Closed-loop Neuropharmacology for Epilepsy: Distant Dream or Future Reality?

Author(s): Irene Aicua-Rapun*, Pascal André, Jan Novy.

Journal Name: Current Neuropharmacology

Volume 17 , Issue 5 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Epilepsy is considered the most frequent severe neurological condition but most patients treated with medication become seizure free. The management of treatment, however, is highly empirical, mainly relying on observation. A closed-loop therapy for epilepsy would be very valuable for more efficient treatment regimens. Here we discuss monitoring treatment (therapeutic drug monitoring) and the potential developments in this field, as well as providing a review of potential biomarkers that could be used to monitor the disease activity. Finally, we consider the pharmacogenetic input in epilepsy treatment.

Keywords: Biomarkers in epilepsy, therapeutic drug monitoring, pharmacogenetics, cytokines, genetic factors, refractory epilepsy, hormones.

[1]
Fisher, R.S.; Acevedo, C.; Arzimanoglou, A.; Bogacz, A.; Cross, J.H.; Elger, C.E.; Engel, J., Jr; Forsgren, L.; French, J.A.; Glynn, M.; Hesdorffer, D.C.; Lee, B.I.; Mathern, G.W.; Moshé, S.L.; Perucca, E.; Scheffer, I.E.; Tomson, T.; Watanabe, M.; Wiebe, S. ILAE official report: a practical clinical definition of epilepsy. Epilepsia, 2014, 55(4), 475-482. [http://dx.doi.org/10.1111/epi.12550]. [PMID: 24730690].
[2]
Hesdorffer, D.C.; Logroscino, G.; Benn, E.K.; Katri, N.; Cascino, G.; Hauser, W.A. Estimating risk for developing epilepsy: a population-based study in Rochester, Minnesota. Neurology, 2011, 76(1), 23-27. [http://dx.doi.org/10.1212/WNL.0b013e318204a36a]. [PMID: 21205691].
[3]
Novy, J.; Belluzzo, M.; Caboclo, L.O.; Catarino, C.B.; Yogarajah, M.; Martinian, L.; Peacock, J.L.; Bell, G.S.; Koepp, M.J.; Thom, M.; Sander, J.W.; Sisodiya, S.M. The lifelong course of chronic epilepsy: The Chalfont experience. Brain, 2013, 136(Pt 10), 3187-3199. [http://dx.doi.org/10.1093/brain/awt117]. [PMID: 23824485].
[4]
Lhatoo, S.D.; Sander, J.W.; Shorvon, S.D. The dynamics of drug treatment in epilepsy: an observational study in an unselected population based cohort with newly diagnosed epilepsy followed up prospectively over 11-14 years. J. Neurol. Neurosurg. Psychiatry, 2001, 71(5), 632-637. [http://dx.doi.org/10.1136/jnnp.71.5.632]. [PMID: 11606675].
[5]
Kwan, P.; Brodie, M.J. Early identification of refractory epilepsy. N. Engl. J. Med., 2000, 342(5), 314-319. [http://dx.doi.org/10.1056/NEJM200002033420503]. [PMID: 10660394].
[6]
Picot, M.C.; Baldy-Moulinier, M.; Daurès, J.P.; Dujols, P.; Crespel, A. The prevalence of epilepsy and pharmacoresistant epilepsy in adults: a population-based study in a Western European country. Epilepsia, 2008, 49(7), 1230-1238. [http://dx.doi.org/10.1111/j.1528-1167.2008.01579.x]. [PMID: 18363709].
[7]
Schiller, Y.; Najjar, Y. Quantifying the response to antiepileptic drugs: effect of past treatment history. Neurology, 2008, 70(1), 54-65. [http://dx.doi.org/10.1212/01.wnl.0000286959.22040.6e]. [PMID: 18166707].
[8]
Löscher, W.; Schmidt, D. Modern antiepileptic drug development has failed to deliver: ways out of the current dilemma. Epilepsia, 2011, 52(4), 657-678. [http://dx.doi.org/10.1111/j.1528-1167.2011.03024.x]. [PMID: 21426333].
[9]
Shafer, S.Q.; Hauser, W.A.; Annegers, J.F.; Klass, D.W. EEG and other early predictors of epilepsy remission: a community study. Epilepsia, 1988, 29(5), 590-600. [http://dx.doi.org/10.1111/j.1528-1157.1988.tb03767.x]. [PMID: 3409845].
[10]
Gatzonis, S.; Triantafyllou, N.; Kateri, M.; Siatouni, A.; Angelopoulos, E.; Kimiskidis, V.K. The prognostic value of electroencephalography in epilepsy: a long-term follow-up study. Neurol. Int., 2010, 2(2), e18. [http://dx.doi.org/10.4081/ni.2010.e18]. [PMID: 21577332].
[11]
Johannessen, S.I.; Battino, D.; Berry, D.J.; Bialer, M.; Krämer, G.; Tomson, T.; Patsalos, P.N. Therapeutic drug monitoring of the newer antiepileptic drugs. Ther. Drug Monit., 2003, 25(3), 347-363. [http://dx.doi.org/10.1097/00007691-200306000-00016]. [PMID: 12766564].
[12]
Nicholas, J.M.; Ridsdale, L.; Richardson, M.P.; Ashworth, M.; Gulliford, M.C. Trends in antiepileptic drug utilisation in UK primary care 1993-2008: cohort study using the General Practice Research Database. Seizure, 2012, 21(6), 466-470. [http://dx.doi.org/10.1016/j.seizure.2012.04.014]. [PMID: 22608976].
[13]
Naik, G.S.; Kodagali, R.; Mathew, B.S.; Thomas, M.; Prabha, R.; Mathew, V.; Fleming, D.H. Therapeutic drug monitoring of levetiracetam and lamotrigine: Is there a need? Ther. Drug Monit., 2014, 37(4), 437-444. [PMID: 25478905].
[14]
Westin, A.A.; Nakken, K.O.; Johannessen, S.I.; Reimers, A.; Lillestølen, K.M.; Brodtkorb, E. Serum concentration/dose ratio of topiramate during pregnancy. Epilepsia, 2009, 50(3), 480-485. [http://dx.doi.org/10.1111/j.1528-1167.2008.01776.x]. [PMID: 19178558].
