Heart rate variability in normal and pathological sleep

Sleep is a physiological process involving different biological systems, from molecular to organ level; its integrity is essential for maintaining health and homeostasis in human beings. Although in the past sleep has been considered a state of quiet, experimental and clinical evidences suggest a noteworthy activation of different biological systems during sleep. A key role is played by the autonomic nervous system (ANS), whose modulation regulates cardiovascular functions during sleep onset and different sleep stages. Therefore, an interest on the evaluation of autonomic cardiovascular control in health and disease is growing by means of linear and non-linear heart rate variability (HRV) analyses. The application of classical tools for ANS analysis, such as HRV during physiological sleep, showed that the rapid eye movement (REM) stage is characterized by a likely sympathetic predominance associated with a vagal withdrawal, while the opposite trend is observed during non-REM sleep. More recently, the use of non-linear tools, such as entropy-derived indices, have provided new insight on the cardiac autonomic regulation, revealing for instance changes in the cardiovascular complexity during REM sleep, supporting the hypothesis of a reduced capability of the cardiovascular system to deal with stress challenges. Interestingly, different HRV tools have been applied to characterize autonomic cardiac control in different pathological conditions, from neurological sleep disorders to sleep disordered breathing (SDB). In summary, linear and non-linear analysis of HRV are reliable approaches to assess changes of autonomic cardiac modulation during sleep both in health and diseases. The use of these tools could provide important information of clinical and prognostic relevance.

[1]  Róbert Bódizs,et al.  The nature of arousal in sleep , 2004, Journal of sleep research.

[2]  Nicola Montano,et al.  Heart rate variability as a clinical tool. , 2002, Italian heart journal : official journal of the Italian Federation of Cardiology.

[3]  E. Bixler,et al.  SLEEP APNOEA IN A HYPERTENSIVE POPULATION , 1984, The Lancet.

[4]  A. Malliani,et al.  Cardiovascular Neural Regulation Explored in the Frequency Domain , 1991, Circulation.

[5]  Prabhakaran Gopalakrishnan,et al.  Obstructive Sleep Apnea and Cardiovascular Disease , 2011, Cardiology in review.

[6]  A. Borbély,et al.  Heart rate dynamics during human sleep , 1994, Physiology & Behavior.

[7]  B. Wallin,et al.  Sympathetic neural control of integrated cardiovascular function: Insights from measurement of human sympathetic nerve activity , 2007, Muscle & nerve.

[8]  M. Turiel,et al.  Power Spectral Analysis of Heart Rate and Arterial Pressure Variabilities as a Marker of Sympatho‐Vagal Interaction in Man and Conscious Dog , 1986, Circulation research.

[9]  O. Devinsky,et al.  Cerebral autoregulation improves in epilepsy patients after temporal lobe surgery , 2004, Journal of Neurology.

[10]  M. Brodie,et al.  Mortality in adults with newly diagnosed and chronic epilepsy: a retrospective comparative study , 2006, The Lancet Neurology.

[11]  R. Brotherstone,et al.  Parasympathetic alteration during sub-clinical seizures , 2012, Seizure.

[12]  M H Bonnet,et al.  Heart Rate Variability in Insomniacs and Matched Normal Sleepers , 1998, Psychosomatic medicine.

[13]  C Baumgartner,et al.  Autonomic symptoms during epileptic seizures. , 2001, Epileptic disorders : international epilepsy journal with videotape.

[14]  T. Tomson,et al.  Heart rate variability in patients with epilepsy 1 Presented in part at the 2nd European Congress of Epileptology, The Hague, September, 1996. 1 , 1998, Epilepsy Research.

[15]  Josemir W Sander,et al.  Sudden unexpected death in epilepsy: People with nocturnal seizures may be at highest risk , 2012, Epilepsia.

[16]  K. Spiegelhalder,et al.  The association between insomnia and cardiovascular diseases , 2010, Nature and science of sleep.

[17]  A. Porta,et al.  Progressive decrease of heart period variability entropy-based complexity during graded head-up tilt. , 2007, Journal of applied physiology.

[18]  L. Stegagno,et al.  Nighttime cardiac sympathetic hyper-activation in young primary insomniacs , 2013, Clinical Autonomic Research.

[19]  J. Trinder,et al.  Autonomic activity during human sleep as a function of time and sleep stage , 2001, Journal of sleep research.

[20]  P. van de Borne,et al.  The impact of chronic primary insomnia on the heart rate – EEG variability link , 2009, Clinical Neurophysiology.

[21]  V. Somers,et al.  Baroreflex control of sympathetic nerve activity and heart rate in obstructive sleep apnea. , 1998, Hypertension.

[22]  H. Huikuri,et al.  Fractal analysis and time- and frequency-domain measures of heart rate variability as predictors of mortality in patients with heart failure. , 2001, The American journal of cardiology.

