Skip to main content
Top
Published in: BMC Neurology 1/2012

Open Access 01-12-2012 | Research article

Clinical significance of serological biomarkers and neuropsychological performances in patients with temporal lobe epilepsy

Authors: Chiung-Chih Chang, Chun-Chung Lui, Chen-Chang Lee, Shang-Der Chen, Wen-Neng Chang, Cheng-Hsien Lu, Nai-Ching Chen, Alice Y W Chang, Samuel H H Chan, Yao-Chung Chuang

Published in: BMC Neurology | Issue 1/2012

Login to get access

Abstract

Background

Temporal lobe epilepsy (TLE) is a common form of focal epilepsy. Serum biomarkers to predict cognitive performance in TLE patients without psychiatric comorbidities and the link with gray matter (GM) atrophy have not been fully explored.

Methods

Thirty-four patients with TLE and 34 sex - and age-matched controls were enrolled for standardized cognitive tests, neuroimaging studies as well as measurements of serum levels of heat shock protein 70 (HSP70), S100ß protein (S100ßP), neuronal specific enolase (NSE), plasma nuclear and mitochondrial DNA levels.

Results

Compared with the controls, the patients with TLE had poorer cognitive performances and higher HSP70 and S100ßP levels (p < 0.01). The patients with higher frequencies of seizures had higher levels of HSP70, NSE and S100ßP (p < 0.01). Serum HSP70 level correlated positively with duration of epilepsy (σ = 0.413, p < 0.01), and inversely with memory scores in the late registration (σ = −0.276, p = 0.01) and early recall score (σ = −0.304, p = 0.007). Compared with the controls, gray matter atrophy in the hippocampal and parahippocampal areas, putamen, thalamus and supplementary motor areas were found in the patient group. The HSP70 levels showed an inverse correlation with hippocampal volume (R square = 0.22, p = 0.007) after controlling for the effect of age.

