Relation of autonomic and cardiac abnormalities to ventricular fibrillation in a rat model of epilepsy

Epilepsy Research

Volumn 108, Issue 1, 2014, Pages 44-56

  Naggar, Isaac ^a   Lazar, Jason ^a   Kamran, Haroon ^a   Orman, Rena ^a   Stewart, Mark ^a  

^a SUNY DOWNSTATE MEDICAL CENTER   (United States)

Author keywords

Arrhythmia; Cardiac hypertrophy; Cardiomyopathy; QT dispersion; Seizure

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTONOMIC DYSFUNCTION; BLOOD PRESSURE MEASUREMENT; CARDIOVASCULAR RISK; CONTROLLED STUDY; CORRELATIONAL STUDY; DISEASE ASSOCIATION; DISEASE MODEL; DISEASE PREDISPOSITION; DISEASE SEVERITY; ECHOCARDIOGRAPHY; ELECTROCARDIOGRAPHY; EPILEPTIC STATE; HEART LEFT VENTRICLE WALL; HEART PERFORMANCE; HEART RATE VARIABILITY; HEART REPOLARIZATION; HEART VENTRICLE FIBRILLATION; HEART VENTRICLE HYPERTROPHY; HEART WEIGHT; HISTOLOGY; HYPOXEMIA; NONHUMAN; PRIORITY JOURNAL; QT DISPERSION; RAT; SYSTOLIC DYSFUNCTION; VAGUS NERVE STIMULATION; VAGUS TONE;

ARRHYTHMIA; CARDIAC HYPERTROPHY; CARDIOMYOPATHY; QT DISPERSION; SEIZURE;

ANIMALS; AUTONOMIC NERVOUS SYSTEM; CARDIOMEGALY; DISEASE MODELS, ANIMAL; EPILEPSY; HEART RATE; MALE; RATS; RATS, SPRAGUE-DAWLEY; VAGUS NERVE; VENTRICULAR FIBRILLATION;

EID: 84890790192     PISSN: 09201211     EISSN: 18726844     Source Type: Journal    
DOI: 10.1016/j.eplepsyres.2013.10.018     Document Type: Article

References (60)

