Abstract
The term “Epilepsy” encompasses a broad spectrum of medical and social disorders that affect about 65 million people worldwide and is commonly defined as a tendency to suffer recurrent seizures. In patients with epilepsy, ictal discharges that occur in (or propagate to) the anterior cingulate, insular, posterior orbito-frontal, and the pre-frontal cortices, along with the amygdala and hypothalamus play a key role in influencing the autonomic nervous system (ANS) at the cortical level. In turn, this can result in cardiac effects which are widespread and range from subtle changes in heart rate variability (HRV) to ictal sinus arrest, and from QT-interval shortening to atrial fibrillation. In addition, cardiac events are the main hypothesized mechanisms underlying sudden unexpected death in epilepsy (SUDEP), which occurs in absence of a known structural cause. Patients with epilepsy also experience long-lasting changes in the regulation of the ANS and target organs. Heart rate (HR) and HRV can be easily measured/estimated when compared to other biomarkers that are commonly associated with seizures (i.e., long-term EEG), and are therefore potentially valuable biomarkers when it comes to characterizing seizures. In this context, a number of linear and nonlinear analysis techniques have been applied in order to detect and characterize epilepsy-related ANS changes. While the physiological and clinical applicability of nonlinear analyses like fractal and complexity measures of HR dynamics are not yet completely understood, in view of recent experimental findings it is reasonable to assume that such indices highlight abnormal patterns of RR interval behaviour that are not easily detected by commonly used moment statistics of HR variation. These findings may provide new insight regarding physiological and seizure-induced states of the complex brain-heart network underlying epilepsy and related autonomic modifications. A better understanding of the autonomic manifestations of seizures would provide practical added value to clinical epileptologists dealing with differential diagnosis of epilepsy and related disorders, as well as aiding in designing more sensitive seizure detection and prediction algorithms.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Ngugi, A.K., et al.: Estimation of the burden of active and life-time epilepsy: a meta-analytic approach. Epilepsia. 51(5), 883–890 (2010)
Berg, A.T., et al.: Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology, 2005–2009. Epilepsia. 51(4), 676–685 (2010)
Eggleston, K.S., Olin, B.D., Fisher, R.S.: Ictal tachycardia: the head-heart connection. Seizure. 23(7), 496–505 (2014)
Sevcencu, C., Struijk, J.J.: Autonomic alterations and cardiac changes in epilepsy. Epilepsia. 51(5), 725–737 (2010)
Nashef, L., et al.: Unifying the definitions of sudden unexpected death in epilepsy. Epilepsia. 53(2), 227–233 (2012)
Devinsky, O.: Effects of seizures on autonomic and cardiovascular function. Epilepsy Curr. 4(2), 43–46 (2004)
Sperling, M.R.: Sudden unexplained death in epilepsy. Epilepsy Curr. 1(1), 21–23 (2001)
Scorza, F.A., et al.: The brain-heart connection: implications for understanding sudden unexpected death in epilepsy. Cardiol. J. 16(5), 394–399 (2009)
Jansen, K., Lagae, L.: Cardiac changes in epilepsy. Seizure. 19(8), 455–460 (2010)
Jeppesen, J., et al.: Heart rate variability analysis indicates preictal parasympathetic overdrive preceding seizure-induced cardiac dysrhythmias leading to sudden unexpected death in a patient with epilepsy. Epilepsia. 55(7), e67–e71 (2014)
Surges, R., Jordan, A., Elger, C.E.: Ictal modulation of cardiac repolarization, but not of heart rate, is lateralized in mesial temporal lobe epilepsy. PLoS One. 8(5), e64765 (2013)
Romigi, A., et al.: Heart rate variability in untreated newly diagnosed temporal lobe epilepsy: evidence for ictal sympathetic dysregulation. Epilepsia. 57(3), 418–426 (2016)
Shorvon, S., Tomson, T.: Sudden unexpected death in epilepsy. Lancet. 378(9808), 2028–2038 (2011)
Porges, S.W.: The polyvagal theory: phylogenetic substrates of a social nervous system. Int. J. Psychophysiol. 42(2), 123–146 (2001)
Russell, A.E.: The pathology of epilepsy. Proc. R. Soc. Med. 1(Med Sect), 72–118 (1908)
van der Lende, M., et al.: Cardiac arrhythmias during or after epileptic seizures. J. Neurol. Neurosurg. Psychiatry. 87(1), 69–74 (2016)
