Research Article
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Evaluation of autonomic nervous system functions by using tilt table test and heart rate variability in epileptic children

Year 2023, Volume: 36 Issue: 1, 87 - 92, 31.01.2023
https://doi.org/10.5472/marumj.1244552

Abstract

Objective: The value of head-up tilt test (HUTT) for differential diagnosis of epilepsy and the autonomic nervous system functions in
epileptic children using heart rate variability (HRV) are studied.
Patients and Methods: The study group consisted of 16 children with idiopatic/criptogenic epilepsy and 12 controls. Heart rate, PR
interval, corrected QT (QTc) interval, QT and QTc dispersion were calculated using 12-lead electrocardiogram (ECG), HRV analysis
was performed using the Holter recordings obtained both during HUTT and throughout the day. Time domain parameters, standard
deviation of all RR intervals (SDNN), the standard deviation of mean NN intervals in five-minutes recording (SDANN), mean standard
deviation of NN intervals in five-minutes recordings (SDNNi), root mean square of successive differences (RMSSD), count divided
by the total number of all NN intervals (pNN50) and frequency domain parameters low frequency (LF), high frequency (HF), lowfrequency/
high-frequency ratio (LF/HF) were calculated in both and compared between the two groups.
Results: Head-up tilt test was positive in 4 epileptic children (25%), none of controls were positive. The heart rate of the patients were
higher than the controls (p=0.015). LF/HF ratio in 24-hour Holter recordings, were significantly lower (1.13±0.6, 1.83±0.7 respectively,
p=0.002); the SDANN during HUTT (28.7±20.2, 18.2 ± 19.9 respectively, p=0.024) were significantly higher in the patients than the
controls.
Conclusion: Head-up tilt test positivity is frequent in epileptic children, and cannot be used in differential diagnosis. HRV calculated
both from 24 hour Holter recordings and Holter recordings under orthostatic stress were impaired in favour of parasympathetic
system in epileptic children.