[15]
Wegner, I.; Edelbroek, P.; de Haan, G.J.; Lindhout, D.; Sander, J.W. Drug monitoring of lamotrigine and oxcarbazepine combination during pregnancy. Epilepsia, 2010, 51(12), 2500-2502. [http://dx.doi.org/10.1111/j.1528-1167.2010.02771.x]. [PMID: 21204816].
[16]
McCormack, M.; Alfirevic, A.; Bourgeois, S.; Farrell, J.J.; Kasperavičiūtė, D.; Carrington, M.; Sills, G.J.; Marson, T.; Jia, X.; de Bakker, P.I.; Chinthapalli, K.; Molokhia, M.; Johnson, M.R.; O’Connor, G.D.; Chaila, E.; Alhusaini, S.; Shianna, K.V.; Radtke, R.A.; Heinzen, E.L.; Walley, N.; Pandolfo, M.; Pichler, W.; Park, B.K.; Depondt, C.; Sisodiya, S.M.; Goldstein, D.B.; Deloukas, P.; Delanty, N.; Cavalleri, G.L.; Pirmohamed, M. HLA-A*3101 and carbamazepine-induced hypersensitivity reactions in Europeans. N. Engl. J. Med., 2011, 364(12), 1134-1143. [http://dx.doi.org/10.1056/NEJMoa1013297]. [PMID: 21428769].
[17]
Chung, W.H.; Hung, S.I.; Hong, H.S.; Hsih, M.S.; Yang, L.C.; Ho, H.C.; Wu, J.Y.; Chen, Y.T. Medical genetics: a marker for Stevens-Johnson syndrome. Nature, 2004, 428(6982), 486. [http://dx.doi.org/10.1038/428486a]. [PMID: 15057820].
[18]
Hoppe, C.; Poepel, A.; Elger, C.E. Epilepsy: accuracy of patient seizure counts. Arch. Neurol., 2007, 64(11), 1595-1599. [http://dx.doi.org/10.1001/archneur.64.11.1595]. [PMID: 17998441].
[19]
Poochikian-Sarkissian, S.; Tai, P.; del Campo, M.; Andrade, D.M.; Carlen, P.L.; Valiante, T.; Wennberg, R.A. Patient awareness of seizures as documented in the epilepsy monitoring unit. Can. J. Neurosci. Nurs., 2009, 31(4), 22-23. [PMID: 20085117].
[20]
Spilker, B.; Segreti, A. Validation of the phenomenon of regression of seizure frequency in epilepsy. Epilepsia, 1984, 25(4), 443-449. [http://dx.doi.org/10.1111/j.1528-1157.1984.tb03441.x]. [PMID: 6378614].
[21]
Spilker, B.; Bruni, J.; Jones, M.; Upton, A.; Cato, A.; Cloutier, G. A double-blind crossover study of cinromide versus placebo in epileptic outpatients with partial seizures. Epilepsia, 1983, 24(4), 410-421. [http://dx.doi.org/10.1111/j.1528-1157.1983.tb04909.x]. [PMID: 6409599].
[22]
Novy, J.; Bartolini, E.; Bell, G.S.; Duncan, J.S.; Sander, J.W. Long-term retention of lacosamide in a large cohort of people with medically refractory epilepsy: a single centre evaluation. Epilepsy Res., 2013, 106(1-2), 250-256. [http://dx.doi.org/10.1016/j.eplepsyres.2013.05.002]. [PMID: 23796862].
[23]
Sander, J.W. New antiepileptic drugs in practice--how do they perform in the real world? Acta Neurol. Scand. Suppl., 2005, 181, 26-29. [http://dx.doi.org/10.1111/j.1600-0404.2005.00505.x]. [PMID: 16238705].
[24]
Hanley, J.A. L.-H. If nothing goes wrong, is everything alright? JAMA, 1983, 259, 1743-1745. [http://dx.doi.org/10.1001/jama.1983.03330370053031]. [PMID: 6827763].
[25]
Kwan, P.; Arzimanoglou, A.; Berg, A.T.; Brodie, M.J.; Allen, H.W.; Mathern, G.; Moshé, S.L.; Perucca, E.; Wiebe, S.; French, J. Definition of drug resistant epilepsy: consensus proposal by the ad hoc task force of the ILAE commission on therapeutic strategies. Epilepsia, 2010, 51(6), 1069-1077. [http://dx.doi.org/10.1111/j.1528-1167.2009.02397.x]. [PMID: 19889013].
[26]
Westover, M.B.; Cormier, J.; Bianchi, M.T.; Shafi, M.; Kilbride, R.; Cole, A.J.; Cash, S.S. Revising the “Rule of Three” for inferring seizure freedom. Epilepsia, 2012, 53(2), 368-376. [http://dx.doi.org/10.1111/j.1528-1167.2011.03355.x]. [PMID: 22191711].
[27]
Sillanpää, M.; Anttinen, A.; Rinne, J.O.; Joutsa, J.; Sonninen, P.; Erkinjuntti, M.; Hermann, B.; Karrasch, M.; Saarinen, M.; Tiitta, P.; Shinnar, S. Childhood-onset epilepsy five decades later. A prospective population-based cohort study. Epilepsia, 2015, 56(11), 1774-1783. [http://dx.doi.org/10.1111/epi.13187]. [PMID: 26434398].
[28]
Sillanpää, M.; Schmidt, D. Epilepsy: long-term rates of childhood-onset epilepsy remission confirmed. Nat. Rev. Neurol., 2015, 11(3), 130-131. [http://dx.doi.org/10.1038/nrneurol.2014.262]. [PMID: 25623788].
[29]
Neligan, A.; Bell, G.S.; Sander, J.W.; Shorvon, S.D. How refractory is refractory epilepsy? Patterns of relapse and remission in people with refractory epilepsy. Epilepsy Res., 2011, 96(3), 225-230. [http://dx.doi.org/10.1016/j.eplepsyres.2011.06.004]. [PMID: 21724372].
[30]
Wang, S.P.; Mintzer, S.; Skidmore, C.T.; Zhan, T.; Stuckert, E.; Nei, M.; Sperling, M.R. Seizure recurrence and remission after switching antiepileptic drugs. Epilepsia, 2013, 54(1), 187-193. [http://dx.doi.org/10.1111/j.1528-1167.2012.03652.x]. [PMID: 22931161].