[23]  J. Miller,et al.  Decreased heart rate variability and its association with increased mortality after acute myocardial infarction. , 1987, The American journal of cardiology.

[24]  P. Castiglioni,et al.  Baroreflex control of heart rate during sleep in severe obstructive sleep apnoea: effects of acute CPAP , 2006, European Respiratory Journal.

[25]  C. Tassinari,et al.  Sudden unexpected death in epilepsy (SUDEP) and sleep. , 2011, Sleep medicine reviews.

[26]  L. Gallicchio,et al.  Sleep duration and mortality: a systematic review and meta‐analysis , 2009, Journal of sleep research.

[27]  R Lazzara,et al.  Heart rate variability during specific sleep stages. A comparison of healthy subjects with patients after myocardial infarction. , 1995, Circulation.

[28]  L Parrino,et al.  The cyclic alternating pattern sequences in the dynamic organization of sleep. , 1988, Electroencephalography and clinical neurophysiology.

[29]  J. Lanquart,et al.  Long-term CPAP treatment partially improves the link between cardiac vagal influence and delta sleep , 2013, BMC Pulmonary Medicine.

[30]  A. Camm,et al.  Heart rate variability in relation to prognosis after myocardial infarction: selection of optimal processing techniques. , 1989, European heart journal.

[31]  M. Josephson,et al.  Advances in Arrhythmia and Electrophysiology Impact of Sleep on Arrhythmogenesis , 2009 .

[32]  A. Malhotra,et al.  Continuous positive airway pressure therapy for treating sleepiness in a diverse population with obstructive sleep apnea: results of a meta-analysis. , 2003 .

[33]  M. Marciani,et al.  Baroreflex Buffering of Sympathetic Activation During Sleep: Evidence From Autonomic Assessment of Sleep Macroarchitecture and Microarchitecture , 2004, Hypertension.

[34]  V. Somers,et al.  Cardiovascular variability characteristics in obstructive sleep apnea , 2001, Autonomic Neuroscience.

[35]  Kalervo Suominen,et al.  Interictal Cardiovascular Autonomic Responses in Patients with Temporal Lobe Epilepsy , 2000, Epilepsia.

[36]  S. Cerutti,et al.  Vegetative Background of Sleep Spectral Analysis of the Heart Rate Variability , 1997, Physiology & Behavior.

[37]  S. Redline,et al.  Association of cardiac autonomic function measures with severity of sleep‐disordered breathing in a community‐based sample , 2008, Journal of sleep research.

[38]  Alberto Porta,et al.  Symbolic analysis detects alterations of cardiac autonomic modulation in congestive heart failure rats , 2009, Autonomic Neuroscience.

[39]  Ruth Bochner,et al.  THE CLINICAL APPLICATION , 1945 .

[40]  L. Stegagno,et al.  Heart rate variability during sleep as a function of the sleep cycle , 2003, Biological Psychology.

[41]  R. Tkacova,et al.  Effects of continuous positive airway pressure on cardiovascular risk profile in patients with severe obstructive sleep apnea and metabolic syndrome. , 2008, Chest.

[42]  R McCarty,et al.  Relationship between plasma norepinephrine and sympathetic neural activity. , 1983, Hypertension.

[43]  F. Cappuccio,et al.  Sleep duration and all-cause mortality: a systematic review and meta-analysis of prospective studies. , 2010, Sleep.

[44]  W C Orr,et al.  Heart rate variability during waking and sleep in healthy males and females. , 1999, Sleep.

[45]  S. Nevsimalova,et al.  Spectral analysis of heart rate variability in sleep. , 2005, Physiological Research.

[46]  G. Cascino,et al.  Population-based study of the incidence of sudden unexplained death in epilepsy , 1998, Neurology.

[47]  S. Quint,et al.  Heart period variability in sleep. , 1995, Electroencephalography and clinical neurophysiology.

[48]  A. Skanes,et al.  Heart Rate Variability in Obstructive Sleep Apnea: A Prospective Study and Frequency Domain Analysis , 2003, Annals of noninvasive electrocardiology : the official journal of the International Society for Holter and Noninvasive Electrocardiology, Inc.

[49]  M. Marciani,et al.  Sleep-related changes in baroreflex sensitivity and cardiovascular autonomic modulation , 2003, Journal of hypertension.

[50]  M. Terzano,et al.  Cyclic alternating pattern and spectral analysis of heart rate variability during normal sleep , 2000, Journal of sleep research.

[51]  B. A. Phillips Long-term Cardiovascular Outcomes in Men With Obstructive Sleep Apnoea-Hypopnoea With or Without Treatment With Continuous Positive Airway Pressure: An Observational Study , 2007 .

[52]  A Voss,et al.  Improved analysis of heart rate variability by methods of nonlinear dynamics. , 1995, Journal of electrocardiology.