References

  • Goetz CG, Pappert EJ. Textbook of Clinical Neurology1st edition. Philadelphia: WB Saunders, 1999; 2: 1064-1132.
  • Bradler WG, Daroff RB, Fenichel GM, Marsden CD. Neurology in clinical practice 3th edition. Philadelphia: Elsevier, 2000; 2: 1745-1779.
  • Swaiman KF, Ashwai S, Ferriero DM. Treatment of the epilepsies. Pediatric Neurology: Principles and practice 4th edition. Philadelphia: Mosby Elsevier, 2006:1105-1151
  • Van Buren JM. Some autonomic concomitant of ictal automatism: a study of temporal lobe attacks. Brain 1958; 81: 505-28. doi:10.1093/brain//81.4.505
  • Marshall DW, Westmoreland BF, Sharbrough FW. Ictal tachycardia during temporal lobe seizures. Mayo Clin Proc 1983; 58: 443-6. PMID: 6865478.
  • Krump JE, Gerardy W. Polygraphic observations in petit mal attacks. Electroenceph Clin Neurophysiol 1959; 11: 609-10.
  • Gastaut H, Brougthon R. Epileptic seizures: clinical features and pathophysiology. Epileptic Seizures. Owerri: Springfield. 1972:25-140.
  • Myers KA, Bello-Espinosa LE, Symonds JD, et al. Heart rate variability in epilepsy: A potential biomarker of sudden unexpected death in epilepsy risk. Epilepsia 2018; 59:1372-80. doi: 10.1111/ epi.14438
  • Nei M, Ho R T, Sperling, M.R. ECG abnormalities during partial seizures in refractory epilepsy. Epilepsia 2000;41:542- 8. doi: 10.1111/j.1528-1157.2000.tb00207.x
  • Topcu B, Akalin F. The autonomic nervous system disregulation, in response to orthostatic stres in children with neurocardiogenic syncope. Cardiol Young 2010; 20: 165- 72. doi:10.1017/S104.795.1109991211
  • Bazett HC. An analysis of time relations of electrocardiograms. Heart 1920; 7:353-70.
  • Thijs RD, Brignole M, Falup-Pecurariu C, et al. Recommendations for tilt table testing and other provocative cardiovascular autonomic tests in conditions that may cause transient loss of consciousness: Consensus statement of the European Federation of Autonomic Societies (EFAS) endorsed by the American Autonomic Society (AAS) and the European Academy of Neurology (EAN) Auton Neurosci 2021;233:102792. doi: 10.1016/j.autneu.2021.102792
  • Berg AT. Epidemiology in epilepsy. Epilepsy Curr 2001;1:55. doi: 10.1046/j.1535-7597.2001.00024.x.
  • Fiest K M, Sauro K M, Samuel Wiebe S, et al. Prevalence and incidence of epilepsy. A systematic review and metaanalysis of international studies. Neurology 2017;88 :296- 303. doi:10.1212/WNL.000.000.0000003509
  • Stafstrom CE. The pathophysiology of epileptic seizures. A primer for pediatricians. Pediatr Rev1998;19:342-51. doi: 10.1542/pir.19-10-342
  • Jansen K, Varon C, Van Huffel S, Lagae L. Peri-ictal ECG changes in childhood epilepsy: Implications for detection systems. Epilepsy Behav 2013;29:72-6. doi:10.1016/j. yebeh.2013.06.030.
  • Berkowitz JB, Auld D, Hulse JE, Campbell RM. Tilt table evaluation for control pediatric patients: comparison with symptomatic patients. Clin Cardiol 1995; 18:521-5. doi:10.1002/clc.496.018.0908
  • Sutton R, Peterson M. The clinical spectrum of neurocardiogenic syncope. J Cardiovasc Electrophysiol 1995;6: 569-76. doi:10.1111/j.1540-8167.1995.tb00429.x
  • Sabri M, Mahmodian, T, Sadri H. Usefulness of the head-up tilt test in distinguishing neurally mediated syncope and epilepsy in children aged 5–20 years old. Pediatr Cardiol 2006;27:600- 3. doi:10.1007/s00246.006.1140-7
  • Akalin F, Tırtır A, Yılmaz Y. Increased QT dispersion in epileptic children. Acta Pediatr 2003;92:916-20. doi:10.1111/j.1651-2227.2003.tb00624.x
  • Walczak TS, Leppik IE, Amelio MD, et al. Incidence and risk factors in sudden unexpected death in epilepsy, a prospective cohort study. Neurology 2001;56:519-25. doi:10.1212/ WNL.56.4.519
  • Opherk C, Coromilas J, Hirsch L J. Heart rate and EKG changes in 102 seizures: analysis of influencing factors. Epilepsy Res 2002; 52: 117-27. SSN 0920-1211, doi:10.1016/ S0920-1211(02)00215-2.
