy. Neurotherapeutics 2012 9 2 245 261 2-s2.0-84859713398 10.1007/s13311-012-0119-8
6. ILAE, Commision on Classification and Terminology of the International League Against Epilepsy, Proposal for revised clinical and electroencephalographic classification of epileptic seizures. From the Commission on Classification and Terminology of the International League Against Epilepsy. Epilepsia 1981 22 4 489 501 10.1111/j.1528-1157.1981.tb06159.x
7. ILAE, Proposal for revised classification of epilepsies and epileptic syndromes. Commission on Classification and Terminology of the International League Against Epilepsy. Epilepsia 1989 30 4 389 399
8. Reynolds E. H., Introduction: epilepsy in the world. Epilepsia 2002 43 6 1 3 2-s2.0-0036039639 (Pubitemid 35006453)
9. Sentíes-Madrid H., Guías del Capítulo Mexicano de la Liga Internacional contra la Epilepsia. Antiepilépticos de primera generación contra antiepilépticos de segunda generación: énfasis en efectos adversos de la segunda generación. 2012
10. Shorvon S. D., Drug treatment of epilepsy in the century of the ILAE: the second 50 years, 1959-2009. Epilepsia 2009 50 3 93 130 2-s2.0-62149128648 10.1111/j.1528-1167.2009.02042.x
11. Löscher W., Schmidt D., Modern antiepileptic drug development has failed to deliver: ways out of the current dilemma. Epilepsia 2011 52 4 657 678 2-s2.0-79953705357 10.1111/j.1528-1167.2011.03024.x
12. Loscher W., In vivo administration of valproate reduces the nerve terminal (synaptosomal) activity of GABA aminotransferase in discrete brain areas of rats. Neuroscience Letters 1993 160 2 177 180 2-s2.0-0027437539 10.1016/0304-3940(93)90407-C (Pubitemid 23294734)
13. Biggs C. S., Pearce B. R., Fowler L. J., Whitton P. S., The effect of sodium valproate on extracellular GABA and other amino acids in the rat ventral hippocampus: an in vivo microdialysis study. Brain Research 1992 594 1 138 142 2-s2.0-0026451073 10.1016/0006-8993(92)91038-G
14. Rowley H. L., Marsden C. A., Martin K. F., Differential effects of phenytoin and sodium valproate on seizure-induced changes in γ -aminobutyric acid and glutamate release in vivo. European Journal of Pharmacology 1995 294 2-3 541 546 2-s2.0-0029558289 10.1016/0014-2999(95)00589-7 (Pubitemid 26013243)
15. Vriend J. P., Alexiuk N. A. M., Effects of valproate on amino acid and monoamine concentrations in striatum of audiogenic seizure-prone Balb/c mice. Molecular and Chemical Neuropathology 1996 27 3 307 324 2-s2.0-0029972872 (Pubitemid 26142653)
16. Bolanos J. P., Medina J. M., Evidence of stimulation of the γ -aminobutyric acid shunt by valproate and E-Δ2-valproate in neonatal rat brain. Molecular Pharmacology 1993 43 3 487 490 2-s2.0-0027535423 (Pubitemid 23082007)
17. Loescher W., Effect of inhibitors of GABA Aminotransferase on the metabolism of GABA in brain tissue and synaptosomal fractions. Journal of Neurochemistry 1981 36 4 1521 1527 2-s2.0-0019795227 (Pubitemid 11070821)
18. van der Laan J. W., de Boer Th. D. B. T., Bruinvels J., Di-n-propylacetate and GABA degradation. Preferential inhibition of succinic semialdehyde dehydrogenase and indirect inhibition of GABA-transaminase. Journal of Neurochemistry 1979 32 6 1769 1780 2-s2.0-0018774833 (Pubitemid 9195173)
19. Whittle S. R., Turner A. J., Effects of anticonvulsant sodium valproate on γ -aminobutyrate and aldehyde metabolism in ox brain. Journal of Neurochemistry 1978 31 6 1453 1459 2-s2.0-0018084690 (Pubitemid 9049848)
20. Collins R. M. Jr., Zielke H. R., Woody R. C., Valproate increases glutaminase and decreases glutamine synthetase activities in primary cultures of rat brain astrocytes. Journal of Neurochemistry 1994 62 3 1137 1143 2-s2.0-0028009975 (Pubitemid 24064530)