Pool, J.L., Ransohoff, J.: Autonomic effects on stimulating rostral portion of cingulate gyri in man. J. Neurophysiol. 12(6), 385–392 (1949)
Oppenheimer, S.M., et al.: Cardiovascular effects of human insular cortex stimulation. Neurology. 42(9), 1727–1732 (1992)
Altenmuller, D.M., Zehender, M., Schulze-Bonhage, A.: High-grade atrioventricular block triggered by spontaneous and stimulation-induced epileptic activity in the left temporal lobe. Epilepsia. 45(12), 1640–1644 (2004)
Leung, H., Kwan, P., Elger, C.E.: Finding the missing link between ictal bradyarrhythmia, ictal asystole, and sudden unexpected death in epilepsy. Epilepsy Behav. 9(1), 19–30 (2006)
Moseley, B., et al.: Autonomic epileptic seizures, autonomic effects of seizures, and SUDEP. Epilepsy Behav. 26(3), 375–385 (2013)
Doyle, O.M., et al.: Heart rate based automatic seizure detection in the newborn. Med. Eng. Phys. 32(8), 829–839 (2010)
Rocamora, R., et al.: Cardiac asystole in epilepsy: clinical and neurophysiologic features. Epilepsia. 44(2), 179–185 (2003)
Schuele, S.U., et al.: Video-electrographic and clinical features in patients with ictal asystole. Neurology. 69(5), 434–441 (2007)
Tinuper, P., et al.: Ictal bradycardia in partial epileptic seizures: autonomic investigation in three cases and literature review. Brain. 124(Pt 12), 2361–2371 (2001)
Moseley, B.D., et al.: The treatment of ictal asystole with cardiac pacing. Epilepsia. 52(4), e16–e19 (2011)
Adjei, P., et al.: Do subclinical electrographic seizure patterns affect heart rate and its variability? Epilepsy Res. 87(2–3), 281–285 (2009)
Di Gennaro, G., et al.: Ictal heart rate increase precedes EEG discharge in drug-resistant mesial temporal lobe seizures. Clin. Neurophysiol. 115(5), 1169–1177 (2004)
Jeppesen, J., et al.: Detection of epileptic-seizures by means of power spectrum analysis of heart rate variability: a pilot study. Technol. Health Care. 18(6), 417–426 (2010)
Massetani, R., et al.: Alteration of cardiac function in patients with temporal lobe epilepsy: different roles of EEG-ECG monitoring and spectral analysis of RR variability. Epilepsia. 38(3), 363–369 (1997)
Toth, V., et al.: Periictal heart rate variability analysis suggests long-term postictal autonomic disturbance in epilepsy. Eur. J. Neurol. 17(6), 780–787 (2010)
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. 17(3), 354–381 (1996)
Blumhardt, L.D., Smith, P.E., Owen, L.: Electrocardiographic accompaniments of temporal lobe epileptic seizures. Lancet. 1(8489), 1051–1056 (1986)
Evrengul, H., et al.: Time and frequency domain analyses of heart rate variability in patients with epilepsy. Epilepsy Res. 63(2–3), 131–139 (2005)
Harnod, T., et al.: Heart rate variability in children with refractory generalized epilepsy. Seizure. 17(4), 297–301 (2008)
Isojarvi, J.I., et al.: Interictal cardiovascular autonomic responses in patients with epilepsy. Epilepsia. 39(4), 420–426 (1998)
Tomson, T., et al.: Heart rate variability in patients with epilepsy. Epilepsy Res. 30(1), 77–83 (1998)
Ansakorpi, H., et al.: Heart rate dynamics in refractory and well controlled temporal lobe epilepsy. J. Neurol. Neurosurg. Psychiatry. 72(1), 26–30 (2002)
El-Sayed, H.L., et al.: Non-invasive assessment of cardioregulatory autonomic functions in children with epilepsy. Acta Neurol. Scand. 115(6), 377–384 (2007)
Dutsch, M., Hilz, M.J., Devinsky, O.: Impaired baroreflex function in temporal lobe epilepsy. J. Neurol. 253(10), 1300–1308 (2006)
Devinsky, O., Perrine, K., Theodore, W.H.: Interictal autonomic nervous system function in patients with epilepsy. Epilepsia. 35(1), 199–204 (1994)
Ferri, R., et al.: Heart rate variability during sleep in children with partial epilepsy. J. Sleep Res. 11(2), 153–160 (2002)
Ronkainen, E., et al.: Suppressed circadian heart rate dynamics in temporal lobe epilepsy. J. Neurol. Neurosurg. Psychiatry. 76(10), 1382–1386 (2005)
Persson, H., et al.: Circadian variation in heart-rate variability in localization-related epilepsy. Epilepsia. 48(5), 917–922 (2007)
Persson, H., Ericson, M., Tomson, T.: Heart rate variability in patients with untreated epilepsy. Seizure. 16(6), 504–508 (2007)
Mativo, P., et al.: Study of cardiac autonomic function in drug-naive, newly diagnosed epilepsy patients. Epileptic Disord. 12(3), 212–216 (2010)
Nilsson, L., et al.: Risk factors for sudden unexpected death in epilepsy: a case-control study. Lancet. 353(9156), 888–893 (1999)
