354
Views
26
CrossRef citations to date
0
Altmetric
Review

Furthering our understanding of SUDEP: the role of animal models

, , , , &
Pages 561-572 | Received 27 Dec 2015, Accepted 21 Mar 2016, Published online: 18 Apr 2016

References

  • Rao VR, Lowenstein DH. Epilepsy. Curr Biol. 2015;25(17):R742– R746.
  • Moshé SL, Perucca E, Ryvlin P, et al. Epilepsy: new advances. Lancet. 2014;385(9971):884–898.
  • Nashef L, Ryvlin P. Sudden unexpected death in epilepsy (SUDEP): update and reflections. Neurol Clin. 2009;27(4):1063–1074.
  • Duncan JS, Sander JW, Sisodiya SM, et al. Adult epilepsy. Lancet. 2006;367(9516):1087–1100.
  • Hesdorffer DC, Tomson T, Benn E, et al. Combined analysis of risk factors for SUDEP. Epilepsia. 2011;52(6):1150–1159.
  • Nei M, Hays R. Sudden unexpected death in epilepsy. Curr Neurol Neurosci Rep. 2010;10(4):319–326.
  • Hesdorffer DC, Tomson T. Sudden unexpected death in epilepsy. Potential role of antiepileptic drugs. CNS Drugs. 2013;27(2):113–119.
  • Schuele SU, Widdess-Walsh P, Bermeo A, et al. Sudden unexplained death in epilepsy: the role of the heart. Cleve Clin J Med. 2007;74(Suppl 1):S121–7.
  • Devinsky O. Sudden, unexpected death in epilepsy. N Engl J Med. 2011;365(19):1801–1811.
  • Surges R, Thijs RD, Tan HL, et al. Sudden unexpected death in epilepsy: risk factors and potential pathomechanisms. Nat Rev Neurol. 2009;5(9):492–504.
  • Scorza FA, Terra VC, Arida RM, et al. Sudden unexpected death in epilepsy and winter temperatures: it’s important to know that it’s c-c-c-c-cold outside. Epilepsy Behav. 2009;14(4):707. author reply 708.
  • So EL. What is known about the mechanisms underlying SUDEP? Epilepsia. 2008;49(Suppl 9):93–98.
  • Stöllberger C, Finsterer J. Cardiorespiratory findings in sudden unexplained/unexpected death in epilepsy (SUDEP). Epilepsy Res. 2004;59(1):51–60.
  • Tejada S, Martorell M, Capó X, et al. Omega-3 fatty acids in the management of epilepsy. Curr Top Med Chem. 2016;16:1–1.
  • DeGiorgio CM, Miller PR, Harper R, et al. Fish oil (n-3 fatty acids) in drug resistant epilepsy: a randomised placebo-controlled crossover study. J Neurol Neurosurg Psychiatry. 2015;86(1):65–70.
  • DeGiorgio CM, Scorza FA. Epilepsy & behavior: 15th anniversary research on omega-3 fatty acids for epilepsy. Epilepsy Behav. 2014;40:124–125.
  • Scorza FA, Cysneiros RM, Arida RM, et al. The other side of the coin: beneficiary effect of omega-3 fatty acids in sudden unexpected death in epilepsy. Epilepsy Behav. 2008;13(2):279–283.
  • Scorza FA, Arida RM, Terra VC, et al. What can be done to reduce the risk of SUDEP? Epilepsy Behav. 2010;18(3):137–138.
  • Seyal M, Pascual F, Lee C-YM, et al. Seizure-related cardiac repolarization abnormalities are associated with ictal hypoxemia. Epilepsia. 2011;52(11):2105–2111.
  • Seyal M, Bateman LM, Li C-S. Impact of periictal interventions on respiratory dysfunction, postictal EEG suppression, and postictal immobility. Epilepsia. 2013;54(2):377–382.