21. Cutrer F. M., Limmroth V., Ayata G., Moskowitz M. A., Attenuation by valproate of c-fos immunoreactivity in trigeminal nucleus caudalis induced by intracisternal capsaicin. British Journal of Pharmacology 1995 116 8 3199 3204 2-s2.0-0029617710 (Pubitemid 26007763)
22. Zeise M. L., Kasparow S., Zieglgansberger W., Valproate suppresses N-methyl-D-aspartate-evoked transient depolarizations in the rat neocortex in vitro. Brain Research 1991 544 2 345 348 2-s2.0-0025876974 10.1016/0006-8993(91) 90078-A
23. Gean P.-W., Huang C.-C., Hung C.-R., Tsai J.-J., Valproic acid suppresses the synaptic response mediated by the NMDA receptors in rat amygdalar slices. Brain Research Bulletin 1994 33 3 333 336 2-s2.0-0028366472 10.1016/0361- 9230(94)90202-X
24. Dreier J. P., Heinemann U., Late low magnesium-induced epileptiform activity in rat entorhinal cortex slices becomes insensitive to the anticonvulsant valproic acid. Neuroscience Letters 1990 119 1 68 70 2-s2.0-0025119256 10.1016/0304-3940(90)90757-Z (Pubitemid 20349729)
25. Buchhalter J. R., Dichter M. A., Effects of valproic acid in cultured mammalian neurons. Neurology 1986 36 2 259 262 2-s2.0-0022624221 (Pubitemid 16124218)
26. Farrant M., Webster R. A., Neuronal activity, amino acid concentration and amino acid release in the substantia nigra of the rat after sodium valproate. Brain Research 1989 504 1 49 56 2-s2.0-0024842228 10.1016/0006-8993(89)91596-5 (Pubitemid 20014038)
27. Gaillard W. D., Zeffiro T., Fazilat S., DeCarli C., Theodore W. H., Effect of valproate on cerebral metabolism and blood flow: an 18F-2-deoxyglusose and 15O water positron emission tomography study. Epilepsia 1996 37 6 515 521 2-s2.0-0029996597 10.1111/j.1528-1157.1996.tb00602.x (Pubitemid 26169184)
28. May T. W., Korn-Merker E., Rambeck B., Clinical pharmacokinetics of oxcarbazepine. Clinical Pharmacokinetics 2003 42 12 1023 1042 2-s2.0-0141650365 10.2165/00003088-200342120-00002 (Pubitemid 37186675)
29. Stefani A., Pisani A., de Murtas M., Mercuri N. B., Marciani M. G., Calabresi P., Action of GP 47779, the active metabolite of oxcarbazepine, on the corticostriatal system. II. Modulation of high-voltage-activated calcium currents. Epilepsia 1995 36 10 997 1002 2-s2.0-0029082313 10.1111/j.1528-1157. 1995.tb00958.x
30. Waldmeier P. C., Baumann P. A., Wicki P., Feldtrauer J.-J., Stierlin C., Schmutz M., Similar potency of carbamazepine, oxcarbazepine, and lamotrigine in inhibiting the release of glutamate and other neurotransmitters. Neurology 1995 45 10 1907 1913 2-s2.0-0029432189 (Pubitemid 27122967)
31. DeLorenzo R. J., Sombati S., Coulter D. A., Effects of topiramate on sustained repetitive firing and spontaneous recurrent seizure discharges in cultured hippocampal neurons. Epilepsia 2000 41 1 S40 S44 2-s2.0-0034128349 (Pubitemid 30202340)
32. White H. S., Brown S. D., Woodhead J. H., Skeen G. A., Wolf H. H., Topiramate enhances GABA-mediated chloride flux and GABA-evoked chloride currents in murine brain neurons and increases seizure threshold. Epilepsy Research 1997 28 3 167 179 2-s2.0-0030758984 10.1016/S0920-1211(97)00045-4 (Pubitemid 27400459)
33. White H. S., Brown S. D., Woodhead J. H., Skeen G. A., Wolf H. H., Topiramate modulates GABA-evoked currents in murine cortical neurons by a nonbenzodiazepine mechanism. Epilepsia 2000 41 1 S17 S20 2-s2.0-0034074118 (Pubitemid 30202335)
34. Valko M., Rhodes C. J., Moncol J., Izakovic M., Mazur M., Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chemico-Biological Interactions 2006 160 1 1 40 2-s2.0-32444433202 10.1016/j.cbi.2005.12.009 (Pubitemid 43227479)
35. Inoue M., Sato E. F., Nishikawa M., Park A.-M., Kira Y., Imada I., Utsumi K., Mitochondrial generation of reactive oxygen species and its role in aerobic life. Current Medicinal Chemistry 2003 10 23 2495 2505 2-s2.0-0344513852 10.2174/0929867033456477 (Pubitemid 37460972)