[31]
Ortibus, E.L.; Sum, J.M.; Hahn, J.S. Predictive value of EEG for outcome and epilepsy following neonatal seizures. Electroencephalogr. Clin. Neurophysiol., 1996, 98(3), 175-185. [http://dx.doi.org/10.1016/0013-4694(95)00245-6]. [PMID: 8631277].
[32]
Kuturec, M.; Emoto, S.E.; Sofijanov, N.; Dukovski, M.; Duma, F.; Ellenberg, J.H.; Hirtz, D.G.; Nelson, K.B. Febrile seizures: is the EEG a useful predictor of recurrences? Clin. Pediatr. (Phila.), 1997, 36(1), 31-36. [http://dx.doi.org/10.1177/000992289703600105]. [PMID: 9007345].
[33]
Badawy, R.A.; Strigaro, G.; Cantello, R. TMS, cortical excitability and epilepsy: the clinical impact. Epilepsy Res., 2014, 108(2), 153-161. [http://dx.doi.org/10.1016/j.eplepsyres.2013.11.014]. [PMID: 24315665].
[34]
Badawy, R.A.B.; Macdonell, R.A.L.; Berkovic, S.F.; Newton, M.R.; Jackson, G.D. Predicting seizure control: cortical excitability and antiepileptic medication. Ann. Neurol., 2010, 67(1), 64-73. [http://dx.doi.org/10.1002/ana.21806]. [PMID: 20186859].
[35]
Kimiskidis, V.K.; Tsimpiris, A.; Ryvlin, P.; Kalviainen, R.; Koutroumanidis, M.; Valentin, A.; Laskaris, N.; Kugiumtzis, D. TMS combined with EEG in genetic generalized epilepsy: A phase II diagnostic accuracy study. Clin. Neurophysiol., 2017, 128(2), 367-381.
[36]
Shafi, M.M.; Vernet, M.; Klooster, D.; Chu, C.J.; Boric, K.; Barnard, M.E.; Romatoski, K.; Westover, M.B.; Christodoulou, J.A.; Gabrieli, J.D.; Whitfield-Gabrieli, S.; Pascual-Leone, A.; Chang, B.S. Physiological consequences of abnormal connectivity in a developmental epilepsy. Ann. Neurol., 2015, 77(3), 487-503. [http://dx.doi.org/10.1002/ana.24343]. [PMID: 25858773].
[37]
Bauer, P.R.; Kalitzin, S.; Zijlmans, M.; Sander, J.W.; Visser, G.H. Cortical excitability as a potential clinical marker of epilepsy: a review of the clinical application of transcranial magnetic stimulation. Int. J. Neural Syst., 2014, 24(2), 1430001. [http://dx.doi.org/10.1142/S0129065714300010]. [PMID: 24475894].
[38]
Badawy, R.A.B.; Macdonell, R.A.L.; Berkovic, S.F.; Vogrin, S.J.; Jackson, G.D.; Cook, M.J. Reply: Transcranial magnetic stimulation as a biomarker for epilepsy. Brain, 2017, 140(3), e19-e19. [http://dx.doi.org/10.1093/brain/aww346]. [PMID: 28364546].
[39]
Zijlmans, M.; Jiruska, P.; Zelmann, R.; Leijten, F.S.S.; Jefferys, J.G.R.; Gotman, J. High-frequency oscillations as a new biomarker in epilepsy. Ann. Neurol., 2012, 71(2), 169-178. [http://dx.doi.org/10.1002/ana.22548]. [PMID: 22367988].
[40]
Cendes, F.; Engel, J., Jr Extending applications for high-frequency oscillations: the ripple effect. Neurology, 2011, 77(6), 518-519. [http://dx.doi.org/10.1212/WNL.0b013e318228c16f]. [PMID: 21753164].
[41]
Goldenholz, D.M.; Seyal, M.; Bateman, L.M.; Gotman, J.; Andrade-Valenca, L.; Zelmann, R.; Dubeau, F. Interictal scalp fast oscillations as a marker of the seizure onset zone. Neurology, 2012, 78(3), 224-225. [http://dx.doi.org/10.1212/01.wnl.0000410956.29629.4d]. [PMID: 22249499].
[42]
Andrade-Valenca, L.P.; Dubeau, F.; Mari, F.; Zelmann, R.; Gotman, J. Interictal scalp fast oscillations as a marker of the seizure onset zone. Neurology, 2011, 77(6), 524-531. [http://dx.doi.org/10.1212/WNL.0b013e318228bee2]. [PMID: 21753167].
[43]
van Klink, N.E.; van ’t Klooster, M.A.; Leijten, F.S.; Jacobs, J.; Braun, K.P.; Zijlmans, M. Ripples on rolandic spikes: A marker of epilepsy severity. Epilepsia, 2016, 57(7), 1179-1189. [http://dx.doi.org/10.1111/epi.13423]. [PMID: 27270830].
[44]
van ’t Klooster, M.A.; van Klink, N.E.; Leijten, F.S.; Zelmann, R.; Gebbink, T.A.; Gosselaar, P.H.; Braun, K.P.; Huiskamp, G.J.; Zijlmans, M. Residual fast ripples in the intraoperative corticogram predict epilepsy surgery outcome. Neurology, 2015, 85(2), 120-128. [http://dx.doi.org/10.1212/WNL.0000000000001727]. [PMID: 26070338].
[45]
Glötzner, F.L.; Planner, M.; Gaab, M. Creatine kinase in serum after grand mal seizures. Eur. Neurol., 1979, 18(6), 399-404. [http://dx.doi.org/10.1159/000115112]. [PMID: 121079].
[46]
Lipka, K.; Bülow, H.H. Lactic acidosis following convulsions. Acta Anaesthesiol. Scand., 2003, 47(5), 616-618. [http://dx.doi.org/10.1034/j.1399-6576.2003.00115.x]. [PMID: 12699523].
[47]
Nevalainen, O.; Auvinen, A.; Ansakorpi, H.; Raitanen, J.; Isojärvi, J. Autoimmunity-related immunological serum markers and survival in a tertiary care cohort of adult patients with epilepsy. Epilepsy Res., 2014, 108(9), 1675-1679. [http://dx.doi.org/10.1016/j.eplepsyres.2014.08.014]. [PMID: 25257831].