1. Akalin F., Tirtir A., Yilmaz Y. Increased QT dispersion in epileptic children. Acta Paediatr. 2003, 92(8):916-920.
2. Bacharova L., Michalak K., Kyselovic J., Klimas J. Relation between QRS amplitude and left ventricular mass in the initial stage of exercise-induced left ventricular hypertrophy in rats. Clin. Exp. Hypertens. 2005, 27(6):533-541. 10.1081/CEH-200068802.
3. Bacharova L., Plandorova J., Klimas J., Krenek P., Kyselovic J. Discrepancy between increased left ventricular mass and normal QRS voltage is associated with decreased connexin 43 expression in early stage of left ventricular hypertrophy in spontaneously hypertensive rats. J. Electrocardiol. 2008, 41(6):730-734. 10.1016/j.jelectrocard.2008.01.013.
4. Bateman L.M., Li C.S., Seyal M. Ictal hypoxemia in localization-related epilepsy: analysis of incidence, severity and risk factors. Brain 2008, 131(Pt 12):3239-3245. 10.1093/brain/awn277.
5. Bealer S.L., Little J.G. Seizures following hippocampal kindling induce QT interval prolongation and increased susceptibility to arrhythmias in rats. Epilepsy Res. 2013, 10.1016/j.eplepsyres.2013.01.002.
6. Bristow M.R., Ginsburg R., Minobe W., Cubicciotti R.S., Sageman W.S., Lurie K., Billingham M.E., Harrison D.C., Stinson E.B. Decreased catecholamine sensitivity and beta-adrenergic-receptor density in failing human hearts. N. Engl. J. Med. 1982, 307(4):205-211. 10.1056/NEJM198207223070401.
7. Covolan L., Mello L.E. Temporal profile of neuronal injury following pilocarpine or kainic acid-induced status epilepticus. Epilepsy Res. 2000, 39(2):133-152.
8. Cunnington C., Garg S., Balachandran K.P. Seizure-associated takotsubo cardiomyopathy presenting with unheralded ventricular fibrillation. Int. J. Cardiol. 2012, 162(1):e21-e23. 10.1016/j.ijcard.2012.05.118.
9. Curia G., Longo D., Biagini G., Jones R.S., Avoli M. The pilocarpine model of temporal lobe epilepsy. J. Neurosci. Methods 2008, 172(2):143-157. 10.1016/j.jneumeth.2008.04.019.
10. Devinsky O. Effects of seizures on autonomic and cardiovascular function. Epilepsy Curr. 2004, 4(2):43-46. 10.1111/j.1535-7597.2004.42001.x.
11. Dogan E.A., Dogan U., Yildiz G.U., Akilli H., Genc E., Genc B.O., Gok H. Evaluation of cardiac repolarization indices in well-controlled partial epilepsy: 12-Lead ECG findings. Epilepsy Res. 2010, 90(1/2):157-163. 10.1016/j.eplepsyres.2010.04.008.
12. Dudek F.E., Clark S., Williams P.A., Grabenstatter H.L. Kainate-induced status epilepticus: a chronic model of acquired epilepsy. Models of Seizures and Epilepsy 2006, 415-432. Elsevier Academic, Amsterdam; Boston. A. Pitkänen, P.A. Schwartzkroin, S.L. Moshé (Eds.).
13. Espinosa P.S., Lee J.W., Tedrow U.B., Bromfield E.B., Dworetzky B.A. Sudden unexpected near death in epilepsy: malignant arrhythmia from a partial seizure. Neurology 2009, 72(19):1702-1703. 10.1212/WNL.0b013e3181a55f90.
14. Falconer B., Rajs J. Post-mortem findings of cardiac lesions in epileptics: a preliminary report. Forensic Sci. 1976, 8(1):63-71.
15. Ferlisi M., Tomei R., Carletti M., Moretto G., Zanoni T. Seizure induced ventricular fibrillation: a case of near-SUDEP. Seizure 2013, 22(3):249-251. 10.1016/j.seizure.2012.12.008.
16. Fowler M.B., Laser J.A., Hopkins G.L., Minobe W., Bristow M.R. Assessment of the beta-adrenergic receptor pathway in the intact failing human heart: progressive receptor down-regulation and subsensitivity to agonist response. Circulation 1986, 74(6):1290-1302.
17. Giorgi F.S., Malhotra S., Hasson H., Veliskova J., Rosenbaum D.M., Moshe S.L. Effects of status epilepticus early in life on susceptibility to ischemic injury in adulthood. Epilepsia 2005, 46(4):490-498. 10.1111/j. 0013-9580.2005.42304.x.
18. Goldman A.M., Glasscock E., Yoo J., Chen T.T., Klassen T.L., Noebels J.L. Arrhythmia in heart and brain: KCNQ1 mutations link epilepsy and sudden unexplained death. Sci. Transl. Med. 2009, 1(2):2ra6. 10.1126/scitranslmed.3000289.
19. Grossman S.P., Dacey D., Halaris A.E., Collier T., Routtenberg A. Aphagia and adipsia after preferential destruction of nerve cell bodies in hypothalamus. Science 1978, 202(4367):537-539.