  • van der Lende M, Surges R, Sander JW, et al. Cardiac arrhythmias during or after epileptic seizures. J Neurol Neurosurg Psychiatry. 2015;87(1):1–6.
  • Surges R, Sander JW. Sudden unexpected death in epilepsy: mechanisms, prevalence, and prevention. Curr Opin Neurol. 2012;25(2):201–207.
  • Johnston SC, Horn JK, Valente J, et al. The role of hypoventilation in a sheep model of epileptic sudden death. Ann Neurol. 1995;37(4):531–537.
  • Johnston SC, Siedenberg R, Min JK, et al. Central apnea and acute cardiac ischemia in a sheep model of epileptic sudden death. Ann Neurol. 1997;42(4):588–594.
  • Simon RP. Epileptic sudden death: animal models. Epilepsia. 1997;38(11 Suppl):S35–S37.
  • Mameli O, Caria MA, Pintus A, et al. Sudden death in epilepsy: an experimental animal model. Seizure. 2006;15(5):275–287.
  • Faingold CL, Randall M, Tupal S. DBA/1 mice exhibit chronic susceptibility to audiogenic seizures followed by sudden death associated with respiratory arrest. Epilepsy Behav. 2010;17(4):436–440.
  • Venit EL, Shepard BD, Seyfried TN. Oxygenation prevents sudden death in seizure-prone mice. Epilepsia. 2004;45(8):993–996.
  • Tupal S, Faingold CL. Evidence supporting a role of serotonin in modulation of sudden death induced by seizures in DBA/2 mice. Epilepsia. 2006;47(1):21–26.
  • Shen HY, Li T, Boison D. A novel mouse model for sudden unexpected death in epilepsy (SUDEP): role of impaired adenosine clearance. Epilepsia. 2010;51(3):465–468.
  • Kommajosyula SP, Randall ME, Faingold CL. Inhibition of adenosine metabolism induces changes in post-ictal depression, respiration, and mortality in genetically epilepsy prone rats. Epilepsy Res. 2015;119:13–19.
  • Scorza FA, de Albuquerque R, Arida RM, et al. Could sudden death syndrome (SDS) in chickens (Gallus gallus) be a valid animal model for sudden unexpected death in epilepsy (SUDEP)? Med Hypotheses. 2009;73(1):67–69.
  • Szabó CA, Knape KD, Leland MM, et al. Mortality in captive baboons with seizures: a new model for SUDEP? Epilepsia. 2009;50(8):1995–1998.
  • Kalume F, Westenbroek RE, Cheah CS, et al. Sudden unexpected death in a mouse model of Dravet syndrome. J Clin Invest. 2013;123(4):1798–1808.
  • Auerbach DS, Jones J, Clawson BC, et al. Altered cardiac electrophysiology and SUDEP in a model of Dravet syndrome. PLoS One. 2013;8(10):e77843.
  • Moore BM, Jerry Jou C, Tatalovic M, et al. The Kv1.1 null mouse, a model of sudden unexpected death in epilepsy (SUDEP). Epilepsia. 2014;55(11):1808–1816.
  • Glasscock E, Yoo JW, Chen TT, et al. Kv1.1 potassium channel deficiency reveals brain-driven cardiac dysfunction as a candidate mechanism for sudden unexplained death in epilepsy. J Neurosci. 2010;30(15):5167–5175.
  • Scorza FA, Siqueira GM, Scorza CA, et al. Two-hit rodent seizure model: a promising new design for research in SUDEP. Epilepsy Behav. 2014;35:26–27.
  • Faingold CL, Tupal S, Randall M. Prevention of seizure-induced sudden death in a chronic SUDEP model by semichronic administration of a selective serotonin reuptake inhibitor. Epilepsy Behav. 2011;22(2):186–190.
  • Blum AS. Respiratory physiology of seizures. J Clin Neurophysiol. 2009;26(5):309–15.