Langan, Y., Nashef, L., Sander, J.W.: Case-control study of SUDEP. Neurology. 64(7), 1131–1133 (2005)
Sander, J.W.: The natural history of epilepsy in the era of new antiepileptic drugs and surgical treatment. Epilepsia. 44(Suppl 1), 17–20 (2003)
Colugnati, D.B., et al.: Carbamazepine does not alter the intrinsic cardiac function in rats with epilepsy. Arq. Neuropsiquiatr. 68(4), 573–578 (2010)
Lotufo, P.A., et al.: A systematic review and meta-analysis of heart rate variability in epilepsy and antiepileptic drugs. Epilepsia. 53(2), 272–282 (2012)
Surges, R., et al.: Sudden unexpected death in epilepsy: risk factors and potential pathomechanisms. Nat. Rev. Neurol. 5(9), 492–504 (2009)
Hesdorffer, D.C., Tomson, T.: Adjunctive antiepileptic drug therapy and prevention of SUDEP. Lancet Neurol. 10(11), 948–949 (2011)
Kenneback, G., et al.: Electrophysiologic effects and clinical hazards of carbamazepine treatment for neurologic disorders in patients with abnormalities of the cardiac conduction system. Am. Heart J. 121(5), 1421–1429 (1991)
Kasarskis, E.J., et al.: Carbamazepine-induced cardiac dysfunction. Characterization of two distinct clinical syndromes. Arch. Intern. Med. 152(1), 186–191 (1992)
Persson, H., Ericson, M., Tomson, T.: Carbamazepine affects autonomic cardiac control in patients with newly diagnosed epilepsy. Epilepsy Res. 57(1), 69–75 (2003)
Tomson, T., Kenneback, G.: Arrhythmia, heart rate variability, and antiepileptic drugs. Epilepsia. 38(11 Suppl), S48–S51 (1997)
Hallioglu, O., et al.: Effects of antiepileptic drug therapy on heart rate variability in children with epilepsy. Epilepsy Res. 79(1), 49–54 (2008)
Tomson, T., Nashef, L., Ryvlin, P.: Sudden unexpected death in epilepsy: current knowledge and future directions. Lancet Neurol. 7(11), 1021–1031 (2008)
Ryvlin, P., Montavont, A., Kahane, P.: Sudden unexpected death in epilepsy: from mechanisms to prevention. Curr. Opin. Neurol. 19(2), 194–199 (2006)
Toichi, M., et al.: A new method of assessing cardiac autonomic function and its comparison with spectral analysis and coefficient of variation of R-R interval. J. Auton. Nerv. Syst. 62(1–2), 79–84 (1997)
Ponnusamy, A., Marques, J.L., Reuber, M.: Comparison of heart rate variability parameters during complex partial seizures and psychogenic nonepileptic seizures. Epilepsia. 53(8), 1314–1321 (2012)
Jeppesen, J., et al.: Comparing maximum autonomic activity of psychogenic non-epileptic seizures and epileptic seizures using heart rate variability. Seizure. 37, 13–19 (2016)
Craig, A.D.: Forebrain emotional asymmetry: a neuroanatomical basis? Trends Cogn. Sci. 9(12), 566–571 (2005)
Thayer, J.F., Lane, R.D.: Claude Bernard and the heart-brain connection: further elaboration of a model of neurovisceral integration. Neurosci. Biobehav. Rev. 33(2), 81–88 (2009)
Guo, C.C., et al.: Dominant hemisphere lateralization of cortical parasympathetic control as revealed by frontotemporal dementia. Proc. Natl. Acad. Sci. U. S. A. 113(17), E2430–E2439 (2016)
Vanderlei, L.C., et al.: Basic notions of heart rate variability and its clinical applicability. Rev. Bras. Cir. Cardiovasc. 24(2), 205–217 (2009)
Pincus, S.M., Viscarello, R.R.: Approximate entropy: a regularity measure for fetal heart rate analysis. Obstet. Gynecol. 79(2), 249–255 (1992)
Fleisher, L.A., Pincus, S.M., Rosenbaum, S.H.: Approximate entropy of heart rate as a correlate of postoperative ventricular dysfunction. Anesthesiology. 78(4), 683–692 (1993)
Sugihara, G., et al.: Detecting causality in complex ecosystems. Science. 338(6106), 496–500 (2012)
Schiecke, K., et al.: Nonlinear directed interactions between heart rate variability and EEG activity in children with temporal lobe epilepsy. I.E.E.E. Trans. Biomed. Eng. 63(12), 2497–2504 (2016)
Barbieri, R., et al: Lower instantaneous entropy of heartbeat dynamics during seizures in untreated temporal lobe epilepsy. In: 2015 Computing in Cardiology Conference (CinC). (2015).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG
About this chapter
Cite this chapter
Romigi, A., Toschi, N. (2017). Cardiac Autonomic Changes in Epilepsy. In: Barbieri, R., Scilingo, E., Valenza, G. (eds) Complexity and Nonlinearity in Cardiovascular Signals. Springer, Cham. https://doi.org/10.1007/978-3-319-58709-7_14
Download citation
DOI: https://doi.org/10.1007/978-3-319-58709-7_14
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-58708-0
Online ISBN: 978-3-319-58709-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)