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Impaired baroreflex function in temporal lobe epilepsy

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Abstract

Changes of cardiovascular function are frequent in temporal lobe epilepsy (TLE). The baroreflex – the most important reflex for cardiovascular stability – has not been studied systematically in TLE. We evaluated cardiovascular variability and baroreflex function in TLE.

In 22 TLE patients and 20 controls, we continuously monitored heart rate (HR) and blood pressure (BP). Time-domain parameters were derived from recordings at rest and from standard cardiovascular reflex tests. Spectral analysis determined sympathetic and parasympathetic modulation of HR and BP in the low (LF-power) and high frequency range (HF-power). We calculated the relative LF- and HF-powers of HR in relation to the sum of LF- and HF-powers. LF/HF-ratio of HR was assessed as a parameter of sympatheticovagal balance. LF-transfer function gain between BP and HR determined baroreflex function.

Time-domain parameters did not differ between TLE patients and controls. Spectral analysis showed decreased absolute LF- and HF-powers but increased relative LF-power and LF/HF-ratio of HR in TLE. LF-transfer function gain between BP and HR was reduced in TLE (p<0.05).

The reduction of absolute LF- and HF-powers indicates decreased total autonomic variability in TLE. However, increased relative LF-power and LF/HF-ratio of HR in TLE show a relative increase of sympathetic tone. Most importantly, we demonstrate an impaired baroreflex function in TLE. These cardiovascular autonomic abnormalities may contribute to cardiac arrhythmia in TLE.

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Abbreviations

BP:

blood pressure

bpm:

beats per minute

BRS:

baroreflex sensitivity

cpm:

cycles per minute

E/I:

exspiratory-inspiratory

HF:

high frequency

HR:

heart rate

HRV:

heart rate variability

LF:

low frequency

nu:

normalized units

OH:

orthostatic hypotension

SD:

standard deviation

SUDEP:

sudden unexplained death in epilepsy patients

TLE:

temporal lobe epilepsy

References

  1. Freeman R, Schachter SC (1995) Autonomic epilepsy. Semin Neurol 15:158–166

    Article  PubMed  CAS  Google Scholar 

  2. Devinsky O (2004) Effects of seizures on autonomic and cardiovascular function. Epilepsy Curr 4:43–46

    Article  PubMed  Google Scholar 

  3. Wannamaker BB (1985) Autonomic nervous system and epilepsy. Epilepsia 26: S31–S39

    PubMed  Google Scholar 

  4. Spyer KM (1999) Central nervous control of the cardiovascular system. In: Mathias CJ, Bannister (eds) Autonomic failure: a textbook of clinical disorders of the autonomic nervous system. Oxford University Press, Oxford, pp 45–55

    Google Scholar 

  5. Devinsky O, Perrine K, Theodore WH (1994) Interictal autonomic nervous system function in patients with epilepsy. Epilepsia 35:199–204

    Article  PubMed  CAS  Google Scholar 

  6. Druschky A, Hilz MJ, Hopp P, Platsch G, Radespiel-Troger M, Druschky K, et al. (2001) Interictal cardiac autonomic dysfunction in temporal lobe epilepsy demonstrated by (123)I.metaiodobenzylguanidine-SPECT. Brain 124:2372–2382

    Article  PubMed  CAS  Google Scholar 

  7. Frysinger RC, Engel J, Harper RM (1993) Interictal heart rate patterns in partial seizure disorders. Neurology 43:2136–2139

    PubMed  CAS  Google Scholar 

  8. Isojarvi JI, Ansakorpi H, Suominen K, Tolonen U, Repo M, Myllyla VV (1998) Interictal cardiovascular autonomic responses in patients with epilepsy. Epilepsia 39:420–426

    Article  PubMed  CAS  Google Scholar 

  9. Hilz MJ, Devinsky O, Doyle W, Mauerer A, Dutsch M (2002) Decrease of sympathetic cardiovascular modulation after temporal lobe epilepsy surgery. Brain 125:985–995

    Article  PubMed  CAS  Google Scholar 

  10. Tomson T, Ericson M, Ihrman C, Lindblad LE (1998) Heart rate variability in patients with epilepsy. Epilepsy Res 30:77–83

    Article  PubMed  CAS  Google Scholar 

  11. Massetani R, Strata G, Galli R, Gori S, Gneri C, Limbruno U, et al. (1997) Alteration of cardiac function in patients with temporal lobe epilepsy: different roles of EEG-ECG monitoring and spectral analysis of RR variability. Epilepsia 38:363–369

    Article  PubMed  CAS  Google Scholar 

  12. Ansakorpi H, Korpelainen JT, Suominen K, Tolonen U, Myllyla VV, Isojarvi JL (2000) Interictal cardiovascular autonomic responses in patients with temporal lobe epilepsy. Epilepsia 41:42–47