  • Buchanan GF, Smith HR, MacAskill A, et al. 5-HT2A receptor activation is necessary for CO2-induced arousal. J Neurophysiol. 2015;114(1):233:43.
  • Buchanan GF, Murray NM, Hajek MA, et al. Serotonin neurones have anti-convulsant effects and reduce seizure-induced mortality. J Physiol. 2014;592(19):4395–4410.
  • Richerson GB, Buchanan GF. The serotonin axis: shared mechanisms in seizures, depression, and SUDEP. Epilepsia. 2011;52(Suppl 1):28–38.
  • Faingold CL, Randall M, Mhaskar Y, et al. Differences in serotonin receptor expression in the brainstem may explain the differential ability of a serotonin agonist to block seizure-induced sudden death in DBA/2 vs. DBA/1 mice. Brain Res. 2011;1418:104–110.
  • Feng H-J, Faingold CL. Abnormalities of serotonergic neurotransmission in animal models of SUDEP. Epilepsy Behav;2015. doi:10.1016/j.yebeh.2015.06.008.
  • Bateman LM, Li CS, Lin TC, et al. Serotonin reuptake inhibitors are associated with reduced severity of ictal hypoxemia in medically refractory partial epilepsy. Epilepsia. 2010;51(10):2211–2214.
  • Fedele DE, Li T, Lan JQ, et al. Adenosine A1 receptors are crucial in keeping an epileptic focus localized. Exp Neurol. 2006;200(1):184–190.
  • During MJ, Spencer DD. Adenosine: a potential mediator of seizure arrest and postictal refractoriness. Ann Neurol. 1992;32(5):618–624.
  • Tseng CJ, Biaggioni I, Appalsamy M, et al. Purinergic receptors in the brainstem mediate hypotension and bradycardia. Hypertension. 1988;11(2):191–197.
  • Barraco RA, Janusz CA, Schoener EP, et al. Cardiorespiratory function is altered by picomole injections of 5’-N-ethylcarboxamidoadenosine into the nucleus tractus solitarius of rats. Brain Res. 1990;507(2):234–246.
  • Mantegazza M, Curia G, Biagini G, et al. Voltage-gated sodium channels as therapeutic targets in epilepsy and other neurological disorders. Lancet Neurol. 2010;9(4):413–424.
  • Qi Y, Wang J, Bomben VC, et al. Hyper-SUMOylation of the Kv7 potassium channel diminishes the M-current leading to seizures and sudden death. Neuron. 2014;83(5):1159–1171.
  • Dodson PD, Forsythe ID. Presynaptic K+ channels: electrifying regulators of synaptic terminal excitability. Trends Neurosci. 2004;27(4):210–217.
  • Nerbonne JM, Kass RS. Molecular physiology of cardiac repolarization. Physiol Rev. 2005;85(4):1205–1253.
  • Curia G, Lucchi C, Vinet J, et al. Pathophysiogenesis of mesial temporal lobe epilepsy: is prevention of damage antiepileptogenic? Curr Med Chem. 2014;21(6):663–688.
  • Glasscock E, Qian J, Yoo JW, et al. Masking epilepsy by combining two epilepsy genes. Nat Neurosci. 2007;10(12):1554–1558.
  • Lopantsev V, Tempel BL, Schwartzkroin PA. Hyperexcitability of CA3 pyramidal cells in mice lacking the potassium channel subunit Kv1.1. Epilepsia. 2003;44(12):1506–1512.
  • Derry CP, Duncan S. Sleep and epilepsy. Epilepsy Behav. 2013;26(3):394–404.
  • Nobili L, Proserpio P, Rubboli G, et al. Sudden unexpected death in epilepsy (SUDEP) and sleep. Sleep Med Rev. 2011;15(4):237–246.
  • Bateman LM, Spitz M, Seyal M. Ictal hypoventilation contributes to cardiac arrhythmia and SUDEP: report on two deaths in video-EEG-monitored patients. Epilepsia. 2010;51(5):916–920.