Conclusions

Our results suggest that serum biomarkers were predictive of higher frequencies of seizures in the TLE group. HSP70 may be considered to be a stress biomarker in patients with TLE in that it correlated inversely with memory scores and hippocampal volume. In addition, the symmetric extratemporal atrophic patterns may be related to damage of neuronal networks and epileptogenesis in TLE.
Appendix
Available only for authorised users
Literature
1.
go back to reference Engel J: A proposed diagnostic scheme for people with epileptic seizures and with epilepsy: report of the ILAE Task Force on Classification and Terminology. Epilepsia. 2001, 42 (6): 796-803. 10.1046/j.1528-1157.2001.10401.x.CrossRefPubMed Engel J: A proposed diagnostic scheme for people with epileptic seizures and with epilepsy: report of the ILAE Task Force on Classification and Terminology. Epilepsia. 2001, 42 (6): 796-803. 10.1046/j.1528-1157.2001.10401.x.CrossRefPubMed
2.
go back to reference Engel J: Report of the ILAE classification core group. Epilepsia. 2006, 47 (9): 1558-1568. 10.1111/j.1528-1167.2006.00215.x.CrossRefPubMed Engel J: Report of the ILAE classification core group. Epilepsia. 2006, 47 (9): 1558-1568. 10.1111/j.1528-1167.2006.00215.x.CrossRefPubMed
3.
go back to reference Thom M, Mathern GW, Cross JH, Bertram EH: Mesial temporal lobe epilepsy: How do we improve surgical outcome?. Ann Neurol. 2010, 68 (4): 424-434. 10.1002/ana.22142.CrossRefPubMedPubMedCentral Thom M, Mathern GW, Cross JH, Bertram EH: Mesial temporal lobe epilepsy: How do we improve surgical outcome?. Ann Neurol. 2010, 68 (4): 424-434. 10.1002/ana.22142.CrossRefPubMedPubMedCentral
4.
go back to reference Tellez-Zenteno JF, Hernandez Ronquillo L, Moien-Afshari F, Wiebe S: Surgical outcomes in lesional and non-lesional epilepsy: a systematic review and meta-analysis. Epilepsy Res. 2010, 89 (2-3): 310-318. 10.1016/j.eplepsyres.2010.02.007.CrossRefPubMed Tellez-Zenteno JF, Hernandez Ronquillo L, Moien-Afshari F, Wiebe S: Surgical outcomes in lesional and non-lesional epilepsy: a systematic review and meta-analysis. Epilepsy Res. 2010, 89 (2-3): 310-318. 10.1016/j.eplepsyres.2010.02.007.CrossRefPubMed
5.
go back to reference Friedman DE, Gilliam FG: Seizure-related injuries are underreported in pharmacoresistant localization-related epilepsy. Epilepsia. 2010, 51 (1): 43-47. 10.1111/j.1528-1167.2009.02170.x.CrossRefPubMed Friedman DE, Gilliam FG: Seizure-related injuries are underreported in pharmacoresistant localization-related epilepsy. Epilepsia. 2010, 51 (1): 43-47. 10.1111/j.1528-1167.2009.02170.x.CrossRefPubMed
6.
go back to reference Chen DK, So YT, Fisher RS: Use of serum prolactin in diagnosing epileptic seizures: report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Neurol. 2005, 65 (5): 668-675. 10.1212/01.wnl.0000178391.96957.d0.CrossRef Chen DK, So YT, Fisher RS: Use of serum prolactin in diagnosing epileptic seizures: report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Neurol. 2005, 65 (5): 668-675. 10.1212/01.wnl.0000178391.96957.d0.CrossRef
7.
go back to reference Cui J, Wang Y, Dong Q, Wu S, Xiao X, Hu J, Chai Z, Zhang Y: Morphine protects against intracellular amyloid toxicity by inducing estradiol release and upregulation of Hsp70. J Neurosci. 2011, 31 (45): 16227-16240. 10.1523/JNEUROSCI.3915-11.2011.CrossRefPubMed Cui J, Wang Y, Dong Q, Wu S, Xiao X, Hu J, Chai Z, Zhang Y: Morphine protects against intracellular amyloid toxicity by inducing estradiol release and upregulation of Hsp70. J Neurosci. 2011, 31 (45): 16227-16240. 10.1523/JNEUROSCI.3915-11.2011.CrossRefPubMed