[48]
Li, G.; Bauer, S.; Nowak, M.; Norwood, B.; Tackenberg, B.; Rosenow, F.; Knake, S.; Oertel, W.H.; Hamer, H.M. Cytokines and epilepsy. Seizure, 2011, 20(3), 249-256. [http://dx.doi.org/10.1016/j.seizure.2010.12.005]. [PMID: 21216630].
[49]
de Vries, E.E.; van den Munckhof, B.; Braun, K.P.; van Royen-Kerkhof, A.; de Jager, W.; Jansen, F.E. Inflammatory mediators in human epilepsy: A systematic review and meta-analysis. Neurosci. Biobehav. Rev., 2016, 63, 177-190. [http://dx.doi.org/10.1016/j.neubiorev.2016.02.007]. [PMID: 26877106].
[50]
Wang, Y.; Wang, D.; Guo, D. Interictal cytokine levels were correlated to seizure severity of epileptic patients: a retrospective study on 1218 epileptic patients. J. Transl. Med., 2015, 13, 378. [http://dx.doi.org/10.1186/s12967-015-0742-3]. [PMID: 26626560].
[51]
Yu, N.; Di, Q.; Hu, Y.; Zhang, Y.F.; Su, L.Y.; Liu, X.H.; Li, L.C. A meta-analysis of pro-inflammatory cytokines in the plasma of epileptic patients with recent seizure. Neurosci. Lett., 2012, 514(1), 110-115. [http://dx.doi.org/10.1016/j.neulet.2012.02.070]. [PMID: 22402188].
[52]
Silveira, G.; de Oliveira, A.C.; Teixeira, A.L. Insights into inflammation and epilepsy from the basic and clinical sciences. J. Clin. Neurosci., 2012, 19(8), 1071-1075. [http://dx.doi.org/10.1016/j.jocn.2011.10.011]. [PMID: 22705131].
[53]
Lehtimäki, K.A.; Keränen, T.; Palmio, J.; Mäkinen, R.; Hurme, M.; Honkaniemi, J.; Peltola, J. Increased plasma levels of cytokines after seizures in localization-related epilepsy. Acta Neurol. Scand., 2007, 116(4), 226-230. [http://dx.doi.org/10.1111/j.1600-0404.2007.00882.x]. [PMID: 17824899].
[54]
Alapirtti, T.; Rinta, S.; Hulkkonen, J.; Mäkinen, R.; Keränen, T.; Peltola, J. Interleukin-6, interleukin-1 receptor antagonist and interleukin-1beta production in patients with focal epilepsy: A video-EEG study. J. Neurol. Sci., 2009, 280(1-2), 94-97. [http://dx.doi.org/10.1016/j.jns.2009.02.355]. [PMID: 19272615].
[55]
Uludag, I.F.; Duksal, T.; Tiftikcioglu, B.I.; Zorlu, Y.; Ozkaya, F.; Kirkali, G. IL-1β, IL-6 and IL1Ra levels in temporal lobe epilepsy. Seizure, 2015, 26, 22-25. [http://dx.doi.org/10.1016/j.seizure.2015.01.009]. [PMID: 25799897].
[56]
Bauer, S.; Cepok, S.; Todorova-Rudolph, A.; Nowak, M.; Köller, M.; Lorenz, R.; Oertel, W.H.; Rosenow, F.; Hemmer, B.; Hamer, H.M. Etiology and site of temporal lobe epilepsy influence postictal cytokine release. Epilepsy Res., 2009, 86(1), 82-88. [http://dx.doi.org/10.1016/j.eplepsyres.2009.05.009]. [PMID: 19520550].
[57]
Bauer, S. Köller, M.; Cepok, S.; Todorova-Rudolph, A.; Nowak, M.; Nockher, W.A.; Lorenz, R.; Tackenberg, B.; Oertel, W.H.; Rosenow, F.; Hemmer, B.; Hamer, H.M. NK and CD4+ T cell changes in blood after seizures in temporal lobe epilepsy. Exp. Neurol., 2008, 211(2), 370-377. [http://dx.doi.org/10.1016/j.expneurol.2008.01.017]. [PMID: 18387608].
[58]
Liimatainen, S.; Fallah, M.; Kharazmi, E.; Peltola, M.; Peltola, J. Interleukin-6 levels are increased in temporal lobe epilepsy but not in extra-temporal lobe epilepsy. J. Neurol., 2009, 256(5), 796-802. [http://dx.doi.org/10.1007/s00415-009-5021-x]. [PMID: 19252806].
[59]
Quirico-Santos, T.; Meira, I.D.; Gomes, A.C.; Pereira, V.C.; Pinto, M.; Monteiro, M.; Souza, J.M.; Alves-Leon, S.V. Resection of the epileptogenic lesion abolishes seizures and reduces inflammatory cytokines of patients with temporal lobe epilepsy. J. Neuroimmunol., 2013, 254(1-2), 125-130. [http://dx.doi.org/10.1016/j.jneuroim.2012.08.004]. [PMID: 23116880].
[60]
Cramer, J.A.; French, J. Quantitative assessment of seizure severity for clinical trials: a review of approaches to seizure components. Epilepsia, 2001, 42(1), 119-129. [http://dx.doi.org/10.1046/j.1528-1157.2001.19400.x]. [PMID: 11207795].
[61]
Mao, L.Y.; Ding, J.; Peng, W.F.; Ma, Y.; Zhang, Y.H.; Fan, W.; Wang, X. Interictal interleukin-17A levels are elevated and correlate with seizure severity of epilepsy patients. Epilepsia, 2013, 54(9), e142-e145. [http://dx.doi.org/10.1111/epi.12337]. [PMID: 23944193].
[62]
Alapirtti, T.; Waris, M.; Fallah, M.; Soilu-Hänninen, M.; Mäkinen, R.; Kharazmi, E.; Peltola, J. C-reactive protein and seizures in focal epilepsy: a video-electroencephalographic study. Epilepsia, 2012, 53(5), 790-796. [http://dx.doi.org/10.1111/j.1528-1167.2012.03449.x]. [PMID: 22462619].
[63]
Quigg, M.; Kiely, J.M.; Shneker, B.; Veldhuis, J.D.; Bertram, E.H., III Interictal and postictal alterations of pulsatile secretions of luteinizing hormone in temporal lobe epilepsy in men. Ann. Neurol., 2002, 51(5), 559-566. [http://dx.doi.org/10.1002/ana.10188]. [PMID: 12112101].
