Ketogenic diet exhibits neuroprotective effects in hippocampus but fails to prevent epileptogenesis in the lithium-pilocarpine model of mesial temporal lobe epilepsy in adult rats

Epilepsia

Volumn 51, Issue 9, 2010, Pages 1829-1836

  Linard, Benjamin ^a   Ferrandon, Arielle ^a   Koning, Estelle ^a   Nehlig, Astrid ^a   Raffo, Emmanuel ^a,b  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b HÔPITAL D ENFANTS   (France)

Author keywords

Calorie restriction; Epileptogenesis; Ketogenic diet; Lithium pilocarpine; Neuroprotection

Indexed keywords

3 HYDROXYBUTYRIC ACID; DIAZEPAM; GLUCOSE; LITHIUM CHLORIDE; PILOCARPINE; SCOPOLAMINE METHYL BROMIDE; SODIUM CHLORIDE; ANTICONVULSIVE AGENT; CARBOHYDRATE DIET; NEUROPROTECTIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTICONVULSANT ACTIVITY; ARTICLE; BRAIN DAMAGE; CALORIC INTAKE; CALORIC RESTRICTION; CARBOHYDRATE DIET; CONTROLLED STUDY; DENTATE GYRUS; ELECTRODE; ELECTROENCEPHALOGRAPHY; ENTORHINAL CORTEX; EPILEPTIC DISCHARGE; EPILEPTIC STATE; EPILEPTOGENESIS; GLUCOSE BLOOD LEVEL; HIPPOCAMPUS; HISTOLOGY; KETOGENIC DIET; LATENT PERIOD; MALE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PYRIFORM CORTEX; RAT; SPIKE WAVE; SUBICULUM; TEMPORAL LOBE EPILEPSY; TREATMENT OUTCOME; VIDEORECORDING; ADMINISTRATION AND DOSAGE; ANIMAL; BRAIN CORTEX; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; DRUG RESISTANCE; EPILEPSY, TEMPORAL LOBE; HUMAN; PROCEDURES; STATISTICS AND NUMERICAL DATA; WISTAR RAT;

ANIMALS; ANTICONVULSANTS; CALORIC RESTRICTION; CEREBRAL CORTEX; DIETARY CARBOHYDRATES; DISEASE MODELS, ANIMAL; DRUG RESISTANCE; ELECTROENCEPHALOGRAPHY; EPILEPSY, TEMPORAL LOBE; HIPPOCAMPUS; HUMANS; KETOGENIC DIET; LITHIUM CHLORIDE; MALE; NEUROPROTECTIVE AGENTS; PILOCARPINE; RATS; RATS, WISTAR; STATUS EPILEPTICUS;

EID: 77956337682     PISSN: 00139580     EISSN: 15281167     Source Type: Journal    
DOI: 10.1111/j.1528-1167.2010.02667.x     Document Type: Article

References (55)