8.
go back to reference Rabinowicz AL, Correale JD, Bracht KA, Smith TD, DeGiorgio CM: Neuron-specific enolase is increased after nonconvulsive status epilepticus. Epilepsia. 1995, 36 (5): 475-479. 10.1111/j.1528-1157.1995.tb00489.x.CrossRefPubMed Rabinowicz AL, Correale JD, Bracht KA, Smith TD, DeGiorgio CM: Neuron-specific enolase is increased after nonconvulsive status epilepticus. Epilepsia. 1995, 36 (5): 475-479. 10.1111/j.1528-1157.1995.tb00489.x.CrossRefPubMed
9.
go back to reference Thom M, Seetah S, Sisodiya S, Koepp M, Scaravilli F: Sudden and unexpected death in epilepsy (SUDEP): evidence of acute neuronal injury using HSP-70 and c-Jun immunohistochemistry. Neuropathol Appl Neurobiol. 2003, 29 (2): 132-143. 10.1046/j.1365-2990.2003.00452.x.CrossRefPubMed Thom M, Seetah S, Sisodiya S, Koepp M, Scaravilli F: Sudden and unexpected death in epilepsy (SUDEP): evidence of acute neuronal injury using HSP-70 and c-Jun immunohistochemistry. Neuropathol Appl Neurobiol. 2003, 29 (2): 132-143. 10.1046/j.1365-2990.2003.00452.x.CrossRefPubMed
10.
go back to reference DeGiorgio CM, Correale JD, Gott PS, Ginsburg DL, Bracht KA, Smith T, Boutros R, Loskota WJ, Rabinowicz AL: Serum neuron-specific enolase in human status epilepticus. Neurol. 1995, 45 (6): 1134-1137.CrossRef DeGiorgio CM, Correale JD, Gott PS, Ginsburg DL, Bracht KA, Smith T, Boutros R, Loskota WJ, Rabinowicz AL: Serum neuron-specific enolase in human status epilepticus. Neurol. 1995, 45 (6): 1134-1137.CrossRef
11.
go back to reference Buttner T, Lack B, Jager M, Wunsche W, Kuhn W, Muller T, Przuntek H, Postert T: Serum levels of neuron-specific enolase and s-100 protein after single tonic-clonic seizures. J Neurol. 1999, 246 (6): 459-461. 10.1007/s004150050383.CrossRefPubMed Buttner T, Lack B, Jager M, Wunsche W, Kuhn W, Muller T, Przuntek H, Postert T: Serum levels of neuron-specific enolase and s-100 protein after single tonic-clonic seizures. J Neurol. 1999, 246 (6): 459-461. 10.1007/s004150050383.CrossRefPubMed
12.
go back to reference Lu C, Li J, Sun W, Feng L, Li L, Liu A, Mao W, Wei H, Gao L, Zhang X, et al: Elevated plasma S100B concentration is associated with mesial temporal lobe epilepsy in Han Chinese: a case-control study. Neurosci Lett. 2010, 484 (2): 139-142. 10.1016/j.neulet.2010.08.036.CrossRefPubMed Lu C, Li J, Sun W, Feng L, Li L, Liu A, Mao W, Wei H, Gao L, Zhang X, et al: Elevated plasma S100B concentration is associated with mesial temporal lobe epilepsy in Han Chinese: a case-control study. Neurosci Lett. 2010, 484 (2): 139-142. 10.1016/j.neulet.2010.08.036.CrossRefPubMed
13.
go back to reference Griffin WS, Yeralan O, Sheng JG, Boop FA, Mrak RE, Rovnaghi CR, Burnett BA, Feoktistova A, Van Eldik LJ: Overexpression of the neurotrophic cytokine S100 beta in human temporal lobe epilepsy. J Neurochem. 1995, 65 (1): 228-233.CrossRefPubMedPubMedCentral Griffin WS, Yeralan O, Sheng JG, Boop FA, Mrak RE, Rovnaghi CR, Burnett BA, Feoktistova A, Van Eldik LJ: Overexpression of the neurotrophic cytokine S100 beta in human temporal lobe epilepsy. J Neurochem. 1995, 65 (1): 228-233.CrossRefPubMedPubMedCentral
14.