[64]
Herzog, A.G.; Coleman, A.E.; Jacobs, A.R.; Klein, P.; Friedman, M.N.; Drislane, F.W.; Ransil, B.J.; Schomer, D.L. Interictal EEG discharges, reproductive hormones, and menstrual disorders in epilepsy. Ann. Neurol., 2003, 54(5), 625-637. [http://dx.doi.org/10.1002/ana.10732]. [PMID: 14595652].
[65]
Smith, M.J.; Adams, L.F.; Schmidt, P.J.; Rubinow, D.R.; Wassermann, E.M. Effects of ovarian hormones on human cortical excitability. Ann. Neurol., 2002, 51(5), 599-603. [http://dx.doi.org/10.1002/ana.10180]. [PMID: 12112106].
[66]
Smith, M.J.; Keel, J.C.; Greenberg, B.D.; Adams, L.F.; Schmidt, P.J.; Rubinow, D.A.; Wassermann, E.M. Menstrual cycle effects on cortical excitability. Neurology, 1999, 53(9), 2069-2072. [http://dx.doi.org/10.1212/WNL.53.9.2069]. [PMID: 10599783].
[67]
Meierkord, H.; Shorvon, S.; Lightman, S.L. Plasma concentrations of prolactin, noradrenaline, vasopressin and oxytocin during and after a prolonged epileptic seizure. Acta Neurol. Scand., 1994, 90(2), 73-77. [http://dx.doi.org/10.1111/j.1600-0404.1994.tb02682.x]. [PMID: 7801741].
[68]
Ben-Menachem, E. Is prolactin a clinically useful measure of epilepsy? Epilepsy Curr., 2006, 6(3), 78-79. [http://dx.doi.org/10.1111/j.1535-7511.2006.00104.x]. [PMID: 16761067].
[69]
Stavropoulos, I.; Pervanidou, P.; Gnardellis, C.; Loli, N.; Theodorou, V.; Mantzou, A.; Soukou, F.; Sinani, O.; Chrousos, G.P. Increased hair cortisol and antecedent somatic complaints in children with a first epileptic seizure. Epilepsy Behav., 2017, 68, 146-152. [http://dx.doi.org/10.1016/j.yebeh.2016.12.015]. [PMID: 28189919].
[70]
van Campen, J.S.; Hompe, E.L.; Jansen, F.E.; Velis, D.N.; Otte, W.M.; van de Berg, F.; Braun, K.P.; Visser, G.H.; Sander, J.W.; Joels, M.; Zijlmans, M. Cortisol fluctuations relate to interictal epileptiform discharges in stress sensitive epilepsy. Brain, 2016, 139(Pt 6), 1673-1679. [http://dx.doi.org/10.1093/brain/aww071]. [PMID: 27036410].
[71]
van Campen, J.S.; Valentijn, F.A.; Jansen, F.E.; Joëls, M.; Braun, K.P. Seizure occurrence and the circadian rhythm of cortisol: a systematic review. Epilepsy Behav., 2015, 47, 132-137. [http://dx.doi.org/10.1016/j.yebeh.2015.04.071]. [PMID: 25982883].
[72]
Pennell, P.B. Hormonal aspects of epilepsy. Neurol. Clin., 2009, 27(4), 941-965. [http://dx.doi.org/10.1016/j.ncl.2009.08.005]. [PMID: 19853217].
[73]
Tomson, T.; Ericson, M.; Ihrman, C.; Lindblad, L.E. Heart rate variability in patients with epilepsy. Epilepsy Res., 1998, 30(1), 77-83. [http://dx.doi.org/10.1016/S0920-1211(97)00094-6]. [PMID: 9551847].
[74]
Ronkainen, E.; Ansakorpi, H.; Huikuri, H.V.; Myllylä, V.V.; Isojärvi, J.I.; Korpelainen, J.T. Suppressed circadian heart rate dynamics in temporal lobe epilepsy. J. Neurol. Neurosurg. Psychiatry, 2005, 76(10), 1382-1386. [http://dx.doi.org/10.1136/jnnp.2004.053777]. [PMID: 16170081].
[75]
Tomson, T.; Ericson, M.; Ihrman, C.; Lindblad, L.E. Heart rate variability in patients with epilepsy. Epilepsy Res., 1998, 30(1), 77-83. [http://dx.doi.org/10.1016/S0920-1211(97)00094-6]. [PMID: 9551847].
[76]
Mukherjee, S.; Tripathi, M.; Chandra, P.S.; Yadav, R.; Choudhary, N.; Sagar, R.; Bhore, R.; Pandey, R.M.; Deepak, K.K. Cardiovascular autonomic functions in well-controlled and intractable partial epilepsies. Epilepsy Res., 2009, 85(2-3), 261-269. [http://dx.doi.org/10.1016/j.eplepsyres.2009.03.021]. [PMID: 19409754].
[77]
Ansakorpi, H.; Korpelainen, J.T.; Huikuri, H.V.; Tolonen, U.; Myllylä, V.V.; Isojärvi, J.I. Heart rate dynamics in refractory and well controlled temporal lobe epilepsy. J. Neurol. Neurosurg. Psychiatry, 2002, 72(1), 26-30. [http://dx.doi.org/10.1136/jnnp.72.1.26]. [PMID: 11784820].
[78]
Ronkainen, E.; Ansakorpi, H.; Huikuri, H.V.; Myllylä, V.V.; Isojärvi, J.I.; Korpelainen, J.T. Suppressed circadian heart rate dynamics in temporal lobe epilepsy. J. Neurol. Neurosurg. Psychiatry, 2005, 76(10), 1382-1386. [http://dx.doi.org/10.1136/jnnp.2004.053777]. [PMID: 16170081].
[79]
Adams, J.E., III; Bodor, G.S.; Dávila-Román, V.G.; Delmez, J.A.; Apple, F.S.; Ladenson, J.H.; Jaffe, A.S. Cardiac troponin I. A marker with high specificity for cardiac injury. Circulation, 1993, 88(1), 101-106. [http://dx.doi.org/10.1161/01.CIR.88.1.101]. [PMID: 8319322].