1. Andre V, Ferrandon A, Marescaux C, Nehlig A 2000a) Electroshocks delay seizures and subsequent epileptogenesis but do not prevent neuronal damage in the lithium-pilocarpine model of epilepsy. Epilepsy Res 42 : 7 22.
2. Andre V, Ferrandon A, Marescaux C, Nehlig A 2000b) The lesional and epileptogenic consequences of lithium-pilocarpine-induced status epilepticus are affected by previous exposure to isolated seizures: effects of amygdala kindling and maximal electroshocks. Neuroscience 99 : 469 481.
3. Andre V, Ferrandon A, Marescaux C, Nehlig A 2001) Vigabatrin protects against hippocampal damage but is not antiepileptogenic in the lithium-pilocarpine model of temporal lobe epilepsy. Epilepsy Res 47 : 99 117.
4. Andre V, Rigoulot MA, Koning E, Ferrandon A, Nehlig A 2003) Long-term pregabalin treatment protects basal cortices and delays the occurrence of spontaneous seizures in the lithium-pilocarpine model in the rat. Epilepsia 44 : 893 903.
5. Appleton DB, DeVivo DC 1974) An animal model for the ketogenic diet. Epilepsia 15 : 211 227.
6. Bough KJ, Eagles DA 1999) A ketogenic diet increases the resistance to pentylenetetrazole-induced seizures in the rat. Epilepsia 40 : 138 143.
7. Bough KJ, Valiyil R, Han FT, Eagles DA 1999) Seizure resistance is dependent upon age and calorie restriction in rats fed a ketogenic diet. Epilepsy Res 35 : 21 28.
8. Bough KJ, Matthews PJ, Eagles DA 2000a) A ketogenic diet has different effects upon seizures induced by maximal electroshock and by pentylenetetrazole infusion. Epilepsy Res 38 : 105 114.
9. Bough KJ, Yao SG, Eagles DA 2000b) Higher ketogenic diet ratios confer protection from seizures without neurotoxicity. Epilepsy Res 38 : 15 25.
10. Bough KJ, Schwartzkroin PA, Rho JM 2003) Calorie restriction and ketogenic diet diminish neuronal excitability in rat dentate gyrus in vivo. Epilepsia 44 : 752 760.
11. Bough KJ, Wetherington J, Hassel B, Pare JF, Gawryluk JW, Greene JG, Shaw R, Smith Y, Geiger JD, Dingledine RJ 2006) Mitochondrial biogenesis in the anticonvulsant mechanism of the ketogenic diet. Ann Neurol 60 : 223 235.
12. Cavalheiro E 1995) The pilocarpine model of epilepsy. Ital J Neurol Sci 16 : 33 37.
13. Clifford DB, Olney JW, Maniotis A, Collins RC, Zorumski CF 1987) The functional anatomy and pathology of lithium-pilocarpine and high-dose pilocarpine seizures. Neuroscience 23 : 953 968.
14. Cross JH 2009) The ketogenic diet in epilepsy - monitoring of efficacy. Epilepsia 50 : 330 331.
15. Davenport VD, Davenport HW 1948) The relation between starvation, metabolic acidosis and convulsive seizures in rats. J Nutr 36 : 139 151.
16. Dube C, Boyet S, Marescaux C, Nehlig A 2000a) Progressive metabolic changes underlying the chronic reorganization of brain circuits during the silent phase of the lithium-pilocarpine model of epilepsy in the immature and adult Rat. Exp Neurol 162 : 146 157.
17. Dube C, Marescaux C, Nehlig A 2000b) A metabolic and neuropathological approach to the understanding of plastic changes that occur in the immature and adult rat brain during lithium-pilocarpine-induced epileptogenesis. Epilepsia 41 (suppl 6 S36 S43.
18. Dube C, Boyet S, Marescaux C, Nehlig A 2001) Relationship between neuronal loss and interictal glucose metabolism during the chronic phase of the lithium-pilocarpine model of epilepsy in the immature and adult rat. Exp Neurol 167 : 227 241.
19. Eagles DA, Boyd SJ, Kotak A, Allan F 2003) Calorie restriction of a high-carbohydrate diet elevates the threshold of PTZ-induced seizures to values equal to those seen with a ketogenic diet. Epilepsy Res 54 : 41 52.
