THE IMPACT OF EPILEPTIC SEIZURES ON THE HEART RHYTHM AND CONDUCTION: A REVIEW ARTICLE
Abstract
Epileptic seizures affect the heart function and can provoke heart rhythm abnormalities and conduction disorders. Dysfunctions of the supra-segmental vegetative structures are thought to play a significant role in the development of arrhythmic syndrome in epilepsy. The asymmetric influence of the left and right cerebral hemispheres on the heart rate, the impact of antiepileptic drugs and other factors on the heart rhythm are still under discussion. The role of heart rhythm abnormalities in the pathogenesis of sudden unexplained death in epilepsy is also reviewed here. We analyze the pathogenesis of cardiac arrhythmias in epilepsy, the occurrence and risk factors, the types of disorders, the role of antiepileptic therapy and the significance of cardiac arrhythmias for the development of sudden death in patients with epilepsy (SUDEP).
About the Authors
Yu. V. RublevaRussian Federation
Rubleva Yulia Vladimirovna – Postgraduate MD, the Pirogov Russian National Medical University.
Ul. Ostrovityanova, 1, Moscow, 117997
M. B. Mironov
Russian Federation
Mironov Mikhail Borisovich – MD, PhD, Associate Prof. at the Department of clinical physiology and functional diagnostics.
Volokolamskoe s., 91, Moscow, 125371
T. M. Krasilshchikova
Russian Federation
Krasil’shchikova Tat’yana Mikhailovna – MD, Assistant professor of neurology, neurosurgery and medical genetics, Faculty of Pediatrics.
Ul. Ostrovityanova, 1, Moscow, 117997
S. G. Burd
Russian Federation
Burd Sergei Georgievich – MD, Professor of neurology, neurosurgery and medical genetics, Faculty of Medicine.
Ul. Ostrovityanova, 1, Moscow, 117997
References
1. Karlov V.A., Petrukhin A.S. Zhurnal nevrologii i psikhiatrii imeni S.S. Korsakova (in Russian). 2002; 9: 9-13.
2. Karlov V.A. Zhurnal nevrologii i psikhiatrii imeni S.S. Korsakova. 2012; 5 108-113.
3. Nozdrachev A.D., Kotel’nikov S.A., Mazhora Yu.P., Naumov K.M. Fiziologiya cheloveka (in Russian). 2005; 31 (2): 116-129.
4. Eddy M., Hugh E. Rickards, Andrea E. The cognitive impact of antiepileptic drugs. Ther Adv Neurol Disord. 2011; 4 (6): 385-407.
5. Kenneback G., Ericson M., Tomson T. et al. Changes in arrhythmia profile and heart rate variability during abrupt withdrawal of antiepileptic drugs. Implications for sudden death. Seizure. 1997; 6: 369-75.
6. Altenmuller D.M., Zehender M., SchulzeBonhage A. High-grade atrioventricular block triggered by spontaneous and stimulationinduced epileptic activity in the left temporal lobe. Epilepsia. 2004; 45: 1640-4.
7. Nei M., Ho R. T., bou-Khalil B.W. et al. EEG and ECG in sudden unexplained death in epilepsy. Epilepsia 2004; 45: 338-45.
8. Shprakh V.V., Sin’kov A.V., Sin’kova G.M. Zhurnal nevrologii i psikhiatrii imeni S.S. Korsakova (in Russian). 2000; 9: 16-20.
9. Drake M. E., Andrews J.M., Castleberry C.M. Electrophysiologic assessment of autonomic function in epilepsy. Seizure. 1998; 7 (2): 91-96.
10. Antyuf’ev V.F., Guzovskii E.V., Myakotnykh V.S. Kardiologiya (in Russian). 1992; 4: 17-20.
11. Persson H., Ericson M., Tomson T. Heart rate variability in patients with untreated epilepsy. Seizure. 2007; 16: 504-08.
12. Mamalyga M. L. Application of innovative technologies in the study of cerebral mechanisms of regulation of the cardiovascular system: Scientific and educational-methodical recommendations [Primenenie innovatsionnykh tekhnologii pri izuchenii tserebral’nykh mekhanizmov regulyatsii serdechno-sosudistoi sistemy: Nauchnye i uchebno-metodicheskie rekomendatsii (in Russian)]. 2015; 9-11.
13. Wiersma A., Bohus B., Koolhaas J.M. Corticotropin-releasing hormone microinfusion in the central amygdala diminishes a cardiac parasympathetic outflow under stressfree conditions. Brain. Res. 1993; 625 (2): 219-227.
14. Kitazawa T., Asakawa K. M3 muscarinic receptors mediate positive inotropic responses in mouse atria: a study with muscarinic receptor knockout mice. J Pharmacol Exp Ther. 2009; 487-93.
