A Circadian Rhythm in Heart Rate Variability Contributes to the Increased Cardiac Sympathovagal Response to Awakening in the Morning

Morning hours are associated with a heightened risk of adverse cardiovascular events. Recent evidence suggests that the sleep-wake cycle and endogenous circadian system modulate cardiac function in humans and may contribute to these epidemiological findings. The aim of the present study was to investigate the interaction between circadian and sleep-wake–dependent processes on heart rate variability (HRV). Fifteen diurnally active healthy young adults underwent a 72-h ultradian sleep-wake cycle (USW) procedure (alternating 60-min wake episodes in dim light and 60-min nap opportunities in total darkness) in time isolation. The present study revealed a significant main effect of sleep-wake–dependent and circadian processes on cardiac rhythmicity, as well as a significant interaction between these processes. Turning the lights off was associated with a rapid increase in mean RR interval and cardiac parasympathetic modulation (high-frequency [HF] power), whereas low-frequency (LF) power and sympathovagal balance (LF:HF ratio) were reduced (p ≤ .001). A significant circadian rhythm in mean RR interval and HRV components was observed throughout the wake and nap episodes (p ≤ .001). Sleep-to-wake transitions occurring in the morning were associated with maximal shifts towards sympathetic autonomic activation as compared to those occurring during the rest of the day. Namely, peak LF:HF ratio was observed in the morning, coincidental with peak salivary cortisol levels. These results contribute to our understanding of the observed increase in cardiovascular vulnerability after awakening in the morning. (Author correspondence: diane.boivin@douglas.mcgill.ca)

[1]  E. Haus,et al.  Twenty-four-hour pattern of angina pectoris, acute myocardial infarction and sudden cardiac death: Role of blood pressure, heart rate and rate-pressure product circadian rhythms , 2007 .

[2]  Frederic Roche,et al.  Cardiac variability and heart-rate increment as a marker of sleep fragmentation in patients with a sleep disorder: a preliminary study. , 2007, Sleep.

[3]  Keri J. Heilman,et al.  Accuracy of the LifeShirt® (Vivometrics) in the detection of cardiac rhythms , 2007, Biological Psychology.

[4]  R. Coleman Periodic movements in sleep (nocturnal myoclonus) and restless legs syndrome , 1982 .

[5]  J. Trinder,et al.  The influence of sleep onset on the diurnal variation in cardiac activity and cardiac control , 2003, Journal of sleep research.

[6]  M. Deuschle,et al.  Chronic but Not Acute Hydrocortisone Treatment Shifts the Response to an Orthostatic Challenge towards Parasympathetic Activity , 2005, Neuroendocrinology.

[7]  Mylan C. Cohen,et al.  Meta-analysis of the morning excess of acute myocardial infarction and sudden cardiac death. , 1997, The American journal of cardiology.

[8]  Nader Rifai,et al.  Effect of sleep loss on C-reactive protein, an inflammatory marker of cardiovascular risk. , 2004, Journal of the American College of Cardiology.

[9]  A. Chesson,et al.  The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology, and Techinical Specifications , 2007 .

[10]  M. Smolensky,et al.  ETHICS AND METHODS FOR BIOLOGICAL RHYTHM RESEARCH ON ANIMALS AND HUMAN BEINGS , 2010, Chronobiology international.

[11]  H Eugene Stanley,et al.  Endogenous circadian rhythm in an index of cardiac vulnerability independent of changes in behavior , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[12]  O. Pachinger,et al.  Comparison of peripheral endothelial function in shift versus nonshift workers. , 2011, The American journal of cardiology.

[13]  Mariska J Vansteensel,et al.  Sleep states alter activity of suprachiasmatic nucleus neurons , 2003, Nature Neuroscience.

[14]  A. Kalsbeek,et al.  The suprachiasmatic nucleus balances sympathetic and parasympathetic output to peripheral organs through separate preautonomic neurons , 2003, The Journal of comparative neurology.

[15]  M. Fujishima,et al.  Modulation of circadian rhythm of blood pressure by cortisol in patients with hypopituitarism. , 1994, Clinical and experimental hypertension.