36. Waldbaum S., Patel M., Mitochondria, oxidative stress, and temporal lobe epilepsy. Epilepsy Research 2010 88 1 23 45 2-s2.0-72249087964 10.1016/j.eplepsyres.2009.09.020
37. Cardenas-Rodriguez N., Huerta-Gertrudis B., Rivera-Espinosa L., Role of oxidative stress in refractory epilepsy: evidence in patients and experimental models. International Journal of Molecular Sciences 2013 14 1 1455 1476 10.3390/ijms14011455
38. Ansari M. A., Ahmad A. S., Ahmad M., Salim S., Yousuf S., Ishrat T., Islam F., Selenium protects cerebral ischemia in rat brain mitochondria. Biological Trace Element Research 2004 101 1 73 86 2-s2.0-9144228723 10.1385/BTER:101:1:73 (Pubitemid 39546227)
39. Bondy S. C., The relation of oxidative stress and hyperexcitation to neurological disease. Proceedings of the Society for Experimental Biology and Medicine 1995 208 4 337 345 2-s2.0-0028969188
40. Dalton T., Temporalspatial patterns of expression of metallothionein-I and -III and other stress related genes in rat brain after kainic acid-induced seizures. Neurochemistry International 1995 27 1 59 71 2-s2.0-0029013734 10.1016/0197-0186(94)00168-T
41. Patel M., Day B. J., Crapo J. D., Fridovich I., McNamara J. O., Requirement for superoxide in excitotoxic cell death. Neuron 1996 16 2 345 355 2-s2.0-0030052530 10.1016/S0896-6273(00)80052-5 (Pubitemid 26072367)
42. Uma Devi P., Kolappa Pillai K., Vohora D., Modulation of pentylenetetrazole-induced seizures and oxidative stress parameters by sodium valproate in the absence and presence of N-acetylcysteine. Fundamental and Clinical Pharmacology 2006 20 3 247 253 2-s2.0-33646508512 10.1111/j.1472-8206. 2006.00401.x
43. Armaan A., Kutluhan S., Yilmaz M., Yilmaz N., Bülbül M., Vural H., Soyupek S., Nazirolu M., Topiramate and vitamin E modulate antioxidant enzyme activities, nitric oxide and lipid peroxidation levels in pentylenetetrazol-induced nephrotoxicity in rats. Basic and Clinical Pharmacology and Toxicology 2008 103 2 166 170 2-s2.0-47649108138 10.1111/j.1742-7843.2008.00271.x (Pubitemid 352019728)
44. Frantseva M. V., Perez Velazquez J. L., Tsoraklidis G., Mendonca A. J., Adamchik Y., Mills L. R., Carlen P. L., Burnham M. W., Oxidative stress is involved in seizure-induced neurodegeneration in the kindling model of epilepsy. Neuroscience 2000 97 3 431 435 2-s2.0-0034112506 10.1016/S0306-4522(00)00041-5 (Pubitemid 30320750)
45. Schweizer U., Bräuer A. U., Köhrle J., Nitsch R., Savaskan N. E., Selenium and brain function: a poorly recognized liaison. Brain Research Reviews 2004 45 3 164 178 2-s2.0-3042693925 10.1016/j.brainresrev.2004.03.004 (Pubitemid 38802869)
46. Kovács R., Schuchmann S., Gabriel S., Kann O., Kardos J., Heinemann U., Free radical-mediated cell damage after experimental status epilepticus in hippocampal slice cultures. Journal of Neurophysiology 2002 88 6 2909 2918 2-s2.0-0036900547 (Pubitemid 35448678)
47. White H. S., Smith M. D., Wilcox K. S., Mechanisms of action of antiepileptic drugs. International Review of Neurobiology 2007 81 85 110 2-s2.0-34047204206 10.1016/S0074-7742(06)81006-8
48. Singh P., Mann K. A., Mangat H. K., Kaur G., Prolonged glutamate excitotoxicity: effects on mitochondrial antioxidants and antioxidant enzymes. Molecular and Cellular Biochemistry 2003 243 1-2 139 145 2-s2.0-0037286186 10.1023/A:1021668314070 (Pubitemid 36240561)
49. Granger D. N., Role of xanthine oxidase and granulocytes in ischemia-reperfusion injury. American Journal of Physiology-Heart and Circulatory Physiology 1988 255 6, part 2 H1269 H1275 2-s2.0-0024203618