  • Mazzola L, Rheims S., Ictal and ınterictal cardiac manifestations in epilepsy. A review of their relation with an altered central control of autonomic functions and with the risk of SUDEP. Front Neurol 2021; 12: 642645,. doi:10.3389/ fneur.2021.642645
  • Galimberti CA, Marchioni E, Barzizza F, Manni R, Sartori I, Tartara A. Partial epileptic seizures of different origin variably affect cardiac rhythm. Epilepsia 1996; 37:742-7. doi:10.1111/j.1528-1157.1996.tb00645.x
  • Wilder-Smith E, Wilder-Smith A. Complex partial seizures as cause of transient cardiac arrhythmia. Schweizerische Medizinische Wochenschrift 1995;125:2237-43.
  • Drake ME, Reider CR, Kay A. Electrocardiography in epilepsy patients without cardiac symptoms. Seizure 1993;2:63-5. doi:10.1016/S1059-1311(05)80104-9
  • Frysinger RC, Engel J, Harper RM. Interictal heart rate patterns in partial seizure disorders. Neurology 1993;43: 2136- 9. doi:10.1212/WNL.43.10.2136
  • Zaza A, Lombardi F. Autonomic indexes based on the analysis of heart rate variability; a view from the sinus node. Cardiovasc Res 2001;50:434-42. doi:10.1016/S0008-6363(01)00240-1
  • 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. Circulation 1996;93:1043-65.
  • Lombardi F, Huikuri H, Schmidt G, Malik M. e-rhythm study group of european heart rhythm association. short-term heart rate variability: easy to measure, difficult to interpret. heart rhythm. 2018;15:1559-60. doi: 10.1016/j.hrthm.2018.05.023.
  • Lahiri M, Kannankeril P, Goldberger J, et al. Assessment of Autonomic Function in Cardiovascular Disease. J Am Coll Cardiol. 2008 May, 51 (18) 1725–1733. doi:10.1016/j. jacc.2008.01.038
  • Singh RB, Cornelissen G, Weydahl A, et al. Circadian heart rate and blood pressure variability considered for research and patient care. Int J Cardiol 2003;87:9-28. doi:10.1016/S0167- 5273(02)00308-X
  • El-Sayed HL, Kotby AA, Tomoum HY, El-Hadidi ES, El Behery SE, El-Ganzory AM. Non-invasive assessment of cardioregulatory autonomic functions in children with epilepsy. Acta Neurol Scand 2007;115:377-84. doi: 10.1111/j.1600-0404.2006.00792.x. PMID: 17511845.
  • Perini, R., Veicsteinas, A. Heart rate variability and autonomic activity at rest and during exercise in various physiological conditions. Eur J Appl Physiol 2003; 90:317-25. doi:10.1007/ s00421.003.0953-9
  • Ferri R, Curzi-Dascalova L, Arzimanoglou A, et al. Heart rate variability during sleep in children with partial epilepsy. J Sleep Res 2002;11:153-60. doi:10.1046/j.1365-2869.2002.00283.x
  • Massetani R, Strata G, Galli R. Alteration of cardiac function in patients with temporal lobe epilepsy: different roles of EEG-ECG monitoring and spectral analysis of RR variability. Epilepsia 1997;38:363-9. doi:10.1111/j.1528-1157.1997. tb01129.x
  • Stein P K. Assessing heart rate variability from real-world Holter reports. Card Electrophysiol Rev 2002;6:239-244. doi:10.1023/A:101.637.6924850
  • Yang TF, Wong TT, Chang KP, et al. Power spectrum analysis of heart rate variability in children with epilepsy. Childs Nerv Syst 2001;17:602-6. doi: 10.1007/s003.810.100505
  • Raju KN, Choudhary N, Gulati S, et al. Comparison of heart rate variability among children with well controlled versus refractory epilepsy: A cross-sectional study. Epilepsy Res 2012;101:88-91. doi:10.1016/j.eplepsyres.2012.03.005
  • Silvetti MS, Drago F, Ragonese P. Heart rate variability in healthy children and adolescents is partially related to age and gender. İnt J Cardiol 2001;8:169 – 74 doi:10.1016/S0167- 5273(01)00537-X
  • Garavaglia L, Gulich D, Defeo MM, Mailland TJ, Irurzun IM. The effect of age on the heart rate variability of healthy subjects. PLoS ONE 2021;16: e0255894. doi:10.1371/journal. pone.0255894
Year 2023, Volume: 36 Issue: 1, 87 - 92, 31.01.2023
https://doi.org/10.5472/marumj.1244552