    Article  PubMed  CAS  Google Scholar 

  13. Ansakorpi H, Korpelainen JT, Huikuri HV, Tolonen U, Myllyla VV, Isojarvi JL (2002) Heart rate dynamics in refractory and well controlled temporal lobe epilepsy. J Neurol Neurosurg Psychiatry 72:26–30

    Article  PubMed  CAS  Google Scholar 

  14. Annegers JF, Coan SP (1999) SUDEP: overview of definitions and review of incidence data. Seizure 8:347–352

    Article  PubMed  CAS  Google Scholar 

  15. Cockerell OC, Johnson AL, Sander JW, Hart YM, Goodridge DM, Shorvon SD (1994) Mortality from epilepsy: results from a prospective population-based study. Lancet 344:918–921

    Article  PubMed  CAS  Google Scholar 

  16. Earnest MP, Thomas GE, Eden RA, Hossack KF (1992) The sudden unexplained death syndrome in epilepsy: demographic, clinical, and postmortem features. Epilepsia 33:310–316

    Article  PubMed  CAS  Google Scholar 

  17. Leestma JE, Kalelkar MB, Teas SS, Jay GW, Hughes JR (1984) Sudden unexpected death associated with seizures: analysis of 66 cases. Epilepsia 25:84–88

    PubMed  CAS  Google Scholar 

  18. Walczak TS, Leppik IE, D’Amelio M, Rarick J, So E, Ahman P, et al. (2001) Incidence and risk factors in sudden unexpected death in epilepsy: a prospective cohort study. Neurology 56:519–525

    PubMed  CAS  Google Scholar 

  19. Terrence CFJ, Wisotzkey HM, Perper JA (1975) Unexpected, unexplained death in epileptic patients. Neurology 25:594–598

    PubMed  Google Scholar 

  20. Frenneaux MP (2004) Autonomic changes in patients with heart failure and in post-myocardial infarction patients. Heart 90:1248–1255

    Article  PubMed  CAS  Google Scholar 

  21. La Rovere MT, Pinna GD, Hohnloser SH, Marcus FI, Mortara A, Nohara R, et al. (2001) Baroreflex sensitivity and heart rate variability in the identification of patients at risk for life-threatening arrhythmias: implication for clinical trials. Circulation: 2072–2077

  22. La Rovere MT, Bersano C, Gnemmi M, Specchia G, Schwartz PJ (2002) Exercise-induced increase in baroreflex sensitivity predicts improved prognosis after myocardial infarction. Circulation 106:945–949

    Article  PubMed  Google Scholar 

  23. Kemmotsu O, Ueda M, Otsuka H, Yamamura T, Winter DC, Eckerle JS (1991) Arterial tonometry for noninvasive, continuous blood pressure monitoring during anesthesia. Anesthesiology 75:333–340

    Article  PubMed  CAS  Google Scholar 

  24. Ewing DJ (1993) Noninvasive evaluation of heart rate: The time domain. In: Low PA (eds) Clinical Autonomic Disorders. Little, Brown & Co., Boston, pp 297–314

    Google Scholar 

  25. Freeman R (1997) Noninvasive evaluation of heart rate variability. The time domain. In: Low PA (eds) Clinical Autonomic Disorders, 2nd ed. Lippincott-Raven Publishers, Philadelphia, pp 297–307

    Google Scholar 

  26. Genovely H, Pfeifer MA (1988) RR-Variation: The autonomic test of choice in diabetes. Diabetes/Metabolism Reviews 4:255–271

    Article  PubMed  CAS  Google Scholar 

  27. Low PA (1997) Laboratory evaluation of autonomic function. In: Low PA (eds) Clinical Autonomic Disorders, 2nd ed. Lippincott-Raven Publishers, Philadelphia, pp 179–208

    Google Scholar 

  28. Mathias CJ, Bannister R (1999) Investigation of autonomic disorders. In: Mathias CJ, Bannister (eds) Autonomic failure: a textbook of clinical disorders of the autonomic nervous system. Oxford University Press, Oxford, pp 169–195

    Google Scholar 

  29. Ziegler D, Laux G, Dannehl K, Spuler M, Muhlen H, Mayer P, et al. (1992) Assessment of cardiovascular autonomic function: age-related normal ranges and reproducibility of spectral analysis, vector analysis, and standard tests of heart rate variation and blood pressure responses. Diabet Med 9:166–175

    Article  PubMed  CAS  Google Scholar 

  30. The Consensus Committee of the American Autonomic Society, the American Academy of Neurology (1996) Consensus statement on the definition of orthostatic hypotension, pure autonomic failure, and multiple system atrophy. Neurology 46:1470