[80]
Woodruff, B.K.; Britton, J.W.; Tigaran, S.; Cascino, G.D.; Burritt, M.F.; McConnell, J.P.; Ravkilde, J.; Molgaard, H.; Andreasen, F.; Dam, M.; Jaffe, A.S. Cardiac troponin levels following monitored epileptic seizures. Neurology, 2003, 60(10), 1690-1692. [http://dx.doi.org/10.1212/01.WNL.0000065881.46964.4F]. [PMID: 12771269].
[81]
Eskandarian, R.; Asghari, N.; Darban, M.; Ghorbani, R. Cardiac troponin levels following complicated and uncomplicated epileptic seizures. Arch. Med. Res., 2011, 42(6), 439-442. [http://dx.doi.org/10.1016/j.arcmed.2011.09.002]. [PMID: 21925221].
[82]
Sieweke, N.; Allendörfer, J.; Franzen, W.; Feustel, A.; Reichenberger, F.; Pabst, W.; Krämer, H.H.; Kaps, M.; Tanislav, C. Cardiac troponin I elevation after epileptic seizure. BMC Neurol., 2012, 12(1), 58. [http://dx.doi.org/10.1186/1471-2377-12-58]. [PMID: 22804867].
[83]
Kan, A.A.; van Erp, S.; Derijck, A.A.; de Wit, M.; Hessel, E.V.; O’Duibhir, E.; de Jager, W.; Van Rijen, P.C.; Gosselaar, P.H.; de Graan, P.N.; Pasterkamp, R.J. Genome-wide microRNA profiling of human temporal lobe epilepsy identifies modulators of the immune response. Cell. Mol. Life Sci., 2012, 69(18), 3127-3145. [http://dx.doi.org/10.1007/s00018-012-0992-7]. [PMID: 22535415].
[84]
Henshall, D.C.; Hamer, H.M.; Pasterkamp, R.J.; Goldstein, D.B.; Kjems, J.; Prehn, J.H.M.; Schorge, S.; Lamottke, K.; Rosenow, F. MicroRNAs in epilepsy: pathophysiology and clinical utility. Lancet Neurol., 2016, 15(13), 1368-1376. [http://dx.doi.org/10.1016/S1474-4422(16)30246-0]. [PMID: 27839653].
[85]
Miller-Delaney, S.F.; Bryan, K.; Das, S.; McKiernan, R.C.; Bray, I.M.; Reynolds, J.P.; Gwinn, R.; Stallings, R.L.; Henshall, D.C. Differential DNA methylation profiles of coding and non-coding genes define hippocampal sclerosis in human temporal lobe epilepsy. Brain, 2015, 138(Pt 3), 616-631. [http://dx.doi.org/10.1093/brain/awu373]. [PMID: 25552301].
[86]
Reschke, C.R.; Henshall, D.C. microRNA and epilepsy. Adv. Exp. Med. Biol., 2015, 888, 41-70. [http://dx.doi.org/10.1007/978-3-319-22671-2_4]. [PMID: 26663178].
[87]
André, P.J.N. L. A. D.; T.; Buclin; Rothuizen, a. L. E. Therapeutic drug monitoring of antiepileptic drugs in the 21st centuy. Epileptologie, 2015, 32, 78-84.
[88]
Ludden, T.M. Nonlinear pharmacokinetics: clinical Implications. Clin. Pharmacokinet., 1991, 20(6), 429-446. [http://dx.doi.org/10.2165/00003088-199120060-00001]. [PMID: 2044328].
[89]
Buchthal, F.; Svensmark, O.; Schiller, P.J. Clinical and electroencephalographic correlations with serum levels of diphenylhydanotin. Arch. Neurol., 1960, 2, 624-630. [http://dx.doi.org/10.1001/archneur.1960.03840120030004]. [PMID: 13805571].
[90]
Lund, L. Anticonvulsant effect of diphenylhydantoin relative to plasma levels. A prospective three-year study in ambulant patients with generalized epileptic seizures. Arch. Neurol., 1974, 31(5), 289-294. [http://dx.doi.org/10.1001/archneur.1974.00490410037002]. [PMID: 4212949].
[91]
Schmidt, D.; Einicke, I.; Haenel, F. The influence of seizure type on the efficacy of plasma concentrations of phenytoin, phenobarbital, and carbamazepine. Arch. Neurol., 1986, 43(3), 263-265. [http://dx.doi.org/10.1001/archneur.1986.00520030053013]. [PMID: 3947275].
[92]
Fröscher, W.; Eichelbaum, M.; Gugler, R.; Hildenbrand, G.; Penin, H. A prospective randomised trial on the effect of monitoring plasma anticonvulsant levels in epilepsy. J. Neurol., 1981, 224(3), 193-201. [http://dx.doi.org/10.1007/BF00313281]. [PMID: 6162015].
[93]
Jannuzzi, G.; Cian, P.; Fattore, C.; Gatti, G.; Bartoli, A.; Monaco, F.; Perucca, E. A multicenter randomized controlled trial on the clinical impact of therapeutic drug monitoring in patients with newly diagnosed epilepsy. Epilepsia, 2000, 41(2), 222-230. [http://dx.doi.org/10.1111/j.1528-1157.2000.tb00144.x]. [PMID: 10691121].
[94]
Morris, R.G.; Black, A.B.; Harris, A.L.; Batty, A.B.; Sallustio, B.C. Lamotrigine and therapeutic drug monitoring: retrospective survey following the introduction of a routine service. Br. J. Clin. Pharmacol., 1998, 46(6), 547-551. [http://dx.doi.org/10.1046/j.1365-2125.1998.00835.x]. [PMID: 9862243].
[95]
Nicholas, J.M.; Ridsdale, L.; Richardson, M.P.; Ashworth, M.; Gulliford, M.C. Trends in antiepileptic drug utilisation in UK primary care 1993-2008: cohort study using the General Practice Research Database. Seizure, 2012, 21(6), 466-470. [http://dx.doi.org/10.1016/j.seizure.2012.04.014]. [PMID: 22608976].
[96]
Malerba, A.; Ciampa, C.; De Fazio, S.; Fattore, C.; Frassine, B.; La Neve, A.; Pellacani, S.; Specchio, L.M.; Tiberti, A.; Tinuper, P.; Perucca, E. Patterns of prescription of antiepileptic drugs in patients with refractory epilepsy at tertiary referral centres in Italy. Epilepsy Res., 2010, 91(2-3), 273-282. [http://dx.doi.org/10.1016/j.eplepsyres.2010.08.002]. [PMID: 20810249].