Abstract

References

  • Goetz CG, Pappert EJ. Textbook of Clinical Neurology1st edition. Philadelphia: WB Saunders, 1999; 2: 1064-1132.
  • Bradler WG, Daroff RB, Fenichel GM, Marsden CD. Neurology in clinical practice 3th edition. Philadelphia: Elsevier, 2000; 2: 1745-1779.
  • Swaiman KF, Ashwai S, Ferriero DM. Treatment of the epilepsies. Pediatric Neurology: Principles and practice 4th edition. Philadelphia: Mosby Elsevier, 2006:1105-1151
  • Van Buren JM. Some autonomic concomitant of ictal automatism: a study of temporal lobe attacks. Brain 1958; 81: 505-28. doi:10.1093/brain//81.4.505
  • Marshall DW, Westmoreland BF, Sharbrough FW. Ictal tachycardia during temporal lobe seizures. Mayo Clin Proc 1983; 58: 443-6. PMID: 6865478.
  • Krump JE, Gerardy W. Polygraphic observations in petit mal attacks. Electroenceph Clin Neurophysiol 1959; 11: 609-10.
  • Gastaut H, Brougthon R. Epileptic seizures: clinical features and pathophysiology. Epileptic Seizures. Owerri: Springfield. 1972:25-140.
  • Myers KA, Bello-Espinosa LE, Symonds JD, et al. Heart rate variability in epilepsy: A potential biomarker of sudden unexpected death in epilepsy risk. Epilepsia 2018; 59:1372-80. doi: 10.1111/ epi.14438
  • Nei M, Ho R T, Sperling, M.R. ECG abnormalities during partial seizures in refractory epilepsy. Epilepsia 2000;41:542- 8. doi: 10.1111/j.1528-1157.2000.tb00207.x
  • Topcu B, Akalin F. The autonomic nervous system disregulation, in response to orthostatic stres in children with neurocardiogenic syncope. Cardiol Young 2010; 20: 165- 72. doi:10.1017/S104.795.1109991211
  • Bazett HC. An analysis of time relations of electrocardiograms. Heart 1920; 7:353-70.
  • Thijs RD, Brignole M, Falup-Pecurariu C, et al. Recommendations for tilt table testing and other provocative cardiovascular autonomic tests in conditions that may cause transient loss of consciousness: Consensus statement of the European Federation of Autonomic Societies (EFAS) endorsed by the American Autonomic Society (AAS) and the European Academy of Neurology (EAN) Auton Neurosci 2021;233:102792. doi: 10.1016/j.autneu.2021.102792
  • Berg AT. Epidemiology in epilepsy. Epilepsy Curr 2001;1:55. doi: 10.1046/j.1535-7597.2001.00024.x.
  • Fiest K M, Sauro K M, Samuel Wiebe S, et al. Prevalence and incidence of epilepsy. A systematic review and metaanalysis of international studies. Neurology 2017;88 :296- 303. doi:10.1212/WNL.000.000.0000003509
  • Stafstrom CE. The pathophysiology of epileptic seizures. A primer for pediatricians. Pediatr Rev1998;19:342-51. doi: 10.1542/pir.19-10-342
  • Jansen K, Varon C, Van Huffel S, Lagae L. Peri-ictal ECG changes in childhood epilepsy: Implications for detection systems. Epilepsy Behav 2013;29:72-6. doi:10.1016/j. yebeh.2013.06.030.
  • Berkowitz JB, Auld D, Hulse JE, Campbell RM. Tilt table evaluation for control pediatric patients: comparison with symptomatic patients. Clin Cardiol 1995; 18:521-5. doi:10.1002/clc.496.018.0908
  • Sutton R, Peterson M. The clinical spectrum of neurocardiogenic syncope. J Cardiovasc Electrophysiol 1995;6: 569-76. doi:10.1111/j.1540-8167.1995.tb00429.x
  • Sabri M, Mahmodian, T, Sadri H. Usefulness of the head-up tilt test in distinguishing neurally mediated syncope and epilepsy in children aged 5–20 years old. Pediatr Cardiol 2006;27:600- 3. doi:10.1007/s00246.006.1140-7
  • Akalin F, Tırtır A, Yılmaz Y. Increased QT dispersion in epileptic children. Acta Pediatr 2003;92:916-20. doi:10.1111/j.1651-2227.2003.tb00624.x
  • Walczak TS, Leppik IE, Amelio MD, et al. Incidence and risk factors in sudden unexpected death in epilepsy, a prospective cohort study. Neurology 2001;56:519-25. doi:10.1212/ WNL.56.4.519
  • Opherk C, Coromilas J, Hirsch L J. Heart rate and EKG changes in 102 seizures: analysis of influencing factors. Epilepsy Res 2002; 52: 117-27. SSN 0920-1211, doi:10.1016/ S0920-1211(02)00215-2.