20. Heart rate variability Standards of measurement, physiological interpretation, and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Eur. Heart J. 1996, 17(3):354-381.
21. Hotta H., Lazar J., Orman R., Koizumi K., Shiba K., Kamran H., Stewart M. Vagus nerve stimulation-induced bradyarrhythmias in rats. Auton. Neurosci. 2009, 151(2):98-105. 10.1016/j.autneu. 2009.07.008.
22. Jansen K., Lagae L. Cardiac changes in epilepsy. Seizure 2010, 19(8):455-460. 10.1016/j.seizure.2010.07.008.
23. Johnson M.S., DeMarco V.G., Heesch C.M., Whaley-Connell A.T., Schneider R.I., Rehmer N.T., Tilmon R.D., Ferrario C.M., Sowers J.R. Sex differences in baroreflex sensitivity, heart rate variability, and end organ damage in the TGR(mRen2)27 rat. Am. J. Physiol. Heart Circ. Physiol. 2011, 301(4):H1540-H1550. 10.1152/ajpheart.00593.2011.
24. Johnston S.C., Horn J.K., Valente J., Simon R.P. The role of hypoventilation in a sheep model of epileptic sudden death. Ann. Neurol. 1995, 37(4):531-537. 10.1002/ana.410370416.
25. Kmecova J., Klimas J. Heart rate correction of the QT duration in rats. Eur. J. Pharmacol. 2010, 641(2/3):187-192. 10.1016/j.ejphar.2010.05.038.
26. Leestma J.E., Walczak T., Hughes J.R., Kalelkar M.B., Teas S.S. A prospective study on sudden unexpected death in epilepsy. Ann. Neurol. 1989, 26(2):195-203. 10.1002/ana.410260203.
27. Little J.G., Bealer S.L. beta adrenergic blockade prevents cardiac dysfunction following status epilepticus in rats. Epilepsy Res. 2012, 99(3):233-239. 10.1016/j.eplepsyres.2011.12.003.
28. Litwin S.E., Katz S.E., Weinberg E.O., Lorell B.H., Aurigemma G.P., Douglas P.S. Serial echocardiographic-Doppler assessment of left ventricular geometry and function in rats with pressure-overload hypertrophy. Chronic angiotensin-converting enzyme inhibition attenuates the transition to heart failure. Circulation 1995, 91(10):2642-2654.
29. Lotufo P.A., Valiengo L., Bensenor I.M., Brunoni A.R. A systematic review and meta-analysis of heart rate variability in epilepsy and antiepileptic drugs. Epilepsia 2012, 53(2):272-282. 10.1111/j.1528-1167.2011.03361.x.
30. Malik M., Batchvarov V.N. Measurement, interpretation and clinical potential of QT dispersion. J. Am. Coll. Cardiol. 2000, 36(6):1749-1766.
31. Mascareno E., Galatioto J., Rozenberg I., Salciccioli L., Kamran H., Lazar J.M., Liu F., Pedrazzini T., Siddiqui M.A. Cardiac lineage protein-1 (CLP-1) regulates cardiac remodeling via transcriptional modulation of diverse hypertrophic and fibrotic responses and angiotensin II-transforming growth factor beta (TGF-beta1) signaling axis. J. Biol. Chem. 2012, 287(16):13084-13093. 10.1074/jbc.M111.288944.
32. Metcalf C.S., Poelzing S., Little J.G., Bealer S.L. Status epilepticus induces cardiac myofilament damage and increased susceptibility to arrhythmias in rats. Am. J. Physiol. Heart Circ. Physiol. 2009, 297(6):H2120-H2127. 10.1152/ajpheart.00724.2009.
33. Metcalf C.S., Radwanski P.B., Bealer S.L. Status epilepticus produces chronic alterations in cardiac sympathovagal balance. Epilepsia 2009, 50(4):747-754. 10.1111/j.1528-1167.2008.01764.x.
34. Naggar I., Uchida S., Kamran H., Lazar J., Stewart M. Autonomic boundary conditions for ventricular fibrillation and their implications for a novel defibrillation technique. J. Physiol. Sci. 2012, 62(6):479-492. 10.1007/s12576-012-0225-8.
35. Nashef L., So E.L., Ryvlin P., Tomson T. Unifying the definitions of sudden unexpected death in epilepsy. Epilepsia 2012, 53(2):227-233. 10.1111/j.1528-1167.2011.03358.x.
36. Natelson B.H., Suarez R.V., Terrence C.F., Turizo R. Patients with epilepsy who die suddenly have cardiac disease. Arch. Neurol. 1998, 55(6):857-860.
37. Nei M., Ho R.T., Sperling M.R. EKG abnormalities during partial seizures in refractory epilepsy. Epilepsia 2000, 41(5):542-548.
38. Neufeld G., Lazar J.M., Chari G., Kamran H., Akajagbor E., Salciccioli L., Kassotis J., Stewart M. Cardiac repolarization indices in epilepsy patients. Cardiology 2009, 114(4):255-260. 10.1159/000233236.
39. O'Gara T., Urban W., Polishchuk D., Pierre-Louis A., Stewart M. Continuous stimulation of transected distal nerves fails to prolong action potential propagation. Clin Orthop Relat Res 2006, 447:209-213. 10.1097/01.blo.0000203481.11797.0f.