15. Ganzinelli S., Joensen L., Borda E., Bernabeo G., Sterin-Borda L. Mechanisms involved in the regulation of mRNA for M2 muscarinic acetylcholine receptors and endothelial and neuronal NO synthases in rat atria. Br J Pharmacol. 2007; 151: 175-185.
16. Skok V. I. Physiology of vegetative ganglia [Fiziologiya vegetativnykh gangliev (in Russian)]. Leningrad. 1970; 235 s.
17. Skok V. I. Structure and physiological properties of neurons of sympathetic ganglia. The natural activity of vegetative ganglia [Stroenie i fiziologicheskie svoistva neironov simpaticheskikh gangliev. Estestvennaya aktivnost’ vegetativnykh gangliev (in Russian)]. Kiev. 1989; 21-23.
18. Lathrop D.A., Spooner P.M. On the neural connection. J Cardiovasc Electrophysiol. 2001; 12: 841-4.
19. Kukanova B., Mravec B. Complex interacardiac nervous system. Bratisl Lek Listy. 2006; 107 (3): 45-51.
20. Thompson G.W., Collier K., Ardell J. L., Kember G., Armour J.A. Functional interdependence of neurons in a single canine intrinsic cardiac ganglionated plexus. J. Physiol. 2000; 528: 561-571
21. Gray A. L., Johnson T.A., Ardell J. L., and Massari V. J. Parasympathetic control of the heart. II. A novel interganglionic intrinsic cardiac circuit mediates neural control of heart rate. J. Appl Physiol. 2004; 96: 2273-2278.
22. Levi M.N., Martin P. Yu. Neurohumoral regulation of the heart. Physiology and pathophysiology of the heart. In 2 tons. Trans. with English. Ed. N. Sperelakis. 2 nd ed. [Neirogumoral’naya regulyatsiya raboty serdtsa. Fiziologiya i patofiziologiya serdtsa. V 2 t. Per. s angl. Pod red. N. Sperelakisa. 2-e izd. (in Russian)]. Moscow. 1990; 2: 64-90.
23. Nagai M., Hoshide S., Kario K. The insular cortex and cardiovascular system: a new insight into the brain-heart axis. J Am Soc Hypertens. 2010 Jul-Aug; 4 (4): 174-82.
24. Jansen K., Lagae L. Cardiac changes in epilepsy. Seizure. October 2010; 19 (8): 455-460.
25. Oppenheimer S.M., Cechetto D. F. Cardiac chronotropic organization of the rat insular cortex. Brain Res. 1990; 533: 66-72.
26. Oppenheimer S.M., Gelb A., Girvin J.P. et al. Cardiovascular effects of human insular cortex stimulation. Neurology. 1992; 42: 1727-32.
27. Oppenheimer S.M., Saleh T., Cechetto D. F. Lateral hypothalamic area neurotransmission and neuromodulation of the specific cardiac effects of insular cortex stimulation. Brain Res. 1992; 581: 133-42.
28. Ostrowsky K., M. Maglin, P. Ryvlin, J. Isnard, M. Guenot, F. Mauguière Representation of pain and somatic sensation in the human insula: a study of responses to direct electrical cortical stimulation. Cerebral Cortex. 2002; 12 (4): 376-385.
29. Rugg-Gunn F.J., Simister R. J., Squirrell M. et al. Cardiac arrhythmias in focal epilepsy: a prospective long-term study. Lancet. 2004; 364: 2212-19.
30. Zijlmans M., Flanagan D., Gotman J. Heart rate changes and ECG abnormalities during epileptic seizures: prevalence and definition of an objective clinical sign. Epilepsia. 2002; 43: 847-54.
31. Surges R. et al. Sudden unexpected death in epilepsy: risk factors and potential pathomechanisms. Macmillan Publishers Limited. 2009; 5: 492-504.
32. Gennaro G. Di, Quarato P., Sebastiano F. Ictal heart rate increase precedes EEG discharge in drug-resistant mesial temporal lobe seizures. Clinical Neurophysiology. 2004; 115: 1169-1177.
33. Massetani R., Strata G., Galli R. et al. Alteration of cardiac function in patients with temporal lobe epilepsy: different role of EEG-ECG monitoring and spectral analysis of RR variability. Epilepsia. 1997; 38 (3): 363-369.
34. Epstein M.A., M.R. Sperling, M.J. O’Connor Cardiac rhythm during temporal lobe seizures. Epilepsia. 2009; 50 (4): 760-775.
35. Freeman R. Cardiovascular manifestations of autonomic epilepsy. Clinical Autonomic Research. 2006; 16: 12-17.
36. Espinosa P.S., Lee J.W., Tedrow U.B. et al. Sudden unexpected near death in epilepsy: malignant arrhythmia from a partial seizure. Neurology. 2009; 72: 1702-03.