[16]  R. Stafford,et al.  Principles and Practice of Sleep Medicine , 2001 .

[17]  Cheryl C. H. Yang,et al.  Sleep and autonomic nervous system changes - enhanced cardiac sympathetic modulations during sleep in permanent night shift nurses. , 2009, Scandinavian journal of work, environment & health.

[18]  S. Boveda,et al.  Depressed low frequency power of heart rate variability as an independent predictor of sudden death in chronic heart failure. , 2000, European heart journal.

[19]  J. Muller,et al.  Circadian variation in cardiovascular events. , 1999, American journal of hypertension.

[20]  David L. Donoho,et al.  WaveLab and Reproducible Research , 1995 .

[21]  Elevated Variance in Heart Rate During Slow-Wave Sleep After Late-Night Physical Activity , 2011, Chronobiology international.

[22]  D. Levy,et al.  Impact of reduced heart rate variability on risk for cardiac events. The Framingham Heart Study. , 1996, Circulation.

[23]  P. Linkowski,et al.  Quantitative Analysis of the 24‐Hour Blood Pressure and Heart Rate Patterns in Young Men , 1991, Hypertension.

[24]  Vincent Ibanez,et al.  Cardiac activation during arousal in humans: further evidence for hierarchy in the arousal response , 2000, Clinical Neurophysiology.

[25]  N. Lamond,et al.  Daytime cardiac autonomic activity during one week of continuous night shift. , 2001, Journal of human ergology.

[26]  A. Folsom,et al.  Low Heart Rate Variability in a 2-Minute Rhythm Strip Predicts Risk of Coronary Heart Disease and Mortality From Several Causes: The ARIC Study , 2000, Circulation.

[27]  W. Zareba,et al.  Heart rate variability. , 2013, Handbook of clinical neurology.

[28]  K. Spiegel,et al.  Impact of sleep debt on metabolic and endocrine function , 1999, The Lancet.

[29]  L. Křivan,et al.  Circadian Variations in the Occurrence of Ventricular Tachyarrhythmias in Patients with Implantable Cardioverter Defibrillators , 2003, Pacing and clinical electrophysiology : PACE.

[30]  Sonia Ancoli-Israel,et al.  Association of Incident Cardiovascular Disease With Periodic Limb Movements During Sleep in Older Men: Outcomes of Sleep Disorders in Older Men (MrOS) Study , 2011, Circulation.

[31]  P. De The autonomic nervous system and the hypothalamus. , 1947, Calcutta medical journal.

[32]  G. Vandewalle,et al.  Robust circadian rhythm in heart rate and its variability: influence of exogenous melatonin and photoperiod , 2007, Journal of sleep research.

[33]  D. Boivin,et al.  Circadian variation of sleep during the follicular and luteal phases of the menstrual cycle. , 2010, Sleep.

[34]  A. Burger,et al.  Circadian patterns of heart rate variability in normals, chronic stable angina and diabetes mellitus. , 1999, International journal of cardiology.

[35]  F. Burzotta,et al.  Prognostic role of heart rate variability in patients with a recent acute myocardial infarction. , 1998, The American journal of cardiology.

[36]  Alain Muzet,et al.  Sleep Processes Exert a Predominant Influence on the 24-h Profile of Heart Rate Variability , 2002, Journal of biological rhythms.

[37]  Shan Lu,et al.  Dynamic Analysis of Heart Rate Variability Based on Orthogonal Wavelet Transform , 2005, 2005 IEEE Engineering in Medicine and Biology 27th Annual Conference.

[38]  Philippe Boudreau,et al.  Predominance of Distal Skin Temperature Changes at Sleep Onset across Menstrual and Circadian Phases , 2011, Journal of biological rhythms.

[39]  C. Czeisler,et al.  Chapter 31 – The Human Circadian Timing System and Sleep-Wake Regulation , 2005 .

[40]  S. Ancoli-Israel,et al.  Diagnosis and treatment of sleep disorders in older adults. , 2006, The American journal of geriatric psychiatry : official journal of the American Association for Geriatric Psychiatry.