[97]
Perucca, E. Is there a role for therapeutic drug monitoring of new anticonvulsants? Clin. Pharmacokinet., 2000, 38(3), 191-204. [http://dx.doi.org/10.2165/00003088-200038030-00001]. [PMID: 10749516].
[98]
Harden, C.L.; Trifiletti, R.; Kutt, H. Felbamate levels in patients with epilepsy. Epilepsia, 1996, 37(3), 280-283. [http://dx.doi.org/10.1111/j.1528-1157.1996.tb00026.x]. [PMID: 8598188].
[99]
Harden, C.L.; Pennell, P.B.; Koppel, B.S.; Hovinga, C.A.; Gidal, B.; Meador, K.J.; Hopp, J.; Ting, T.Y.; Hauser, W.A.; Thurman, D.; Kaplan, P.W.; Robinson, J.N.; French, J.A.; Wiebe, S.; Wilner, A.N.; Vazquez, B.; Holmes, L.; Krumholz, A.; Finnell, R.; Shafer, P.O.; Le Guen, C.L. Management issues for women with epilepsy--focus on pregnancy (an evidence-based review): III. Vitamin K, folic acid, blood levels, and breast-feeding: Report of the Quality Standards Subcommittee and Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology and the American Epilepsy Society. Epilepsia, 2009, 50(5), 1247-1255. [http://dx.doi.org/10.1111/j.1528-1167.2009.02130.x]. [PMID: 19507305].
[100]
Patsalos, P.N.; Berry, D.J.; Bourgeois, B.F.; Cloyd, J.C.; Glauser, T.A.; Johannessen, S.I.; Leppik, I.E.; Tomson, T.; Perucca, E. Antiepileptic drugs--best practice guidelines for therapeutic drug monitoring: a position paper by the subcommission on therapeutic drug monitoring, ILAE Commission on Therapeutic Strategies. Epilepsia, 2008, 49(7), 1239-1276. [http://dx.doi.org/10.1111/j.1528-1167.2008.01561.x]. [PMID: 18397299].
[101]
D’Anto, J.W.W.; Rossetti, A.O.; Decosterd, L.A.; Buclin, T.; Novy, J. Lamotrigine serum levels: ceiling effect in people with epilepsy in remission? Epilepsy Behav., 2017. [http://dx.doi.org/10.1016/j.yebeh.2017.03.031].
[102]
Poolos, N.P.; Castagna, C.E.; Williams, S.; Miller, A.B.; Story, T.J. Association between antiepileptic drug dose and long-term response in patients with refractory epilepsy. Epilepsy Behav., 2017, 69, 59-68. [http://dx.doi.org/10.1016/j.yebeh.2016.10.010]. [PMID: 28235655].
[103]
Decosterd, L.; Mercier, T.; André, P.; Bertholet, S.; Rothuizen, L.A.O.R.; Buclin, T. Multiplex mass spectrometry analysis of latest-generation antiepileptic drugs: A clinically useful laboratory tool for improved real-time patients’ care. Epileptologie, 2015, 32, 85-89.
[104]
Patsalos, P.N.; Berry, D.J. Therapeutic drug monitoring of antiepileptic drugs by use of saliva. Ther. Drug Monit., 2013, 35(1), 4-29. [http://dx.doi.org/10.1097/FTD.0b013e31827c11e7]. [PMID: 23288091].
[105]
Milovanovic, J.R.; Jankovic, S.M. Population pharmacokinetics of lamotrigine in patients with epilepsy. Int. J. Clin. Pharmacol. Ther., 2009, 47(12), 752-760. [http://dx.doi.org/10.5414/CPP47752]. [PMID: 19954714].
[106]
Jankovic, S.M.; Jovanovic, D.; Milovanovic, J.R. Pharmacokinetic modeling of carbamazepine based on clinical data from Serbian epileptic patients. Methods Find. Exp. Clin. Pharmacol., 2008, 30(9), 707-713. [http://dx.doi.org/10.1358/mf.2008.30.9.1323496]. [PMID: 19229380].
[107]
Balestrini, S.; Sisodiya, S.M. Pharmacogenomics in epilepsy. Neurosci. Lett., 2017. [PMID: 28082152].
[108]
Tate, S.K.; Depondt, C.; Sisodiya, S.M.; Cavalleri, G.L.; Schorge, S.; Soranzo, N.; Thom, M.; Sen, A.; Shorvon, S.D.; Sander, J.W.; Wood, N.W.; Goldstein, D.B. Genetic predictors of the maximum doses patients receive during clinical use of the anti-epileptic drugs carbamazepine and phenytoin. Proc. Natl. Acad. Sci. USA, 2005, 102(15), 5507-5512. [http://dx.doi.org/10.1073/pnas.0407346102]. [PMID: 15805193].
[109]
Menzler, K.; Hermsen, A.; Balkenhol, K.; Duddek, C.; Bugiel, H.; Bauer, S.; Schorge, S.; Reif, P.S.; Klein, K.M.; Haag, A.; Oertel, W.H.; Hamer, H.M.; Knake, S.; Trucks, H.; Sander, T.; Rosenow, F. A common SCN1A splice-site polymorphism modifies the effect of carbamazepine on cortical excitability--a pharmacogenetic transcranial magnetic stimulation study. Epilepsia, 2014, 55(2), 362-369. [http://dx.doi.org/10.1111/epi.12515]. [PMID: 24417206].
[110]
Devinsky, O.; Cross, J.H.; Laux, L.; Marsh, E.; Miller, I.; Nabbout, R.; Scheffer, I.E.; Thiele, E.A.; Wright, S. Trial of Cannabidiol for Drug-Resistant Seizures in the Dravet Syndrome. N. Engl. J. Med., 2017, 376(21), 2011-2020. [http://dx.doi.org/10.1056/NEJMoa1611618]. [PMID: 28538134].