go back to reference Palmio J, Keranen T, Alapirtti T, Hulkkonen J, Makinen R, Holm P, Suhonen J, Peltola J: Elevated serum neuron-specific enolase in patients with temporal lobe epilepsy: a video-EEG study. Epilepsy Res. 2008, 81 (2-3): 155-160. 10.1016/j.eplepsyres.2008.05.006.CrossRefPubMed Palmio J, Keranen T, Alapirtti T, Hulkkonen J, Makinen R, Holm P, Suhonen J, Peltola J: Elevated serum neuron-specific enolase in patients with temporal lobe epilepsy: a video-EEG study. Epilepsy Res. 2008, 81 (2-3): 155-160. 10.1016/j.eplepsyres.2008.05.006.CrossRefPubMed
15.
go back to reference Hashimoto K, Watanabe K, Nishimura T, Iyo M, Shirayama Y, Minabe Y: Behavioral changes and expression of heat shock protein hsp-70 mRNA, brain-derived neurotrophic factor mRNA, and cyclooxygenase-2 mRNA in rat brain following seizures induced by systemic administration of kainic acid. Brain Res. 1998, 804 (2): 212-223. 10.1016/S0006-8993(98)00708-2.CrossRefPubMed Hashimoto K, Watanabe K, Nishimura T, Iyo M, Shirayama Y, Minabe Y: Behavioral changes and expression of heat shock protein hsp-70 mRNA, brain-derived neurotrophic factor mRNA, and cyclooxygenase-2 mRNA in rat brain following seizures induced by systemic administration of kainic acid. Brain Res. 1998, 804 (2): 212-223. 10.1016/S0006-8993(98)00708-2.CrossRefPubMed
16.
go back to reference Ryufuku M, Toyoshima Y, Kitaura H, Zheng Y, Fu YJ, Miyahara H, Murakami H, Masuda H, Kameyama S, Takahashi H, et al: Hypertrophy of hippocampal end folium neurons in patients with mesial temporal lobe epilepsy. Neuropathology. 2011, 31 (5): 476-485. 10.1111/j.1440-1789.2010.01191.x.CrossRefPubMed Ryufuku M, Toyoshima Y, Kitaura H, Zheng Y, Fu YJ, Miyahara H, Murakami H, Masuda H, Kameyama S, Takahashi H, et al: Hypertrophy of hippocampal end folium neurons in patients with mesial temporal lobe epilepsy. Neuropathology. 2011, 31 (5): 476-485. 10.1111/j.1440-1789.2010.01191.x.CrossRefPubMed
17.
go back to reference Yang T, Hsu C, Liao W, Chuang JS: Heat shock protein 70 expression in epilepsy suggests stress rather than protection. Acta Neuropathol. 2008, 115 (2): 219-230. 10.1007/s00401-007-0297-3.CrossRefPubMed Yang T, Hsu C, Liao W, Chuang JS: Heat shock protein 70 expression in epilepsy suggests stress rather than protection. Acta Neuropathol. 2008, 115 (2): 219-230. 10.1007/s00401-007-0297-3.CrossRefPubMed
18.
go back to reference Tsai NW, Lin TK, Chen SD, Chang WN, Wang HC, Yang TM, Lin YJ, Jan CR, Huang CR, Liou CW, et al: The value of serial plasma nuclear and mitochondrial DNA levels in patients with acute ischemic stroke. Clin Chim Acta. 2011, 412 (5-6): 476-479. 10.1016/j.cca.2010.11.036.CrossRefPubMed Tsai NW, Lin TK, Chen SD, Chang WN, Wang HC, Yang TM, Lin YJ, Jan CR, Huang CR, Liou CW, et al: The value of serial plasma nuclear and mitochondrial DNA levels in patients with acute ischemic stroke. Clin Chim Acta. 2011, 412 (5-6): 476-479. 10.1016/j.cca.2010.11.036.CrossRefPubMed
19.
go back to reference Lu CH, Chang WN, Tsai NW, Chuang YC, Huang CR, Wang HC: The value of serial plasma nuclear and mitochondrial DNA levels in adult community-acquired bacterial meningitis. QJM. 2010, 103 (3): 169-175. 10.1093/qjmed/hcp201.CrossRefPubMed Lu CH, Chang WN, Tsai NW, Chuang YC, Huang CR, Wang HC: The value of serial plasma nuclear and mitochondrial DNA levels in adult community-acquired bacterial meningitis. QJM. 2010, 103 (3): 169-175. 10.1093/qjmed/hcp201.CrossRefPubMed
20.
go back to reference Pitkanen A, Sutula TP: Is epilepsy a progressive disorder? Prospects for new therapeutic approaches in temporal-lobe epilepsy. Lancet Neurol. 2002, 1 (3): 173-181. 10.1016/S1474-4422(02)00073-X.CrossRefPubMed Pitkanen A, Sutula TP: Is epilepsy a progressive disorder? Prospects for new therapeutic approaches in temporal-lobe epilepsy. Lancet Neurol. 2002, 1 (3): 173-181. 10.1016/S1474-4422(02)00073-X.CrossRefPubMed