37. Leutmezer F., Schernthaner C., Lurger S. et al. Electrocardiographic changes at the onset of epileptic seizures. Epilepsia. 2003; 44: 348-54.
38. Tinuper P., Bisulli F., Cerullo A. et al. Ictal bradycardia in partial epileptic seizures: autonomic investigation in three cases and literature review. Brain. 2001; 124: 2361-71.
39. Rocamora R., Kurthen M., Lickfett L. et al. Cardiac asystole in epilepsy: clinical and neurophysiologic features. Epilepsia. 2003; 44: 179-85.
40. Britton J.W., Ghearing G.R., Benarroch E. E. et al. The ictal bradycardia syndrome: localization and lateralization. Epilepsia. 2006; 47: 737-44.
41. Rossetti A.O., Dworetzky B.A., Madsen J.R. et al. Ictal asystole with convulsive syncope mimicking secondary generalisation: a depth electrode study. J Neurol Neurosurg Psychiatry. 2005; 76: 885-7.
42. Schuele S.U., Bermeo A.C., Alexopoulos A.V., Locatelli E.R., Burgess R.C., Dinner D.S. et al. Videoelectrographic and clinical features in patients with ictal asystole. Neurology. 2007; 69: 434-441.
43. Keilson M. J., Hauser W.A., Magrill J.P., Goldman M. ECG abnormalities in patients with epilepsy. Neurology. 1987; 37: 1624-1626.
44. Petkar S., Cooper P., Fitzpatrick A. High incidence of ECG abnormalities in severe epilepsy. World Congress of Cardiology. 2006; 1335.
45. Nei M., Sperling M.R., Mintzer S., Ho R. T. Long-term cardiac rhythm and repolarization abnormalities in refractory focal and generalized epilepsy. Epilepsia. 2012 Aug; 53 (8): e137-40. DOI: 10.1111/j.1528-1167.2012.03561.x. Epub 2012 Jun 18.
46. Lathers C.M., Schraeder P. L., Weiner F. L. Synchronization of cardiac autonomic neural discharge with epileptogenic activity: the lockstep phenomenon. Electroencephalogr Clin Neurophysiol. 1987; 67: 247-59.
47. Tomson T., Ericson M., Ihrman C., Lindblad L. E. Heart rate variability in patients with epilepsy. Epilepsy Res. 1998; 30: 77-83.
48. Nashef L., Hindocha N., Makoff A. Risk factors in sudden death in epilepsy (SUDEP): the quest for mechanisms. Epilepsia. 2007; 48: 859-71.
49. Nashef L., So E. L., Ryvlin P., Tomson T. Unifying the definitions of sudden unexpected death in epilepsy. Epilepsia. 2012 Feb; 53 (2): 227-33. DOI: 10.1111/j.1528-1167.2011.03358.x. Epub 2011 Dec 22.
50. Van der Lende M., Surges R., Sander J.W., Thijs R.D. Cardiac arrhythmias during or after epileptic seizures. J Neurol Neurosurg Psychiatry. 2015 Jun 2.
51. Earnest M.P., Thomas G. E., Eden R.A., Hossack K. F. The sudden unexplained death syndrome in epilepsy: demographic, clinical, and postmortem features. Epilepsia. 1992; 33 (2): 310-6.
52. Hilz M. J., Devinsky O., Doyle W., Mauerer A., Dütsch M. Decrease of sympathetic cardiovascular modulation after temporal lobe epilepsy surgery. Brain. 2002; 125: 985-995.
53. Kovach J.A., Nearing B.D., Verrier R. L. An angerlike behavioral state potentiates myocardial ischemia-induced T-wave alternans in canines. J Am Coll Cardiol. 2001; 37: 1719-25.
54. Tavernor S. J. Electrocardiograph QT lengthening associated with epileptiform EEG discharges – a role in sudden unexplained death in epilepsy? Seizure. 1996; 5 (l): 79-83.
55. Natelson B.H., Suarez R.V., Terrence C. F. et al. Patients with epilepsy who die suddenly have cardiac disease. Arch Neurol. 1998; 55: 857-60.
56. 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: 492-495.
57. Kloster R., Engelskjon T. Sudden unexpected death in epilepsy (SUDEP): a clinical perspective and a search for risk factors. J Neurol Neurosurg Psychiatry. 1999; 67: 439-44.
58. Codrea T.S., ager-Pedersen S., Baandrup U. et al. Sudden unexpected death in epilepsy: is death by seizures a cardiac disease? Am J Forensic Med Pathol. 2005; 26: 99-105.
59. Cordero D. L., Cagin N.A., Natelson B.H. Neurocardiology update: role of the nervous system in coronary vasomotion. Cardiovasc Res. 1995; 29: 319-28.
