Non-invasive assessment of cardioregulatory autonomic functions in children with epilepsy
E. S. El-Hadidi
Clinical Pathology, Ain Shams University, Cairo, Egypt
Search for more papers by this authorE. S. El-Hadidi
Clinical Pathology, Ain Shams University, Cairo, Egypt
Search for more papers by this authorAbstract
Objectives – We aimed to evaluate the interictal cardiovascular autonomic functions in pediatric patients with idiopathic epilepsy, both partial and generalized.
Materials and methods – The study included 25 patients with idiopathic epilepsy and 50 control subjects. Patients underwent five standardized clinical cardiovascular reflex autonomic tests [resting heart rate (HR), HR response to deep breathing and to Valsalva maneuver, the 30:15 ratio of HR response to standing, and blood pressure response to standing], as well as a 12 lead surface electrocardiogram. Heart rate variability (HRV) was tested via 24-h Holter monitoring and the time domain parameters (SDNN, PNN50, rMSDD) were assessed. Excretion of vanillyl mandelic acid and metanephrine was measured in 24-h urine collection.
Results – Clinical reflex autonomic tests showed mild dysfunction in 8%, moderate dysfunction in 44% and severe dysfunction in 4% of patients. The HRV parameter, SDNN, was reduced in all age groups, while rMSDD and PNN50 were reduced only in the older age group. Metanephrine levels were significantly reduced in the patients group. Patients with uncontrolled epilepsy had a significantly higher frequency of autonomic dysfunction as assessed by clinical scoring.
Conclusion – Cardiac autonomic dysfunction is not uncommon in pediatric patients with epilepsy. Altered cardiovascular regulation seems to be related to the epilepsy itself rather than to the characteristics of the disorder.
References
- 1 Cockerell OC. The mortality of epilepsy. Curr Opin Neurol 1996; 9: 93–6.
- 2 Nashef L, Fish DR, Sander JW, Shorvon SD. Incidence of sudden unexpected death in an adult outpatient cohort with epilepsy at a tertiary referral centre. J Neurol Neurosurg Psychiatry 1995; 58: 462–4.
- 3 Langan Y, Nolan N, Hutchinson M. The incidence of sudden unexpected death in epilepsy in South Dublin and Wicklow. Seizure 1998; 7: 355–8.
- 4 Leestma JE, Walczak T, Hughes JR, Kalelkar MB, Teas SS. A prospective study on sudden unexpected death in epilepsy. Ann Neurol 1989; 26: 195–203.
- 5 Nashef L. Sudden unexpected death in epilepsy: terminology and definitions. Epilepsia 1997; 38: S6–8.
- 6 Dasheiff RM. Sudden unexpected death in epilepsy: a series from an epilepsy surgery program and speculation on the relationship to sudden cardiac death. J Clin Neurophysiol 1991; 8: 216–22.
- 7 Natelson BH, Suarez RV, Terrence CF, Turizo R. Patients with epilepsy who die suddenly have cardiac disease. Arch Neurol 1998; 55: 857–60.
- 8 Tomson T, Ericson M, Ihrman C, Lindblad LE. Heart rate variability in patients with epilepsy. Epilepsy Res 1998; 30: 77–83.
- 9 Duncan JS, Sander JW. The Chalfont Seizure Severity Scale. J Neurol Neurosurg Psychiatry 1991; 54: 873–6.
- 10 Ewing DJ, Martyn CN, Young RJ, Clarke BF. The value of cardiovascular autonomic function tests: 10 years experience in diabetes. Diabetes Care 1985; 8: 491–8.
- 11 Ewing DJ. Analysis of heart rate variability and other non-invasive tests with special reference to diabetes mellitus. In: R Bannister, CJ Mathias, eds. Autonomic failure. Oxford, UK: Oxford University Press, 1992; 312–33.
- 12 Scott WA. Assessment of the autonomic nervous system. In: HD Allen, HP Gutgesell, EB Clark, DJ Driscoll, eds. Moss and Adams’ heart disease in infants, children and adolescents including the fetus and young adult. Baltimore, MD: Lippincott Williams & Wilkins, 2001; 172–6.
- 13 Hartwig MS, Cardoso SS, Hathaway DK, Gaber AO. Reliability and validity of cardiovascular and vasomotor autonomic function tests. Diabetes Care 1994; 17: 1433–40.
- 14 Ewing DJ, Clarke BF. Diagnosis and management of diabetic autonomic neuropathy. Br Med J 1982; 85: 916–8.
- 15 Barkai L, Madacsy L. Cardiovascular autonomic dysfunction in diabetes mellitus. Arch Dis Child 1995; 73: 515–8.
- 16 Veglio M, Carpano-Maglioli P, Tonda L et al. Autonomic neuropathy in non-insulin-dependent diabetic patients: correlation with age, sex, duration and metabolic control of diabetes. Diabete Metab 1990; 16: 200–6.
- 17 Nashef L, Walker F, Allen P, Sander JW, Shorvon SD, Fish DR. Apnoea and bradycardia during epileptic seizures: relation to sudden death in epilepsy. J Neurol Neurosurg Psychiatry 1996; 60: 297–300.