20. Erecinska M, Nelson D, Daikhin Y, Yudkoff M 1996) Regulation of GABA level in rat brain synaptosomes: fluxes through enzymes of the GABA shunt and effects of glutamate, calcium, and ketone bodies. J Neurochem 67 : 2325 2334.
21. Fernandes MJ, Dube C, Boyet S, Marescaux C, Nehlig A 1999) Correlation between hypermetabolism and neuronal damage during status epilepticus induced by lithium and pilocarpine in immature and adult rats. J Cereb Blood Flow Metab 19 : 195 209.
22. François J, Ferrandon A, Koning E, Nehlig A 2005) A new drug RWJ 333369 protects limbic aeras in the lithium-pilocarpine model (li-pilo) of epilepsy and delays or prevents the occurence of spontaneous seizures. (abstract). Epilepsia 46 : 269 270.
23. Francois J, Koning E, Ferrandon A, Nehlig A 2006) The combination of topiramate and diazepam is partially neuroprotective in the hippocampus but not antiepileptogenic in the lithium-pilocarpine model of temporal lobe epilepsy. Epilepsy Res 72 : 147 163.
24. Freeman JM, Kelley MT, Freeman JB, a Tkd, treatment for epilepsy reD, New York 2000) The ketogenic diet: a treatment for epilepsy. 3rd ed. Demos, New York.
25. Gasior M, Rogawski MA, Hartman AL 2006) Neuroprotective and disease-modifying effects of the ketogenic diet. Behav Pharmacol 17 : 431 439.
26. Greene AE, Todorova MT, McGowan R, Seyfried TN 2001) Caloric restriction inhibits seizure susceptibility in epileptic EL mice by reducing blood glucose. Epilepsia 42 : 1371 1378.
27. Hansen SL, Nielsen AH, Knudsen KE, Artmann A, Petersen G, Kristiansen U, Hansen SH, Hansen HS 2009) Ketogenic diet is antiepileptogenic in pentylenetetrazole kindled mice and decrease levels of N-acylethanolamines in hippocampus. Neurochem Int 54 : 199 204.
28. Hartman AL, Vining EP 2007) Clinical aspects of the ketogenic diet. Epilepsia 48 : 31 42.
29. Hirsch E, Baram T, Snead O 1992) Ontogenic study of lithium-pilocarpine- induced status epilepticus in rats. Brain Res 583 : 120 126.
30. Hori A, Tandon P, Holmes GL, Stafstrom CE 1997) Ketogenic diet: effects on expression of kindled seizures and behavior in adult rats. Epilepsia 38 : 750 758.
31. Lehmann TN, Gabriel S, Eilers A, Njunting M, Kovacs R, Schulze K, Lanksch WR, Heinemann U 2001) Fluorescent tracer in pilocarpine-treated rats shows widespread aberrant hippocampal neuronal connectivity. Eur J Neurosci 14 : 83 95.
32. Leite J, Bortolotto Z, Cavalheiro E 1990) Spontaneous recurrent sizures in rats : an experimental model of partial epilepsy. Neurosci Biobehav Rev 14 : 511 517.
33. Loscher W, Fiedler M 1996) The role of technical, biological and pharmacological factors in the laboratory evaluation of anticonvulsant drugs. VI. Seasonal influences on maximal electroshock and pentylenetetrazol seizure thresholds. Epilepsy Res 25 : 3 10.
34. Maalouf M, Sullivan PG, Davis L, Kim DY, Rho JM 2007) Ketones inhibit mitochondrial production of reactive oxygen species production following glutamate excitotoxicity by increasing NADH oxidation. Neuroscience 145 : 256 264.
35. Maalouf M, Rho JM, Mattson MP 2009) The neuroprotective properties of calorie restriction, the ketogenic diet, and ketone bodies. Brain Res Rev 59 : 293 315.
36. Mahoney AW, Hendricks DG, Bernhard N, Sisson DV 1983) Fasting and ketogenic diet effects on audiogenic seizures susceptibility of magnesium deficient rats. Pharmacol Biochem Behav 18 : 683 687.
37. Muller-Schwarze AB, Tandon P, Liu Z, Yang Y, Holmes GL, Stafstrom CE 1999) Ketogenic diet reduces spontaneous seizures and mossy fiber sprouting in the kainic acid model. Neuroreport 10 : 1517 1522.