50. Hensley K., Maidt M. L., Pye Q. N., Stewart C. A., Wack M., Tabatabaie T., Floyd R. A., Quantitation of protein-bound 3-nitrotyrosine and 3,4-dihydroxyphenylalanine by high-performance liquid chromatography with electrochemical array detection. Analytical Biochemistry 1997 251 2 187 195 2-s2.0-0031554894 10.1006/abio.1997.2281 (Pubitemid 27392677)
51. Kurekci A. E., Alpay F., Tanindi S., Gokcay E., Ozcan O., Akin R., Isimer A., Sayal A., Plasma trace element, plasma glutathione peroxidase, and superoxide dismutase levels in epileptic children receiving antiepileptic drug therapy. Epilepsia 1995 36 6 600 604 2-s2.0-0029071815 10.1111/j.1528-1157.1995. tb02574.x
52. Cengiz M., Yüksel A., Seven M., The effects of carbamazepine and valproic acid on the erythrocyte glutathione, glutathione peroxidase, superoxide dismutase and serum lipid peroxidation in epileptic children. Pharmacological Research 2000 41 4 423 425 2-s2.0-0033840503 10.1006/phrs.1999.0603
53. Yüksel A., Cengiz M., Seven M., Ulutin T., Erythrocyte glutathione, glutathione peroxidase, superoxide dismutase and serum lipid peroxidation in epileptic children with valproate and carbamazepine monotherapy. Journal of Basic and Clinical Physiology and Pharmacology 2000 11 1 73 81 2-s2.0-0033927211 (Pubitemid 30470388)
54. Yüksel A., Cengiz M., Seven M., Ulutin T., Changes in the antioxidant system in epileptic children receiving antiepileptic drugs: two-year prospective studies. Journal of Child Neurology 2001 16 8 603 606 2-s2.0-0034850858 (Pubitemid 32798887)
55. Verrotti A., Basciani F., Trotta D., Pomilio M. P., Morgese G., Chiarelli F., Serum copper, zinc, selenium, glutathione peroxidase and superoxide dismutase levels in epileptic children before and after 1 year of sodium valproate and carbamazepine therapy. Epilepsy Research 2002 48 1-2 71 75 2-s2.0-0036163554 10.1016/S0920-1211(01)00322-9 (Pubitemid 34127718)
56. Sołowiej E., Sobaniec W., The effect of antiepileptic drug therapy on antioxidant enzyme activity and serum lipid peroxidation in young patients with epilepsy. Neurologia i Neurochirurgia Polska 2003 37 5 991 1003 2-s2.0-18244430557
57. Hamed S. A., Abdellah M. M., El-Melegy N., Blood levels of trace elements, electrolytes, and oxidative stress/antioxidant systems in epileptic patients. Journal of Pharmacological Sciences 2004 96 4 465 473 2-s2.0-12444315074 10.1254/jphs.FPJ04032X (Pubitemid 40144068)
58. Bolayir E., Celik K., Tas A., Topaktas S., Bakir S., The effects of oxcarbazepine on oxidative stress in epileptic patients. Methods and Findings in Experimental and Clinical Pharmacology 2004 26 5 345 348 2-s2.0-3242715879 10.1358/mf.2004.26.5.831325 (Pubitemid 38954810)
59. Martínez-Ballesteros C., Pita-Calandre E., Sánchez- González Y., Rodríguez-López C. M., Agil A., Lipid peroxidation in adult epileptic patients treated with valproic acid. Revista de Neurologia 2004 38 2 101 106 2-s2.0-1342333394 (Pubitemid 38252129)
60. Sobaniec W., Solowiej E., Kulak W., Bockowski L., Smigielska-Kuzia J., Artemowicz B., Evaluation of the influence of antiepileptic therapy on antioxidant enzyme activity and lipid peroxidation in erythrocytes of children with epilepsy. Journal of Child Neurology 2006 21 7 558 562 2-s2.0-33748035379 10.2310/7010.2006.00115 (Pubitemid 44295134)
61. Peker E., Oktar S., Ari M., Kozan R., Doan M., Çaan E., Söüt S., Nitric oxide, lipid peroxidation, and antioxidant enzyme levels in epileptic children using valproic acid. Brain Research 2009 1297 194 197 2-s2.0-71749119931 10.1016/j.brainres.2009.08.048
62. Güneş S., Dirik E., Yiş U., Seçkin E., Kuralay F., Köse S., Ünalp A., Oxidant status in children after febrile seizures. Pediatric Neurology 2009 40 1 47 49 2-s2.0-57049172473 10.1016/j.pediatrneurol.2008.09.006