21.
go back to reference Andersson-Roswall L, Engman E, Samuelsson H, Malmgren K: Cognitive outcome 10 years after temporal lobe epilepsy surgery: a prospective controlled study. Neurol. 2010, 74 (24): 1977-1985. 10.1212/WNL.0b013e3181e39684.CrossRef Andersson-Roswall L, Engman E, Samuelsson H, Malmgren K: Cognitive outcome 10 years after temporal lobe epilepsy surgery: a prospective controlled study. Neurol. 2010, 74 (24): 1977-1985. 10.1212/WNL.0b013e3181e39684.CrossRef
22.
go back to reference Baxendale S, Heaney D, Thompson PJ, Duncan JS: Cognitive consequences of childhood-onset temporal lobe epilepsy across the adult lifespan. Neurol. 2010, 75 (8): 705-711. 10.1212/WNL.0b013e3181eee3f0.CrossRef Baxendale S, Heaney D, Thompson PJ, Duncan JS: Cognitive consequences of childhood-onset temporal lobe epilepsy across the adult lifespan. Neurol. 2010, 75 (8): 705-711. 10.1212/WNL.0b013e3181eee3f0.CrossRef
23.
go back to reference Keller SS, Roberts N: Voxel-based morphometry of temporal lobe epilepsy: an introduction and review of the literature. Epilepsia. 2008, 49 (5): 741-757. 10.1111/j.1528-1167.2007.01485.x.CrossRefPubMed Keller SS, Roberts N: Voxel-based morphometry of temporal lobe epilepsy: an introduction and review of the literature. Epilepsia. 2008, 49 (5): 741-757. 10.1111/j.1528-1167.2007.01485.x.CrossRefPubMed
24.
go back to reference Yang T, Zhou D, Stefan H: Why mesial temporal lobe epilepsy with hippocampal sclerosis is progressive: uncontrolled inflammation drives disease progression?. J Neurol Sci. 2010, 296 (1-2): 1-6. 10.1016/j.jns.2010.06.002.CrossRefPubMed Yang T, Zhou D, Stefan H: Why mesial temporal lobe epilepsy with hippocampal sclerosis is progressive: uncontrolled inflammation drives disease progression?. J Neurol Sci. 2010, 296 (1-2): 1-6. 10.1016/j.jns.2010.06.002.CrossRefPubMed
25.
go back to reference Tan TY, Lu CH, Chuang HY, Lin TK, Liou CW, Chang WN, Chuang YC: Long-term antiepileptic drug therapy contributes to the acceleration of atherosclerosis. Epilepsia. 2009, 50 (6): 1579-1586. 10.1111/j.1528-1167.2009.02024.x.CrossRefPubMed Tan TY, Lu CH, Chuang HY, Lin TK, Liou CW, Chang WN, Chuang YC: Long-term antiepileptic drug therapy contributes to the acceleration of atherosclerosis. Epilepsia. 2009, 50 (6): 1579-1586. 10.1111/j.1528-1167.2009.02024.x.CrossRefPubMed
26.
go back to reference Lo YM, Tein MS, Lau TK, Haines CJ, Leung TN, Poon PM, Wainscoat JS, Johnson PJ, Chang AM, Hjelm NM: Quantitative analysis of fetal DNA in maternal plasma and serum: implications for noninvasive prenatal diagnosis. Am J Hum Genet. 1998, 62 (4): 768-775. 10.1086/301800.CrossRefPubMedPubMedCentral Lo YM, Tein MS, Lau TK, Haines CJ, Leung TN, Poon PM, Wainscoat JS, Johnson PJ, Chang AM, Hjelm NM: Quantitative analysis of fetal DNA in maternal plasma and serum: implications for noninvasive prenatal diagnosis. Am J Hum Genet. 1998, 62 (4): 768-775. 10.1086/301800.CrossRefPubMedPubMedCentral
27.
go back to reference Chiu RW, Chan LY, Lam NY, Tsui NB, Ng EK, Rainer TH, Lo YM: Quantitative analysis of circulating mitochondrial DNA in plasma. Clin Chem. 2003, 49 (5): 719-726. 10.1373/49.5.719.CrossRefPubMed Chiu RW, Chan LY, Lam NY, Tsui NB, Ng EK, Rainer TH, Lo YM: Quantitative analysis of circulating mitochondrial DNA in plasma. Clin Chem. 2003, 49 (5): 719-726. 10.1373/49.5.719.CrossRefPubMed