  • Mazzola L, Rheims S., Ictal and ınterictal cardiac manifestations in epilepsy. A review of their relation with an altered central control of autonomic functions and with the risk of SUDEP. Front Neurol 2021; 12: 642645,. doi:10.3389/ fneur.2021.642645
  • Galimberti CA, Marchioni E, Barzizza F, Manni R, Sartori I, Tartara A. Partial epileptic seizures of different origin variably affect cardiac rhythm. Epilepsia 1996; 37:742-7. doi:10.1111/j.1528-1157.1996.tb00645.x
  • Wilder-Smith E, Wilder-Smith A. Complex partial seizures as cause of transient cardiac arrhythmia. Schweizerische Medizinische Wochenschrift 1995;125:2237-43.
  • Drake ME, Reider CR, Kay A. Electrocardiography in epilepsy patients without cardiac symptoms. Seizure 1993;2:63-5. doi:10.1016/S1059-1311(05)80104-9
  • Frysinger RC, Engel J, Harper RM. Interictal heart rate patterns in partial seizure disorders. Neurology 1993;43: 2136- 9. doi:10.1212/WNL.43.10.2136
  • Zaza A, Lombardi F. Autonomic indexes based on the analysis of heart rate variability; a view from the sinus node. Cardiovasc Res 2001;50:434-42. doi:10.1016/S0008-6363(01)00240-1
  • 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. Circulation 1996;93:1043-65.
  • Lombardi F, Huikuri H, Schmidt G, Malik M. e-rhythm study group of european heart rhythm association. short-term heart rate variability: easy to measure, difficult to interpret. heart rhythm. 2018;15:1559-60. doi: 10.1016/j.hrthm.2018.05.023.
  • Lahiri M, Kannankeril P, Goldberger J, et al. Assessment of Autonomic Function in Cardiovascular Disease. J Am Coll Cardiol. 2008 May, 51 (18) 1725–1733. doi:10.1016/j. jacc.2008.01.038
  • Singh RB, Cornelissen G, Weydahl A, et al. Circadian heart rate and blood pressure variability considered for research and patient care. Int J Cardiol 2003;87:9-28. doi:10.1016/S0167- 5273(02)00308-X
  • El-Sayed HL, Kotby AA, Tomoum HY, El-Hadidi ES, El Behery SE, El-Ganzory AM. Non-invasive assessment of cardioregulatory autonomic functions in children with epilepsy. Acta Neurol Scand 2007;115:377-84. doi: 10.1111/j.1600-0404.2006.00792.x. PMID: 17511845.
  • Perini, R., Veicsteinas, A. Heart rate variability and autonomic activity at rest and during exercise in various physiological conditions. Eur J Appl Physiol 2003; 90:317-25. doi:10.1007/ s00421.003.0953-9
  • Ferri R, Curzi-Dascalova L, Arzimanoglou A, et al. Heart rate variability during sleep in children with partial epilepsy. J Sleep Res 2002;11:153-60. doi:10.1046/j.1365-2869.2002.00283.x
  • Massetani R, Strata G, Galli R. Alteration of cardiac function in patients with temporal lobe epilepsy: different roles of EEG-ECG monitoring and spectral analysis of RR variability. Epilepsia 1997;38:363-9. doi:10.1111/j.1528-1157.1997. tb01129.x
  • Stein P K. Assessing heart rate variability from real-world Holter reports. Card Electrophysiol Rev 2002;6:239-244. doi:10.1023/A:101.637.6924850
  • Yang TF, Wong TT, Chang KP, et al. Power spectrum analysis of heart rate variability in children with epilepsy. Childs Nerv Syst 2001;17:602-6. doi: 10.1007/s003.810.100505
  • Raju KN, Choudhary N, Gulati S, et al. Comparison of heart rate variability among children with well controlled versus refractory epilepsy: A cross-sectional study. Epilepsy Res 2012;101:88-91. doi:10.1016/j.eplepsyres.2012.03.005
  • Silvetti MS, Drago F, Ragonese P. Heart rate variability in healthy children and adolescents is partially related to age and gender. İnt J Cardiol 2001;8:169 – 74 doi:10.1016/S0167- 5273(01)00537-X
  • Garavaglia L, Gulich D, Defeo MM, Mailland TJ, Irurzun IM. The effect of age on the heart rate variability of healthy subjects. PLoS ONE 2021;16: e0255894. doi:10.1371/journal. pone.0255894
There are 41 citations in total.