[111]
Pierson, T.M.; Yuan, H.; Marsh, E.D.; Fuentes-Fajardo, K.; Adams, D.R.; Markello, T.; Golas, G.; Simeonov, D.R.; Holloman, C.; Tankovic, A.; Karamchandani, M.M.; Schreiber, J.M.; Mullikin, J.C.; Tifft, C.J.; Toro, C.; Boerkoel, C.F.; Traynelis, S.F.; Gahl, W.A. GRIN2A mutation and early-onset epileptic encephalopathy: personalized therapy with memantine. Ann. Clin. Transl. Neurol., 2014, 1(3), 190-198. [http://dx.doi.org/10.1002/acn3.39]. [PMID: 24839611].
[112]
Chung, W.H.; Chang, W.C.; Lee, Y.S.; Wu, Y.Y.; Yang, C.H.; Ho, H.C.; Chen, M.J.; Lin, J.Y.; Hui, R.C.; Ho, J.C.; Wu, W.M.; Chen, T.J.; Wu, T.; Wu, Y.R.; Hsih, M.S.; Tu, P.H.; Chang, C.N.; Hsu, C.N.; Wu, T.L.; Choon, S.E.; Hsu, C.K.; Chen, D.Y.; Liu, C.S.; Lin, C.Y.; Kaniwa, N.; Saito, Y.; Takahashi, Y.; Nakamura, R.; Azukizawa, H.; Shi, Y.; Wang, T.H.; Chuang, S.S.; Tsai, S.F.; Chang, C.J.; Chang, Y.S.; Hung, S.I. Genetic variants associated with phenytoin-related severe cutaneous adverse reactions. JAMA, 2014, 312(5), 525-534. [http://dx.doi.org/10.1001/jama.2014.7859]. [PMID: 25096692].
[113]
Dombrowski, S.M.; Desai, S.Y.; Marroni, M.; Cucullo, L.; Goodrich, K.; Bingaman, W.; Mayberg, M.R.; Bengez, L.; Janigro, D. Overexpression of multiple drug resistance genes in endothelial cells from patients with refractory epilepsy. Epilepsia, 2001, 42(12), 1501-1506. [http://dx.doi.org/10.1046/j.1528-1157.2001.12301.x]. [PMID: 11879359].
[114]
Aronica, E.; Gorter, J.A.; Ramkema, M.; Redeker, S.; Ozbas-Gerçeker, F.; van Vliet, E.A.; Scheffer, G.L.; Scheper, R.J.; van der Valk, P.; Baayen, J.C.; Troost, D. Expression and cellular distribution of multidrug resistance-related proteins in the hippocampus of patients with mesial temporal lobe epilepsy. Epilepsia, 2004, 45(5), 441-451. [http://dx.doi.org/10.1111/j.0013-9580.2004.57703.x]. [PMID: 15101825].
[115]
Grover, S.; Kukreti, R. A systematic review and meta-analysis of the role of ABCC2 variants on drug response in patients with epilepsy. Epilepsia, 2013, 54(5), 936-945. [http://dx.doi.org/10.1111/epi.12132]. [PMID: 23506516].
[116]
Wang, J.; Tan, L.; Tan, L.; Tian, Y.; Ma, J.; Tan, C.C.; Wang, H.F.; Liu, Y.; Tan, M.S.; Jiang, T.; Yu, J.T. Circulating microRNAs are promising novel biomarkers for drug-resistant epilepsy. Sci. Rep., 2015, 5, 10201. [http://dx.doi.org/10.1038/srep10201]. [PMID: 25984652].
[117]
Chen, P.; Lin, J.J.; Lu, C.S.; Ong, C.T.; Hsieh, P.F.; Yang, C.C.; Tai, C.T.; Wu, S.L.; Lu, C.H.; Hsu, Y.C.; Yu, H.Y.; Ro, L.S.; Lu, C.T.; Chu, C.C.; Tsai, J.J.; Su, Y.H.; Lan, S.H.; Sung, S.F.; Lin, S.Y.; Chuang, H.P.; Huang, L.C.; Chen, Y.J.; Tsai, P.J.; Liao, H.T.; Lin, Y.H.; Chen, C.H.; Chung, W.H.; Hung, S.I.; Wu, J.Y.; Chang, C.F.; Chen, L.; Chen, Y.T.; Shen, C.Y. Carbamazepine-induced toxic effects and HLA-B*1502 screening in Taiwan. N. Engl. J. Med., 2011, 364(12), 1126-1133. [http://dx.doi.org/10.1056/NEJMoa1009717]. [PMID: 21428768].
[118]
Ozeki, T.; Mushiroda, T.; Yowang, A.; Takahashi, A.; Kubo, M.; Shirakata, Y.; Ikezawa, Z.; Iijima, M.; Shiohara, T.; Hashimoto, K.; Kamatani, N.; Nakamura, Y. Genome-wide association study identifies HLA-A*3101 allele as a genetic risk factor for carbamazepine-induced cutaneous adverse drug reactions in Japanese population. Hum. Mol. Genet., 2011, 20(5), 1034-1041. [http://dx.doi.org/10.1093/hmg/ddq537]. [PMID: 21149285].
[119]
McCormack, M.; Alfirevic, A.; Bourgeois, S.; Farrell, J.J.; Kasperavičiūtė, D.; Carrington, M.; Sills, G.J.; Marson, T.; Jia, X.; de Bakker, P.I.W.; Chinthapalli, K.; Molokhia, M.; Johnson, M.R.; O’Connor, G.D.; Chaila, E.; Alhusaini, S.; Shianna, K.V.; Radtke, R.A.; Heinzen, E.L.; Walley, N.; Pandolfo, M.; Pichler, W.; Park, B.K.; Depondt, C.; Sisodiya, S.M.; Goldstein, D.B.; Deloukas, P.; Delanty, N.; Cavalleri, G.L.; Pirmohamed, M. HLA-A*3101 and carbamazepine-induced hypersensitivity reactions in Europeans. N. Engl. J. Med., 2011, 364(12), 1134-1143. [http://dx.doi.org/10.1056/NEJMoa1013297]. [PMID: 21428769].
[120]
Chen, Z.; Liew, D.; Kwan, P. Effects of a HLA-B*15:02 screening policy on antiepileptic drug use and severe skin reactions. Neurology, 2014, 83(22), 2077-2084. [http://dx.doi.org/10.1212/WNL.0000000000001034]. [PMID: 25355835].


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 17
ISSUE: 5
Year: 2019
Page: [447 - 458]
Pages: 12
DOI: 10.2174/1570159X16666180308154646
Price: $58

Article Metrics

PDF: 13
HTML: 4