- 18 Nei M, HO RT, Sperling MR. EKG abnormalities during partial seizures in refractory epilepsy. Epilepsia 2000; 41: 542–8.
- 19 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.
- 20 Ansakorpi H, Korpelainen JT, Suominen K, Tolonen U, Myllyla VV, Isojarvi JIT. Interictal cardiovascular autonomic responses in patients with temporal lobe epilepsy. Epilepsia 2000; 41: 42–7.
- 21 Ansakorpi H, Korpelainen JT, Huikuri HV, Tolonen U, Myllyla VV, Isojarvi JI. Heart rate dynamics in refractory and well controlled temporal lobe epilepsy. J Neurol Neurosurg Psychiatry 2002; 72: 26–30.
- 22 Zaatreh MM, Quint SR, Tennison MB, D'Cruz O, Vaughn BB. Heart rate variability during interictal epileptiform discharges. Epilepsy Res 2003; 54: 85–90.
- 23 Yang TF, Wong TT, Chang KP et al. Power spectrum analysis of heart rate variability in children with epilepsy. Childs Nerv Syst 2000; 17: 602–6.
- 24 Harvey AS, Nolan T, Carlin JB. Community based study of the mortality in children with epilepsy. Epilepsia 1993; 34: 597–603.
- 25 Oppenheimer SM, Cechetto DF, Hachinski VC. Cerebrogenic cardiac arrhythmias. Cerebral electrocardiographic influences and their role in sudden death. Arch Neurol 1990; 47: 513–9.
- 26 Isojarvi JIT, Ansakorpi H, Suominen K, Tolonen U, Repo M, Myllyla VV, Interictal cardiovascular responses in patients with epilepsy. Epilepsia 1998; 39: 420–6.
- 27 Drake ME Jr, Andrews JM, Castleberry CM. Electrophysiologic assessment of autonomic function in epilepsy. Seizure 1998; 7: 91–6.
- 28 Berilgen MS, Sari T, Bulut S, Mungen B. Effects of epilepsy on autonomic nervous system and respiratory function tests. Epilepsy Behav 2004; 5: 513–6.
- 29 Tsuji H, Venditti FJ Jr, Manders ES et al. Determinants of heart rate variability. J Am Coll Cardiol 1996; 28: 1539–46.
- 30 Vikman S, Makikallio TH, Yli-Mayry S et al. Altered complexity and correlation properties of R-R interval dynamics before the spontaneous onset of paroxysmal atrial fibrillation. Circulation 1999; 100: 2079–84.
- 31 Stein PK, Bosner MS, Kleiger RE, Conger BM. Heart rate variability: a measure of cardiac autonomic tone. Am Heart J 1994; 127: 1376–81.
- 32 Persson H, Kumlien E, Ericson M, Tomson T. Preoperative heart rate variability in relation to surgery outcome in refractory epilepsy. Neurology 2005; 65: 1021–5.
- 33 Ronkainen E, Ansakorpi H, Huikuri HV, Myllyla VV, Isojarvi JI, Korpelainen JT. Suppressed circadian heart rate dynamics in temporal lobe epilepsy. J Neurol Neurosurg Psychiatry 2005; 76: 1382–6.
- 34 Massetani R, Strata G, Galli 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 1997; 38: 363–9.
- 35 Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Heart rate variability: standards of measurement, physiological interpretation and clinical use. Circulation 1996; 93: 1043–65.
- 36 Huikuri HV. Heart rate variability in coronary artery disease. J Intern Med 1995; 237: 349–57.
- 37 Huikuri HV, Seppanen T, Koistinen MJ et al. Abnormalities in beat-to-beat dynamics of heart rate before the spontaneous onset of life-threatening ventricular tachyarrhythmias in patients with prior myocardial infarction myocardial infarction. Circulation 1996; 93: 1836–44.
- 38 Huikuri HV, Makikallio TH, Airaksinen KE et al. Power-law relationship of heart variability as a predictor of mortality in elderly. Circulation 1998; 97: 2031–6.
- 39 Laxer KD, Sourkes TL, Fang TY, Young SN, Gautheir SG, Missala K. Monoamine metabolites in the CSF of epileptic patients. Neurology 1979; 29: 1157–61.
- 40 Kapustecki J, Rociszewska D, Pierzchala K. Secretion of catecholamines in urine of patients with tonic–clonic epileptic seizures. Wiad Lek 2000; 53: 199–506 (English abstract).
- 41 Devinsky O. Effects of seizures on autonomic and cardiovascular function. Epilepsy Curr 2004; 4: 43–6.
- 42 Tinuper P, Bisulli F, Cerullo A et al. Ictal bradycardia in partial epileptic seizures. Autonomic investigations in three cases and literature review. Brain 2001; 124: 2361–71.
- 43 Persson H, Ericson M, Tomson T. Carbamazepine affects cardiac control in patients with newly diagnosed epilepsy. Epilepsy Res 2003; 7: 69–75.