  • Surges R, Adjei P, Kallis C, et al. Pathologic cardiac repolarization in pharmacoresistant epilepsy and its potential role in sudden unexpected death in epilepsy: a case-control study. Epilepsia. 2010;51(2):233–242.
  • Tomson T, Walczak T, Sillanpaa M, et al. Sudden unexpected death in epilepsy: a review of incidence and risk factors. Epilepsia. 2005;46:54–61.
  • Imaeda N. Characterization of serum enzyme activities and electrolyte levels in broiler chickens after death from sudden death syndrome. Poult Sci. 1999;78(1):66–69.
  • Newberry RC, Gardiner EE, Hunt JR. Behavior of chickens prior to death from sudden death syndrome. Poult Sci. 1987;66(9):1446–1450.
  • Bateman LM, Li CS, Seyal M. Ictal hypoxemia in localization-related epilepsy: analysis of incidence, severity and risk factors. Brain. 2008;131:3239–3245.
  • Campos RR, Tolentino-Silva FRP, Mello LE. Respiratory pattern in a rat model of epilepsy. Epilepsia. 2003;44(5):712–717.
  • Gualtieri F, Marinelli C, Longo D, et al. Hypoxia markers are expressed in interneurons exposed to recurrent seizures. Neuromolecular Med. 2013;15(1):133–146.
  • Budzińska K. Hypoglossal and phrenic nerve responses to changes in oxygen tension during picrotoxin-induced seizures in the rat. J Physiol Pharmacol. 2004;55(Suppl 3):31–39.
  • Kanter RK, Strauss JA, Sauro MD. Comparison of neurons in rat medulla oblongata with Fos immunoreactivity evoked by seizures, chemoreceptor, or baroreceptor stimulation. Neuroscience. 1996;73(3):807–816.
  • Terndrup TE, Fordyce WE. Respiratory drive during status epilepticus and its treatment: comparison of diazepam and lorazepam. Epilepsy Res. 1995;20(1):21–30.
  • Aiba I, Noebels JL. Spreading depolarization in the brainstem mediates sudden cardiorespiratory arrest in mouse SUDEP models. Sci Transl Med. 2015;7:282ra46.
  • Paydarfar D, Eldridge FL, Scott SC, et al. Respiratory responses to focal and generalized seizures in cats. Am J Physiol. 1991;260(5 Pt 2):R934–R940.
  • Paydarfar D, Eldridge FL, Wagner PG, et al. Neural respiratory responses to cortically induced seizures in cats. Respir Physiol. 1992;89(2):225–237.
  • St.-John WM, Rudkin AH, Homes GL, et al. Changes in respiratory modulated neural activities, consistent with obstructive and central apnea, during fictive seizures in an in situ anaesthetized rat preparation. Epilepsy Res. 2006;70:218–228.
  • Faingold CL, Tupal S, Randall M. Prevention of seizure-induced sudden death in a chronic SUDEP model by semichronic administration of a selective serotonin reuptake inhibitor. Epilepsy Behav. 2011;22(2):186–190.
  • Buchanan GF, Murray NM, Hajek MA, et al. Serotonin neurones have anti-convulsant effects and reduce seizure-induced mortality. J Physiol. 2014;592(Pt 19):4395–4410.
  • Sowers LP, Massey CA, Gehlbach BK, et al. Sudden unexpected death in epilepsy: fatal post-ictal respiratory and arousal mechanisms. Respir Physiol Neurobiol. 2013;189(2):315–323.
  • Richerson GB. Serotonergic neurons as carbon dioxide sensors that maintain pH homeostasis. Nat Rev Neurosci. 2004;5(6):449–461.
  • Feldman JL, Mitchell GS, Nattie EE. Breathing: rhythmicity, plasticity, chemosensitivity. Annu Rev Neurosci. 2003;26:239–266.