Details

Primary Language English
Subjects Clinical Sciences
Journal Section Original Research
Authors

Azad Redjepov This is me 0000-0002-7448-3004

Sinem Altunyuva Usta This is me 0000-0002-6779-0698

Yuksel Yılmaz This is me 0000-0002-5863-1265

Figen Akalın This is me 0000-0003-3836-3117

Publication Date January 31, 2023
Published in Issue Year 2023 Volume: 36 Issue: 1

Cite

APA Redjepov, A., Altunyuva Usta, S., Yılmaz, Y., Akalın, F. (2023). Evaluation of autonomic nervous system functions by using tilt table test and heart rate variability in epileptic children. Marmara Medical Journal, 36(1), 87-92. https://doi.org/10.5472/marumj.1244552
AMA Redjepov A, Altunyuva Usta S, Yılmaz Y, Akalın F. Evaluation of autonomic nervous system functions by using tilt table test and heart rate variability in epileptic children. Marmara Med J. January 2023;36(1):87-92. doi:10.5472/marumj.1244552
Chicago Redjepov, Azad, Sinem Altunyuva Usta, Yuksel Yılmaz, and Figen Akalın. “Evaluation of Autonomic Nervous System Functions by Using Tilt Table Test and Heart Rate Variability in Epileptic Children”. Marmara Medical Journal 36, no. 1 (January 2023): 87-92. https://doi.org/10.5472/marumj.1244552.
EndNote Redjepov A, Altunyuva Usta S, Yılmaz Y, Akalın F (January 1, 2023) Evaluation of autonomic nervous system functions by using tilt table test and heart rate variability in epileptic children. Marmara Medical Journal 36 1 87–92.
IEEE A. Redjepov, S. Altunyuva Usta, Y. Yılmaz, and F. Akalın, “Evaluation of autonomic nervous system functions by using tilt table test and heart rate variability in epileptic children”, Marmara Med J, vol. 36, no. 1, pp. 87–92, 2023, doi: 10.5472/marumj.1244552.
ISNAD Redjepov, Azad et al. “Evaluation of Autonomic Nervous System Functions by Using Tilt Table Test and Heart Rate Variability in Epileptic Children”. Marmara Medical Journal 36/1 (January 2023), 87-92. https://doi.org/10.5472/marumj.1244552.
JAMA Redjepov A, Altunyuva Usta S, Yılmaz Y, Akalın F. Evaluation of autonomic nervous system functions by using tilt table test and heart rate variability in epileptic children. Marmara Med J. 2023;36:87–92.
MLA Redjepov, Azad et al. “Evaluation of Autonomic Nervous System Functions by Using Tilt Table Test and Heart Rate Variability in Epileptic Children”. Marmara Medical Journal, vol. 36, no. 1, 2023, pp. 87-92, doi:10.5472/marumj.1244552.
Vancouver Redjepov A, Altunyuva Usta S, Yılmaz Y, Akalın F. Evaluation of autonomic nervous system functions by using tilt table test and heart rate variability in epileptic children. Marmara Med J. 2023;36(1):87-92.