[41]  C. Saper,et al.  Hypothalamic regulation of sleep and circadian rhythms , 2005, Nature.

[42]  F. Scheer,et al.  Impact of the human circadian system, exercise, and their interaction on cardiovascular function , 2010, Proceedings of the National Academy of Sciences.

[43]  V. Somers,et al.  Early Morning Attenuation of Endothelial Function in Healthy Humans , 2004, Circulation.

[44]  M. Rondon,et al.  Day-night pattern of autonomic nervous system modulation in patients with heart failure with and without sleep apnea. , 2011, International journal of cardiology.

[45]  Jean Claude Barthelemy,et al.  Cardiovascular variability during periodic leg movements: a spectral analysis approach , 2005, Clinical Neurophysiology.

[46]  Ross Pigeau,et al.  Heart rate activation during spontaneous arousals from sleep: effect of sleep deprivation , 2004, Clinical Neurophysiology.

[47]  V Pichot,et al.  Wavelet transform to quantify heart rate variability and to assess its instantaneous changes. , 1999, Journal of applied physiology.

[48]  Daniel J Buysse,et al.  Circadian and homeostatic modulation of sleep in older adults during a 90-minute day study. , 2004, Sleep.

[49]  G. Parati,et al.  Autonomic cardiac modulation in obstructive sleep apnea: effect of an oral jaw-positioning appliance. , 2006, Chest.

[50]  S. Quan,et al.  Association of Incident Cardiovascular Disease With Progression of Sleep-Disordered Breathing , 2011, Circulation.

[51]  John Trinder,et al.  Sleep and circadian influences on cardiac autonomic nervous system activity. , 1997, American journal of physiology. Heart and circulatory physiology.

[52]  Jens Peter Bonde,et al.  Health – online first Shift work and the risk of ischemic heart disease – a systematic review of the epidemiologic evidence , 2009 .

[53]  A. Wirz-Justice,et al.  Age-related attenuation of the evening circadian arousal signal in humans , 2005, Neurobiology of Aging.

[54]  K. Chien,et al.  Habitual sleep duration and insomnia and the risk of cardiovascular events and all-cause death: report from a community-based cohort. , 2010, Sleep.

[55]  J. Gottdiener,et al.  Circadian variation of ambulatory myocardial ischemia. Triggering by daily activities and evidence for an endogenous circadian component. , 1996, Circulation.

[56]  F. Scheer,et al.  Existence of an Endogenous Circadian Blood Pressure Rhythm in Humans That Peaks in the Evening , 2011, Circulation research.

[57]  A. Camm,et al.  Mortality in Patients After a Recent Myocardial Infarction: A Randomized, Placebo-Controlled Trial of Azimilide Using Heart Rate Variability for Risk Stratification , 2004, Circulation.

[58]  K. Kräuchi,et al.  HEART-RATE VARIABILITY IN WOMEN DURING 40-HOUR PROLONGED WAKEFULNESS , 2010, Chronobiology international.

[59]  A. Yamashina,et al.  Effects of CPAP therapy on the sympathovagal balance and arterial stiffness in obstructive sleep apnea. , 2010, Respiratory medicine.

[60]  D. Hegney,et al.  The Effect of Shift Rotation on Employee Cortisol Profile, Sleep Quality, Fatigue, and Attention Level: A Systematic Review , 2011, The journal of nursing research : JNR.

[61]  Francois M. Abboud,et al.  Sympathetic-Nerve Activity During Sleep in Normal Subjects , 1993 .

[62]  W C Dement,et al.  Distribution of REM sleep on a 90 minute sleep-wake schedule. , 1980, Sleep.

[63]  A. Malliani,et al.  Heart rate variability. Standards of measurement, physiological interpretation, and clinical use , 1996 .

[64]  A. Chesson,et al.  The American Academy of Sleep Medicine (AASM) Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications , 2007 .

[65]  Daniel E Casey,et al.  Metabolic issues and cardiovascular disease in patients with psychiatric disorders. , 2005, The American journal of medicine.