  • Zeng C, Long X, Cotten JF, et al. Fluoxetine prevents respiratory arrest without enhancing ventilation in DBA/1 mice. Epilepsy Behav. 2015;45:1–7.
  • Faingold CL, Kommajosyula SP, Long X, et al. Serotonin and sudden death: differential effects of serotonergic drugs on seizure-induced respiratory arrest in DBA/1 mice. Epilepsy Behav. 2014;37:198–203.
  • Teply RM, Packard KA, White ND, et al. Treatment of depression in patients with concomitant cardiac disease. Prog Cardiovasc Dis. 2015. doi:10.1016/j.pcad.2015.11.003.
  • Maljuric NM, Noordam R, Aarts N, et al. Use of selective serotonin re-uptake inhibitors and the heart rate corrected QT interval in a real-life setting: the population-based Rotterdam Study. Br J Clin Pharmacol. 2015;80(4):698–705.
  • Lusetti M, Licata M, Silingardi E, et al. Cardiac toxicity in selective serotonin reuptake inhibitor users. Am J Forensic Med Pathol. 2015;36(4):293–297.
  • Applegate CD, Tecott LH. Global increases in seizure susceptibility in mice lacking 5-HT2C receptors: a behavioral analysis. Exp Neurol. 1998;154(2):522–530.
  • Upton N, Stean T, Middlemiss D, et al. Studies on the role of 5-HT2C and 5-HT2B receptors in regulating generalised seizure threshold in rodents. Eur J Pharmacol. 1998;359(1):33–40.
  • Brennan TJ, Seeley WW, Kilgard M, et al. Sound-induced seizures in serotonin 5-HT2c receptor mutant mice. Nat Genet. 1997;16(4):387–390.
  • Wada Y, Shiraishi J, Nakamura M, et al. Prolonged but not acute fluoxetine administration produces its inhibitory effect on hippocampal seizures in rats. Psychopharmacology (Berl). 1995;118(3):305–309.
  • Favale E, Rubino V, Mainardi P, et al. Anticonvulsant effect of fluoxetine in humans. Neurology. 1995;45(10):1926–1927.
  • Ahmad S, Fowler LJ, Whitton PS. Lamotrigine, carbamazepine and phenytoin differentially alter extracellular levels of 5-hydroxytryptamine, dopamine and amino acids. Epilepsy Res. 2005;63(23):141–149.
  • Gettys GC, Liu F, Kimlin E, et al. Adenosine A(1) receptors in mouse pontine reticular formation depress breathing, increase anesthesia recovery time, and decrease acetylcholine release. Anesthesiology. 2013;118(2):327–36.
  • Huang Z-L, Zhang Z, Qu W-M. Roles of adenosine and its receptors in sleepwake regulation. Int Rev Neurobiol. 2014;119:349–371.
  • Lévesque M, Avoli M. The kainic acid model of temporal lobe epilepsy. Neurosci Biobehav Rev. 2013;37(10 Pt 2):2887–2899.
  • Lathers CM, Schraeder PL. Autonomic dysfunction in epilepsy: characterization of autonomic cardiac neural discharge associated with pentylenetetrazol-induced epileptogenic activity. Epilepsia. 1982;23(6):633–647.
  • Goodman JH, Homan RW, Crawford IL. Kindled seizures elevate blood pressure and induce cardiac arrhythmias. Epilepsia. 1990;31(5):489–495.
  • Goodman JH, Homan RW, Crawford IL. Kindled seizures activate both branches of the autonomic nervous system. Epilepsy Res. 1999;34(23):169–176.
  • Pansani AP, Colugnati DB, Schoorlemmer GHM, et al. Repeated amygdalakindled seizures induce ictal rebound tachycardia in rats. Epilepsy Behav. 2011;22(3):442–449.
  • Darbin O, Casebeer DJ, Naritoku DK. Cardiac dysrhythmia associated with the immediate postictal state after maximal electroshock in freely moving rat. Epilepsia. 2002;43(4):336–341.