38. Noh HS, Kim YS, Lee HP, Chung KM, Kim DW, Kang SS, Cho GJ, Choi WS 2003) The protective effect of a ketogenic diet on kainic acid-induced hippocampal cell death in the male ICR mice. Epilepsy Res 53 : 119 128.
39. Raffo E, Francois J, Ferrandon A, Koning E, Nehlig A 2008) Calorie-restricted ketogenic diet increases thresholds to all patterns of pentylenetetrazol-induced seizures: critical importance of electroclinical assessment. Epilepsia 49 : 320 328.
40. Rho JM, Kim DW, Robbins CA, Anderson GD, Schwartzkroin PA 1999) Age-dependent differences in flurothyl seizure sensitivity in mice treated with a ketogenic diet. Epilepsy Res 37 : 233 240.
41. Rho JM, Robbins CA, Wenzel J, Tempel BL, Schwartzkroin PA 2000) An experimental ketogenic diet promotes long-term survival and reduces synaptic reorganization in the hippocampus of epileptic KV1.1 null mutant mice. Epilepsia 41 (s7 34.
42. Rigoulot MA, Koning E, Ferrandon A, Nehlig A 2004) Neuroprotective properties of topiramate in the lithium-pilocarpine model of epilepsy. J Pharmacol Exp Ther 308 : 787 795.
43. Roch C, Leroy C, Nehlig A, Namer IJ 2002a) Magnetic resonance imaging in the study of the lithium-pilocarpine model of temporal lobe epilepsy in adult rats. Epilepsia 43 : 325 335.
44. Roch C, Leroy C, Nehlig A, Namer IJ 2002b) Predictive value of cortical injury for the development of temporal lobe epilepsy in 21-day-old rats: an MRI approach using the lithium-pilocarpine model. Epilepsia 43 : 1129 1136.
45. Rogers AE 1979) Nutrition. In Baker HJ, Lindsey JR, Weisbroth SH (Eds) The laboratory rat. Academic Press, New York, pp. 124 152.
46. Santiago JF, Carvalho FF, Perosa SR, Siliano MR, Cruz JW, Fernandes MJ, Cavalheiro EA, Amado D, da Graca Naffah-Mazzacoratti M 2006) Effect of glycemic state in rats submitted to status epilepticus during development. Arq Neuropsiquiatr 64 : 233 239.
47. Su SW, Cilio MR, Sogawa Y, Silveira DC, Holmes GL, Stafstrom CE 2000) Timing of ketogenic diet initiation in an experimental epilepsy model. Brain Res Dev Brain Res 125 : 131 138.
48. Sullivan PG, Rippy NA, Dorenbos K, Concepcion RC, Agarwal AK, Rho JM 2004) The ketogenic diet increases mitochondrial uncoupling protein levels and activity. Ann Neurol 55 : 576 580.
49. Swink TD, Vining EP, Freeman JM 1997) The ketogenic diet: 1997. Adv Pediatr 44 : 297 329.
50. Thavendiranathan P, Mendonca A, Dell C, Likhodii SS, Musa K, Iracleous C, Cunnane SC, Burnham WM 2000) The MCT ketogenic diet: effects on animal seizure models. Exp Neurol 161 : 696 703.
51. Thavendiranathan P, Chow C, Cunnane S, McIntyre Burnham W 2003) The effect of the 'classic' ketogenic diet on animal seizure models. Brain Res 959 : 206 213.
52. Turski W, Cavalheiro E, Schwarz M, Czuczwar S, Kleinrok Z, Turski L 1983) Limbic seizures produced by pilocarpine in rats: behavioral, electroencephalographic and neuropathological study. Behav Brain Res 9 : 315 335.
53. Turski L, Ikonomidou C, Turski W, Bortolotto Z, Cavalheiro E 1989) Cholinergic mechanisms and epileptogenesis. The seizures induced by pilocarpine: a novel experimental model of intractable epilepsy. Synapse 3 : 154 171.
54. Vining EP, Freeman JM, Ballaban-Gil K, Camfield CS, Camfield PR, Holmes GL, Shinnar S, Shuman R, Trevathan E, Wheless JW 1998) A multicenter study of the efficacy of the ketogenic diet. Arch Neurol 55 : 1433 1437.
55. Yudkoff M, Daikhin Y, Nissim I, Lazarow A 2001) Ketogenic diet, amino acid metabolism, and seizure control. J Neurosci Res 66 : 931 940.