28.
29.
go back to reference Chang CC, Chang WN, Lui CC, Wang JJ, Chen CF, Lee YC, Chen SS, Lin YT, Huang CW, Chen C: Longitudinal study of carbon monoxide intoxication by diffusion tensor imaging with neuropsychiatric correlation. J Psychiatry Neurosci. 2010, 35 (2): 115-125. 10.1503/jpn.090057.CrossRefPubMedPubMedCentral Chang CC, Chang WN, Lui CC, Wang JJ, Chen CF, Lee YC, Chen SS, Lin YT, Huang CW, Chen C: Longitudinal study of carbon monoxide intoxication by diffusion tensor imaging with neuropsychiatric correlation. J Psychiatry Neurosci. 2010, 35 (2): 115-125. 10.1503/jpn.090057.CrossRefPubMedPubMedCentral
30.
go back to reference Chang CC, Chang YY, Chang WN, Lee YC, Wang YL, Lui CC, Huang CW, Liu WL: Cognitive deficits in multiple system atrophy correlate with frontal atrophy and disease duration. Eur J Neurol. 2009, 16 (10): 1144-1150. 10.1111/j.1468-1331.2009.02661.x.CrossRefPubMed Chang CC, Chang YY, Chang WN, Lee YC, Wang YL, Lui CC, Huang CW, Liu WL: Cognitive deficits in multiple system atrophy correlate with frontal atrophy and disease duration. Eur J Neurol. 2009, 16 (10): 1144-1150. 10.1111/j.1468-1331.2009.02661.x.CrossRefPubMed
31.
go back to reference Chang CC, Lee YC, Chang WN, Chen SS, Lui CC, Chang HW, Liu WL, Wang YL: Damage of white matter tract correlated with neuropsychological deficits in carbon monoxide intoxication after hyperbaric oxygen therapy. J Neurotrauma. 2009, 26 (8): 1263-1270. 10.1089/neu.2008.0619.CrossRefPubMed Chang CC, Lee YC, Chang WN, Chen SS, Lui CC, Chang HW, Liu WL, Wang YL: Damage of white matter tract correlated with neuropsychological deficits in carbon monoxide intoxication after hyperbaric oxygen therapy. J Neurotrauma. 2009, 26 (8): 1263-1270. 10.1089/neu.2008.0619.CrossRefPubMed
32.
go back to reference Chang CC, Kramer JH, Lin KN, Chang WN, Wang YL, Huang CW, Lin YT, Chen C, Wang PN: Validating the Chinese version of the Verbal Learning Test for screening Alzheimer's disease. J Int Neuropsychol Soc. 2010, 16 (2): 244-251. 10.1017/S1355617709991184.CrossRefPubMed Chang CC, Kramer JH, Lin KN, Chang WN, Wang YL, Huang CW, Lin YT, Chen C, Wang PN: Validating the Chinese version of the Verbal Learning Test for screening Alzheimer's disease. J Int Neuropsychol Soc. 2010, 16 (2): 244-251. 10.1017/S1355617709991184.CrossRefPubMed
33.
go back to reference Ashburner J, Friston KJ: Voxel-based morphometry-the methods. NeuroImage. 2000, 11 (6 Pt 1): 805-821.CrossRefPubMed Ashburner J, Friston KJ: Voxel-based morphometry-the methods. NeuroImage. 2000, 11 (6 Pt 1): 805-821.CrossRefPubMed
34.
go back to reference Lanneau D, Wettstein G, Bonniaud P, Garrido C: Heat shock proteins: cell protection through protein triage. ScientificWorldJournal. 2010, 10: 1543-1552.CrossRefPubMed Lanneau D, Wettstein G, Bonniaud P, Garrido C: Heat shock proteins: cell protection through protein triage. ScientificWorldJournal. 2010, 10: 1543-1552.CrossRefPubMed
35.
go back to reference Ayala GX, Tapia R: HSP70 expression protects against hippocampal neurodegeneration induced by endogenous glutamate in vivo. Neuropharmacol. 2008, 55 (8): 1383-1390. 10.1016/j.neuropharm.2008.08.035.CrossRef Ayala GX, Tapia R: HSP70 expression protects against hippocampal neurodegeneration induced by endogenous glutamate in vivo. Neuropharmacol. 2008, 55 (8): 1383-1390. 10.1016/j.neuropharm.2008.08.035.CrossRef
37.