    Google Scholar 

  31. Hilz MJ, Stemper B, Sauer P, Haertl U, Singer W, Axelrod FB (1999) Cold face test demonstrates parasympathetic cardiac dysfunction in familial dysautonomia. Am J Physiol 276: R1833–R1839

    PubMed  CAS  Google Scholar 

  32. Saul JP, Berger RD, Albrecht P, Stein SP, Chen MH, Cohen RJ (1991) Transfer function analysis of the circulation: unique insights into cardiovascular regulation. Am J Physiol 261: H1231–H1245

    PubMed  CAS  Google Scholar 

  33. Saul JP (1990) Beat-to-beat variations of heart rate reflect modulation of cardiac autonomic outflow. News Physiol Sci 5:32–37

    Google Scholar 

  34. Task Force of the European Society of Cardiology, the North American Society of Pacing and Electrophysiology (1996) Heart rate variability: standards of measurement, physiological interpretation, and clinical use. Circulation 93:1043–1065

    Google Scholar 

  35. Bernardi L, Leuzzi S, Radaelli A, Passino C, Johnston JA, Sleight P (1994) Low-frequency spontaneous fluctuations of R-R interval and blood pressure in conscious humans: a baroreceptor or central phenomenon? Clin Sci (Colch) 87:649–654

    CAS  Google Scholar 

  36. Pagani M, Lombardi F, Guzzetti S, Rimoldi O, Furlan R, Pizzinelli P, et al. (1986) Power spectral analysis of heart rate and arterial pressure variabilities as a marker of sympatho-vagal interaction in man and conscious dog. Circ Res 59:178–193

    PubMed  CAS  Google Scholar 

  37. Pomeranz B, Macaulay RJ, Caudill MA, Kutz I, Adam D, Gordon D, et al. (1985) Assessment of autonomic function in humans by heart rate spectral analysis. Am J Physiol 248:H151–H153

    PubMed  CAS  Google Scholar 

  38. Robbe HW, Mulder LJ, Ruddel H, Langewitz WA, Veldman JB, Mulder G (1987) Assessment of baroreceptor reflex sensitivity by means of spectral analysis. Hypertension 10:538–543

    PubMed  CAS  Google Scholar 

  39. Berger RD, Saul JP, Cohen RJ (1989) Transfer function analysis of autonomic regulation. I. Canine atrial rate response. Am J Physiol 256: H142–H152

    PubMed  CAS  Google Scholar 

  40. Ansakorpi H, Korpelainen JT, Tanskanen P, Huikuri HV, Koivula A, Tolonen U, et al. (2004) Cardiovascular regulation and hippocampal sclerosis. Epilepsia 45:933–939

    Article  PubMed  Google Scholar 

  41. Lathers CM, Schraeder PL, Weiner FL (1987) Synchronization of cardiac autonomic neural discharge with epileptogenic activity: the lockstep phenomenon. Electroencephalogr Clin Neurophysiol 67:247–259

    Article  PubMed  CAS  Google Scholar 

  42. Lanfranchi PA, Somers VK (2002) Arterial baroreflex function and cardiovascular variability: interactions and implications. Am J Physiol Regul Integr Comp Physiol 283:R815–R826

    PubMed  Google Scholar 

  43. Somers VK, Abboud FM (1994) Baroreflexes in health and disease. In: Levy MN, Schwartz PJ (eds) Vagal control of the heart: experimental basis and clinical implications. Futura Publishing Company, Inc., Armonk, NY, pp 381–402

    Google Scholar 

  44. Blumhardt LD, Smith PE, Owen L (1996) Electrocardiographic accompaniments of temporal lobe epileptic seizures. Lancet 1:1051–1056

    Google Scholar 

  45. Keilson MJ, Hauser WA, Magrill JP, Goldman M (1987) ECG abnormalities in patients with epilepsy. Neurology 37:1624–1626

    PubMed  CAS  Google Scholar 

  46. Sharabi Y, Dendi R, Holmes C, Goldstein DS (2003) Baroreflex failure as a late sequela of neck irradiation. Hypertension 42:110–116

    Article  PubMed  CAS  Google Scholar 

  47. Timmers HJ, Wieling W, Karemaker JM, Lenders JW (2004) Baroreflex failure: a neglected type of secondary hypertension. Neth J Med 62:151–155

    PubMed  CAS  Google Scholar 

  48. Hayward LF, Felder RB (1998) Lateral parabrachial nucleus modulates baroreflex regulation of sympathetic nerve activity. Am J Physiol Regul Integr Comp Physiol 274:R1274–R1282