63. Varoglu A. O., Yildirim A., Aygul R., Gundogdu O. L., Sahin Y. N., Effects of valproate, carbamazepine, and levetiracetam on the antioxidant and oxidant systems in epileptic patients and their clinical importance. Clinical Neuropharmacology 2010 33 3 155 157 2-s2.0-77953228720 10.1097/WNF. 0b013e3181d1e133
64. Arhan E., Serdaroglu A., Ozturk B., Ozturk H. S., Ozcelik A., Kurt N., Kutsal E., Sevinc N., Effects of epilepsy and antiepileptic drugs on nitric oxide, lipid peroxidation and xanthine oxidase system in children with idiopathic epilepsy. Seizure 2011 20 2 138 142 2-s2.0-79551577307 10.1016/j.seizure.2010.11.003
65. Zhang Y. J., Zhang M., Wang X. C., Effects of sodium valproate on neutrophils' oxidative metabolism and oxidant status in children with idiopathic epilepsy. Chinese Journal of Pediatrics 2011 49 10 776 781
66. Chaudhary S., Parvez S., An in vitro approach to assess the neurotoxicity of valproic acid-induced oxidative stress in cerebellum and cerebral cortex of young rats. Neuroscience 2012 225 258 268 10.1016/j.neuroscience.2012.08.060
67. Yiş U., Seçkin E., Kurul S. H., Kuralay F., Dirik E., Effects of epilepsy and valproic acid on oxidant status in children with idiopathic epilepsy. Epilepsy Research 2009 84 2-3 232 237 2-s2.0-64149083246 10.1016/j.eplepsyres.2009.02.003
68. Aycicek A., Iscan A., The effects of carbamazepine, valproic acid and phenobarbital on the oxidative and antioxidative balance in epileptic children. European Neurology 2007 57 2 65 69 2-s2.0-33846987936 10.1159/000098053
69. Seçkin Ş., Başaran-Küçükgergin C., Uysal M., Effect of acute and chronic administration of sodium valproate on lipid peroxidation and antioxidant system in rat liver. Pharmacology and Toxicology 1999 85 6 294 298 2-s2.0-0033461218 (Pubitemid 30012378)
70. Cardile V., Pavone A., Renis M., Maci T., Perciavalle V., Effects of gabapentin and topiramate in primary rat astrocyte cultures. NeuroReport 2001 12 8 1705 1708 2-s2.0-0035854084 (Pubitemid 32521490)
71. Pavone A., Cardile V., An in vitro study of new antiepileptic drugs and astrocytes. Epilepsia 2003 44 10 34 39 2-s2.0-0142072675 10.1046/j.1528-1157.44. s10.5.x (Pubitemid 37280391)
72. Agarwal N. B., Agarwal N. K., Mediratta P. K., Sharma K. K., Effect of lamotrigine, oxcarbazepine and topiramate on cognitive functions and oxidative stress in PTZ-kindled mice. Seizure 2011 20 3 257 262 2-s2.0-79952452229 10.1016/j.seizure.2010.12.006
73. Muriach M., López-Pedrajas R., Barcia J. M., Sanchez-Villarejo M. V., Almansa I., Romero F. J., Cocaine causes memory and learning impairments in rats: involvement of nuclear factor kappa B and oxidative stress, and prevention by topiramate. Journal of Neurochemistry 2010 114 3 675 684 2-s2.0-77954338704 10.1111/j.1471-4159.2010.06794.x
74. Kutluhan S., Nazirolu M., Çelik Ö., Yilmaz M., Effects of selenium and topiramate on lipid peroxidation and antioxidant vitamin levels in blood of pentylentetrazol-induced epileptic rats. Biological Trace Element Research 2009 129 1-3 181 189 2-s2.0-67650486346 10.1007/s12011-008-8287-4
75. Nazirolu M., Uuz A. C., Gokçimen A., Bülbül M., Karatopuk D. U., Türker Y., Çerçi C., Tenoxicam modulates antioxidant redox system and lipid peroxidation in rat brain. Neurochemical Research 2008 33 9 1832 1837 2-s2.0-48349141606 10.1007/s11064-008-9643-7
76. Kubera M., Budziszewska B., Jaworska-Feil L., Basta-Kaim A., Leśkiewicz M., Tetich M., Maes M., Kenis G., Marciniak A., Czuczwar S. J., Jagła G., Nowak W., Lasoń W., Effect of topiramate on the kainate-induced status epilepticus, lipid peroxidation and immunoreactivity of rats. Polish Journal of Pharmacology 2004 56 5 553 561 2-s2.0-19944429222 (Pubitemid 40123655)
77. Cardenas-Rodriguez N., Coballase-Urrutia E., Huerta-Gertrudis B., Antioxidant activity of topiramate: an antiepileptic agent. Neurological Sciences 2013 34 5 741 747 10.1007/s10072-012-1127-5