40. Opeskin K., Thomas A., Berkovic S.F. Does cardiac conduction pathology contribute to sudden unexpected death in epilepsy?. Epilepsy Res. 2000, 40(1):17-24.
41. Opherk C., Coromilas J., Hirsch L.J. Heart rate and EKG changes in 102 seizures: analysis of influencing factors. Epilepsy Res. 2002, 52(2):117-127.
42. Panicker G.K., Karnad D.R., Natekar M., Kothari S., Narula D., Lokhandwala Y. Intra- and interreader variability in QT interval measurement by tangent and threshold methods in a central electrocardiogram laboratory. J. Electrocardiol. 2009, 42(4):348-352. 10.1016/j.jelectrocard.2009.01.003.
43. Perrone B.L., Vari R.C., Kreisman N.R. Recurrent seizures alter renal function and plasma atrial natriuretic peptide levels in rats. Epilepsia 1995, 36(7):649-657.
44. Rugg-Gunn F.J., Simister R.J., Squirrell M., Holdright D.R., Duncan J.S. Cardiac arrhythmias in focal epilepsy: a prospective long-term study. Lancet 2004, 364(9452):2212-2219. 10.1016/S0140-6736(04)17594-6.
45. Sahn D.J., DeMaria A., Kisslo J., Weyman A. Recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation 1978, 58(6):1072-1083.
46. Sakamoto K., Saito T., Orman R., Koizumi K., Lazar J., Salciccioli L., Stewart M. Autonomic consequences of kainic acid-induced limbic cortical seizures in rats: peripheral autonomic nerve activity, acute cardiovascular changes, and death. Epilepsia 2008, 49(6):982-996. 10.1111/j.1528-1167.2008.01545.x.
47. Schraeder P.L., Lathers C.M. Cardiac neural discharge and epileptogenic activity in the cat: an animal model for unexplained death. Life Sci. 1983, 32(12):1371-1382.
48. Schuele S.U. Effects of seizures on cardiac function. J. Clin. Neurophysiol. 2009, 26(5):302-308. 10.1097/WNP.0b013e3181b7f13b.
49. Sevcencu C., Struijk J.J. Autonomic alterations and cardiac changes in epilepsy. Epilepsia 2010, 51(5):725-737. 10.1111/j.1528-1167.2009.02479.x.
50. Seyal M., Pascual F., Lee C.Y., Li C.S., Bateman L.M. Seizure-related cardiac repolarization abnormalities are associated with ictal hypoxemia. Epilepsia 2011, 52(11):2105-2111. 10.1111/j.1528-1167.2011.03262.x.
51. Shinbane J.S., Wood M.A., Jensen D.N., Ellenbogen K.A., Fitzpatrick A.P., Scheinman M.M. Tachycardia-induced cardiomyopathy: a review of animal models and clinical studies. J. Am. Coll. Cardiol. 1997, 29(4):709-715.
52. Shorvon S., Tomson T. Sudden unexpected death in epilepsy. Lancet 2011, 378(9808):2028-2038. 10.1016/S0140-6736(11)60176-1.
53. Stewart M. The urethane/kainate seizure model as a tool to explore physiology and death associated with seizures. Sudden Death in Epilepsy: Forensic and Clinical Issues 2011, 627-644. CRC Press, Boca Raton, FL. C. Lathers, P.L. Schraeder, M.W. Bungo, J.E. Leetsma (Eds.).
54. Surges R., Taggart P., Sander J.W., Walker M.C. Too long or too short? New insights into abnormal cardiac repolarization in people with chronic epilepsy and its potential role in sudden unexpected death. Epilepsia 2010, 51(5):738-744. 10.1111/j.1528-1167.2010.02571.x.
55. Tavernor S.J., Brown S.W., Tavernor R.M., Gifford C. Electrocardiograph QT lengthening associated with epileptiform EEG discharges - a role in sudden unexplained death in epilepsy?. Seizure 1996, 5(1):79-83.
56. Thayer J.F., Yamamoto S.S., Brosschot J.F. The relationship of autonomic imbalance, heart rate variability and cardiovascular disease risk factors. Int. J. Cardiol. 2010, 141(2):122-131. 10.1016/j.ijcard.2009.09.543.
57. Tigaran S., Molgaard H., McClelland R., Dam M., Jaffe A.S. Evidence of cardiac ischemia during seizures in drug refractory epilepsy patients. Neurology 2003, 60(3):492-495.
58. Tigaran S., Rasmussen V., Dam M., Pedersen S., Hogenhaven H., Friberg B. ECG changes in epilepsy patients. Acta Neurol. Scand. 1997, 96(2):72-75.
59. Towfighi J., Housman C., Mauger D., Vannucci R.C. Effect of seizures on cerebral hypoxic-ischemic lesions in immature rats. Brain Res Dev. Brain Res. 1999, 113(1/2):83-95.
60. Walton N.Y., Rubinstein B.K., Treiman D.M. Cardiac hypertrophy secondary to status epilepticus in the rat. Epilepsy Res. 1995, 20(2):121-124.