60. Leestma J. E., Annegers J. F., Brodie M. J. et al. Sudden unexplained death in epilepsy: observations from a large clinical development program. Epilepsia. 1997; 38: 47-55.
61. Tomson T., Walczak T., Sillanpaa M. Sudden unexpected death in epilepsy: a review of incidence and risk factors. Epilepsia. 2005; 46 (11): 54-61.
62. Walczak T. Do antiepileptic drugs play a role in sudden unexpected death in epilepsy? Drug Saf. 2003; 26: 673-83.
63. Lear-Kaul K.C., Coughlin L., Dobersen M. J. Sudden unexpected death in epilepsy: a retrospective study. Am J Forensic Med Pathol. 2005; 26: 11-17.
64. Opeskin S. Berkovic Risk factors for sudden unexpected death in epilepsy: a controlled prospective study based on coroners cases. Seizure. 2003; 12: 456-464.
65. Hennessy M. J., Tighe M.G., Binnie C.D. et al. Sudden withdrawal of carbamazepine increases cardiac sympathetic activity in sleep. Neurology. 2001; 57: 1650-4.
66. Timmings P. L. sudden unexpected death in epilepsy: a local audit. Seizure. 1993; 2: 287-290.
67. Nilsson L., Bergman U., Diwan V. et al. Antiepileptic drug therapy and its management in sudden unexpected death in epilepsy: a case-control study. Epilepsia. 2001; 42: 667-73.
68. Devinsky O., Pacia S., Tatambhotla G. Bradycardia and asystole induced by partial seizures: a case report and literature review. Neurology. 1997; 48 (6): 1712-1714.
69. Tomson T., Kenneback G. Arrhythmia, heart rate variability and anti-epileptic drugs. Epilepsia. 1997; 38: 48-51.
70. Isojarvi J. I., Ansakorpi H., Suominen K. et al. Interictal cardiovascular autonomic responses in patients with epilepsy. Epilepsia. 1998; 39: 420-6.
71. Evrengul H., Tanriverdi H., Dursunoglu D. et al. Time and frequency domain analyses of heart rate variability in patients with epilepsy. Epilepsy Res. 2005; 63: 131-9.
72. Druschky A., Hilz M. J., Hopp P. et al. Interictal cardiac autonomic dysfunction in temporal lobe epilepsy demonstrated by [(123)I]metaiodobenzylguanidine-SPECT. Brain. 2001; 124: 2372-82.
73. Al A.B., Adabag A.S., Houghland M.A. et al. Brugada pattern electrocardiogram associated with supratherapeutic phenytoin levels and the risk of sudden death. Pacing Clin Electrophysiol. 2007; 30: 713-15.
74. Stollberger C., Hoftberger R., Finsterer J. Lamotrigine-trigged obstructive hypertrophic cardiomyopathy, epilepsy and metabolic myopathy. Int J Cardiol. 2009.
75. Aurlien D., Tauboll E., Gjerstad L. Lamotrigine in idiopathic epilepsy – increased risk of cardiac death? Acta Neurol Scand. 2007; 115 (3): 199-203.
76. Saetre E. et al. Cardiac function and antiepileptic drug treatment in the elderly: A comparison between lamotrigine and sustained-release carbamazepine. Epilepsia. DOI:10.1111/j.1528–11672009.02069.x.
77. Dixon R. et al. Lamotrigine does not prolong QTc in a thorough QT/QTc study in healthy subjects. Br. J. Clin. Pharmacol. 2008; 66: 396-404.
78. Cheng-Hakimian A., Anderson G.D., Miller J.W. Rufinamide: pharmacology, clinical trials, and role in clinical practice. Int. J. Clin.Pract. 2006; 60: 1497-1501.
79. Desilvey D. L., Moss, A. J. Primidone in the treatment of the long QT syndrome: QT shortening and ventricular arrhythmia suppression. Ann. Intern. Med. 1980; 93: 53-54.
80. Ishizue N., Niwano S., Saito M. et al. Polytherapy with sodium channel-blocking antiepileptic drugs is associated with arrhythmogenic ST-T abnormality in patients with epilepsy. Seizure. 2016 Aug; 40: 81-7. DOI: 10.1016/j.seizure.2016.06.004.
81. Yuen A.W. et al. erythrocyte and plasma fatty acid profiles in patients with epilepsy: does carbamazepine affect omega-3 fatty acid concentrations? Epilepsy Behav. 2008; 12: 317-323.
Review
For citations:
Rubleva Yu.V., Mironov M.B., Krasilshchikova T.M., Burd S.G. THE IMPACT OF EPILEPTIC SEIZURES ON THE HEART RHYTHM AND CONDUCTION: A REVIEW ARTICLE. Epilepsy and paroxysmal conditions. 2017;9(4):50-63. (In Russ.) https://doi.org/10.17749/2077-8333.2017.9.4.050-063

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