go back to reference Pham N, Fazio V, Cucullo L, Teng Q, Biberthaler P, Bazarian JJ, Janigro D: Extracranial sources of S100B do not affect serum levels. PLoS One. 2010, 5 (9): e12691. doi:10.1371/journal.pone.0012691 Pham N, Fazio V, Cucullo L, Teng Q, Biberthaler P, Bazarian JJ, Janigro D: Extracranial sources of S100B do not affect serum levels. PLoS One. 2010, 5 (9): e12691. doi:10.1371/journal.pone.0012691
38.
go back to reference Steinhoff BJ, Tumani H, Otto M, Mursch K, Wiltfang J, Herrendorf G, Bittermann HJ, Felgenhauer K, Paulus W, Markakis E: Cisternal S100 protein and neuron-specific enolase are elevated and site-specific markers in intractable temporal lobe epilepsy. Epilepsy Res. 1999, 36 (1): 75-82. 10.1016/S0920-1211(99)00026-1.CrossRefPubMed Steinhoff BJ, Tumani H, Otto M, Mursch K, Wiltfang J, Herrendorf G, Bittermann HJ, Felgenhauer K, Paulus W, Markakis E: Cisternal S100 protein and neuron-specific enolase are elevated and site-specific markers in intractable temporal lobe epilepsy. Epilepsy Res. 1999, 36 (1): 75-82. 10.1016/S0920-1211(99)00026-1.CrossRefPubMed
39.
go back to reference Kleindienst A, Meissner S, Eyupoglu IY, Parsch H, Schmidt C, Buchfelder M: Dynamics of S100B release into serum and cerebrospinal fluid following acute brain injury. Acta Neurochir Suppl. 2010, 106: 247-250. 10.1007/978-3-211-98811-4_46.CrossRefPubMed Kleindienst A, Meissner S, Eyupoglu IY, Parsch H, Schmidt C, Buchfelder M: Dynamics of S100B release into serum and cerebrospinal fluid following acute brain injury. Acta Neurochir Suppl. 2010, 106: 247-250. 10.1007/978-3-211-98811-4_46.CrossRefPubMed
40.
go back to reference Leutmezer F, Wagner O, Baumgartner C: Serum s-100 protein is not a suitable seizure marker in temporal lobe epilepsy. Epilepsia. 2002, 43 (10): 1172-1174. 10.1046/j.1528-1157.2002.50101.x.CrossRefPubMed Leutmezer F, Wagner O, Baumgartner C: Serum s-100 protein is not a suitable seizure marker in temporal lobe epilepsy. Epilepsia. 2002, 43 (10): 1172-1174. 10.1046/j.1528-1157.2002.50101.x.CrossRefPubMed
41.
go back to reference Palmio J, Peltola J, Vuorinen P, Laine S, Suhonen J, Keranen T: Normal CSF neuron-specific enolase and S-100 protein levels in patients with recent non-complicated tonic-clonic seizures. J Neurol Sci. 2001, 183 (1): 27-31. 10.1016/S0022-510X(00)00478-0.CrossRefPubMed Palmio J, Peltola J, Vuorinen P, Laine S, Suhonen J, Keranen T: Normal CSF neuron-specific enolase and S-100 protein levels in patients with recent non-complicated tonic-clonic seizures. J Neurol Sci. 2001, 183 (1): 27-31. 10.1016/S0022-510X(00)00478-0.CrossRefPubMed
42.
go back to reference Fournie GJ, Martres F, Pourrat JP, Alary C, Rumeau M: Plasma DNA as cell death marker in elderly patients. Gerontol. 1993, 39 (4): 215-221. 10.1159/000213536.CrossRef Fournie GJ, Martres F, Pourrat JP, Alary C, Rumeau M: Plasma DNA as cell death marker in elderly patients. Gerontol. 1993, 39 (4): 215-221. 10.1159/000213536.CrossRef
Metadata
Title
Clinical significance of serological biomarkers and neuropsychological performances in patients with temporal lobe epilepsy
Authors
Chiung-Chih Chang
Chun-Chung Lui
Chen-Chang Lee
Shang-Der Chen
Wen-Neng Chang
Cheng-Hsien Lu
Nai-Ching Chen
Alice Y W Chang
Samuel H H Chan
Yao-Chung Chuang
Publication date
01-12-2012
Publisher
BioMed Central
Published in
BMC Neurology / Issue 1/2012
Electronic ISSN: 1471-2377
DOI
https://doi.org/10.1186/1471-2377-12-15

Other articles of this Issue 1/2012

BMC Neurology 1/2012 Go to the issue