    CAS  Google Scholar 

  49. Saleh TM, Connell BJ (1997) Modulation of the cardiac baroreflex following reversible blockade of the parabrachial nucleus in the rat. Brain Res 767:201–207

    Article  PubMed  CAS  Google Scholar 

  50. Mraovitch S, Kumada M, Reis DJ (1982) Role of the nucleus parabrachialis in cardiovascular regulation in the cat. Brain Res 232:57–75

    Article  PubMed  CAS  Google Scholar 

  51. Dampney RAL, Polson JW, Potts PD, Hirooka Y, Horiuchi J (2003) Functional organization of brain pathways subserving the baroreceptor reflex: studies in conscious animals using immediate early gene expression. Cell Mol Neurobiol 23:597–616

    Article  PubMed  CAS  Google Scholar 

  52. Zhang ZH, Rashba S, Oppenheimer SM (1998) Insular cortex lesions alter baroreceptor sensitivity in the urethane-anesthetized rat. Brain Res 813:73–81

    Article  PubMed  CAS  Google Scholar 

  53. Zhang ZH, Oppenheimer SM (2000) Baroreceptive and somatosensory convergent thalamic neurons project to the posterior insular cortex in the rat. Brain Res 861:241–256

    Article  PubMed  CAS  Google Scholar 

  54. Dam M, Tigaran S, Rasmussen K, Rehling M, Molgaard H (2001) Sudden unexpected death in epilepsy: regional myocardial blood flow during seizure. Neurology 56 Suppl 3:A233–A234

    Google Scholar 

  55. Tigaran S, Molgaard H, McClelland R, Dam M, Jaffe AS (2003) Evidence of cardiac ischemia during seizures in drug refractory epilepsy patients. Neurology 60:492–495

    PubMed  CAS  Google Scholar 

  56. Greene-Chandos DL, Landt Y, Hirsch R, Landt M, Edwards D, Ladenson J (2001) Pediatric epilepsy patients without cardiac history show elevated troponin I levels. Neurology 56 Suppl 3:A233

    Google Scholar 

  57. Natelson BH, Suarez RV, Terrence CF, Turizo R (1998) Patients with epilepsy who die suddenly have cardiac disease. Arch Neurol 55:857–60

    Article  PubMed  CAS  Google Scholar 

  58. Persson H, Ericson M, Tomson T (2003) Carbamazepine affects autonomic cardiac control in patients with newly diagnosed epilepsy. Epilepsy Res 57:69–75

    Article  PubMed  CAS  Google Scholar 

  59. Bernardi L, Valle F, Coco M, Calciati A, Sleight P (1996) Physical activity influences heart rate variability and very-low frequency components in Holter electrocardiograms. Cardiovasc Res 32:234–237

    Article  PubMed  CAS  Google Scholar 

  60. Lee CM, Wood RH, Welsch MA (2003) Influence of short-term endurance exercise training on heart rate variability. Med Sci Sports Exerc 35:961–969

    Article  PubMed  Google Scholar 

  61. Ueno LM, Moritani T (2003) Effects of long-term exercise training on cardiac autonomic nervous activities and baroreflex sensitivity. Eur J Appl Physiol 89:109–114

    PubMed  Google Scholar 

  62. O’Sullivan SE, Bell C (2000) The effects of exercise and training on human cardiovascular reflex control. J Auton Nerv Syst 81:16–24

    Article  PubMed  CAS  Google Scholar 

  63. Shin K, Minamitani H, Onishi S, Yamazaki H, Lee M (1997) Autonomic differences between athletes and nonathletes: spectral analysis approach. Med Sci Sports Exerc 29:148–190

    Google Scholar 

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Acknowledgements

M.D. received a postdoctoral grant from the German Academic Exchange Service, and the study was partially supported by unrestricted grants from Sanofi-Synthelabo, Germany and from Pharmacia-Upjohn, USA.

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Authors and Affiliations

  1. Department of Neurology, University of Erlangen-Nuremberg, Schwabachanlage 6, 91054, Erlangen, Germany

    Mathias Dütsch MD & Max J. Hilz MD, PhD

  2. Department of Neurology, New York University School of Medicine, 560, First Avenue, NB 7 W 11, New York, NY, 10016, USA

    Max J. Hilz MD, PhD & Orrin Devinsky MD

Authors
  1. Mathias Dütsch MD
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  2. Max J. Hilz MD, PhD
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  3. Orrin Devinsky MD
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Correspondence to Max J. Hilz MD, PhD.

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Received in revised form: 15 February 2006

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Dütsch, M., Hilz, M.J. & Devinsky, O. Impaired baroreflex function in temporal lobe epilepsy. J Neurol 253, 1300–1308 (2006). https://doi.org/10.1007/s00415-006-0210-3

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