  • Damasceno DD, Ferreira AJ, Doretto MC, et al. Cardiovascular dysautonomia after seizures induced by maximal electroshock in Wistar rats. Seizure. 2012;21(9):711–716.
  • Colugnati DB, Gomes PAP, Arida RM, et al. Analysis of cardiac parameters in animals with epilepsy: possible cause of sudden death? Arq Neuropsiquiatr. 2005;63(4):1035–1041.
  • Metcalf CS, Radwanski PB, Bealer SL. Status epilepticus produces chronic alterations in cardiac sympathovagal balance. Epilepsia. 2009;50(4):747–754.
  • Metcalf CS, Poelzing S, Little JG, et al. Status epilepticus induces cardiac myofilament damage and increased susceptibility to arrhythmias in rats. Am J Physiol Heart Circ Physiol. 2009;297(6):H2120–H2127.
  • Pansani AP, Sonoda EY, Scorza FA, et al. Premature ventricular complexes: How benign are they in epilepsy? Epilepsy Behav. 2015;52(Pt A):74–75.
  • Sakamoto K, Saito T, Orman R, et al. Autonomic consequences of kainic acidinduced limbic cortical seizures in rats: peripheral autonomic nerve activity, acute cardiovascular changes, and death. Epilepsia. 2008;49(6):982–996.
  • Hotta H, Koizumi K, Stewart M. Cardiac sympathetic nerve activity during kainic acid-induced limbic cortical seizures in rats. Epilepsia. 2009;50(4):923–927.
  • Naggar I, Lazar J, Kamran H, et al. Relation of autonomic and cardiac abnormalities to ventricular fibrillation in a rat model of epilepsy. Epilepsy Res. 2014;108(1):44–56.
  • Biet M, Morin N, Lessard-Beaudoin M, et al. Prolongation of action potential duration and QT interval during epilepsy linked to increased contribution of neuronal sodium channels to cardiac late Na+ current: potential mechanism for sudden death in epilepsy. Circ Arrhythm Electrophysiol. 2015;8(4):912–920.
  • Damasceno DD, Savergnini SQ, Gomes ERM, et al. Cardiac dysfunction in rats prone to audiogenic epileptic seizures. Seizure. 2013;22(4):259–266.
  • Fazan R, Silva CAA, Oliveira JAC, et al. Evaluation of cardiovascular risk factors in the Wistar audiogenic rat (WAR) strain. PLoS One. 2015;10(6):e0129574. doi:10.1371/journal.pone.0129574.
  • Voss A, Kurths J, Kleiner HJ, et al. The application of methods on non-linear dynamics for the improved and predictive recognition of patients threatened by sudden cardiac death. Cardiovasc Res. 1996;31:419–433.
  • Colugnati DB, Pansani AP, Scorza CA, et al. Phenytoin is not involved with changes in heart rate of rats with epilepsy. Epilepsy Behav. 2015;52(Pt A):42–43.
  • Sonoda EYF, Colugnati DB, Scorza CA, et al. Is cold the new hot in sudden unexpected death in epilepsy? Effect of low temperature on heart rate of rats with epilepsy. Arq Neuropsiquiatr. 2008;66(4):848–852.
  • Pansani AP, Colugnati DB, Sonoda EYF, et al. Tachycardias and sudden unexpected death in epilepsy: a gold rush by an experimental route. Epilepsy Behav. 2010;19(3):546–547.
  • Scorza CA, Cavalheiro EA, Scorza FA. SUDEP research: challenges for the future. Epilepsy Behav. 2013;28(1):134–135.
  • Devinsky OFD. The future of SUDEP research. In: Chapman D, Panelli R, Hanna JJT, editors. Sudden unexpected death in epilepsy: continuing the global conversation. Camberwell, Australia: Epilepsy Australia, Epilepsy Bereaved and SUDEP Aware; 2011. p. 78–79.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.