[53]  S Akselrod,et al.  Fluctuations in autonomic nervous activity during sleep displayed by power spectrum analysis of heart rate variability , 1995, Neurology.

[54]  M. Malik,et al.  Sympathovagal balance: a critical appraisal. , 1998, Circulation.

[55]  J. Muller,et al.  Sympathetic activity as the cause of the morning increase in cardiac events. A likely culprit, but the evidence remains circumstantial. , 1995, Circulation.

[56]  G. Tofler,et al.  Effects of continuous positive airway pressure on coagulability in obstructive sleep apnoea: a randomised, placebo-controlled crossover study , 2012, Thorax.

[57]  Heikki V Huikuri,et al.  Measurement of heart rate variability by methods based on nonlinear dynamics. , 2003, Journal of electrocardiology.

[58]  J. Paton,et al.  The yin and yang of cardiac autonomic control: Vago-sympathetic interactions revisited , 2005, Brain Research Reviews.

[59]  D. Hillman,et al.  Association of sleep apnoea with myocardial infarction in men , 1990, The Lancet.

[60]  Alberto Porta,et al.  Assessment of cardiac autonomic modulation during graded head-up tilt by symbolic analysis of heart rate variability. , 2007, American journal of physiology. Heart and circulatory physiology.

[61]  H V Huikuri,et al.  Suppressed circadian heart rate dynamics in temporal lobe epilepsy , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[62]  M. Partinen,et al.  Sleep apnea and mortality in an aged cohort. , 1988, American journal of public health.

[63]  Elena Urrestarazu,et al.  Changes in the Heart Rate Variability in Patients with Obstructive Sleep Apnea and Its Response to Acute CPAP Treatment , 2012, PloS one.

[64]  A. Goldberger,et al.  Nonlinear dynamics in sudden cardiac death syndrome: Heartrate oscillations and bifurcations , 1988, Experientia.

[65]  Y. Shinohara,et al.  Platelet activation in patients with obstructive sleep apnea syndrome and effects of nasal-continuous positive airway pressure. , 2002, The Tokai journal of experimental and clinical medicine.

[66]  L. Ferini-Strambi,et al.  Cardiac autonomic function during sleep in several neuropsychiatric disorders , 1997, Journal of Neurology.

[67]  Shih-Jen Tsai,et al.  Reduced physiologic complexity is associated with poor sleep in patients with major depression and primary insomnia. , 2011, Journal of affective disorders.

[68]  H. Nagaraja,et al.  Heart rate variability: origins, methods, and interpretive caveats. , 1997, Psychophysiology.

[69]  M Ericson,et al.  Preoperative heart rate variability in relation to surgery outcome in refractory epilepsy , 2005, Neurology.

[70]  T. Tomson,et al.  Circadian Variation in Heart‐Rate Variability in Localization‐related Epilepsy , 2007, Epilepsia.

[71]  M. Uusitupa,et al.  Cardiac sympathovagal balance during sleep apnea episodes. , 1996, Clinical physiology.

[72]  M Vallverdú,et al.  Heart rate variability analysis based on time–frequency representation and entropies in hypertrophic cardiomyopathy patients , 2008, Physiological measurement.

[73]  J. Lacour,et al.  Reduced cardiac sympathetic autonomic tone after long-term nasal continuous positive airway pressure in obstructive sleep apnoea syndrome. , 1999, Clinical physiology.

[74]  Claire Médigue,et al.  Autonomic control of the cardiovascular system during sleep in normal subjects , 2002, European Journal of Applied Physiology.

[75]  E H HON,et al.  THE FETAL ELECTROCARDIOGRAM. IV. UNUSUAL VARIATIONS IN THE QRS COMPLEX DURING LABOR. , 1965, American journal of obstetrics and gynecology.

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

[77]  Sergio Cerutti,et al.  Entropy, entropy rate, and pattern classification as tools to typify complexity in short heart period variability series , 2001, IEEE Transactions on Biomedical Engineering.

[78]  C. Saper,et al.  Homeostatic, circadian, and emotional regulation of sleep , 2005, The Journal of comparative neurology.

[79]  D. Cardinali,et al.  Nonlinear analysis of heart rate variability within independent frequency components during the sleep–wake cycle , 2010, Autonomic Neuroscience.

[80]  C. Baumgartner,et al.  Electrocardiographic Changes at the Onset of Epileptic Seizures , 2003, Epilepsia.

[81]  Y. Kayama,et al.  Locus coeruleus neuronal activity during the sleep-waking cycle in mice , 2010, Neuroscience.

[82]  Paul Linkowski,et al.  Effects of Aging and Cardiac Denervation on Heart Rate Variability During Sleep , 2001, Circulation.

[83]  A. Porta,et al.  Heart rate variability explored in the frequency domain: A tool to investigate the link between heart and behavior , 2009, Neuroscience & Biobehavioral Reviews.

[84]  V. Somers,et al.  Nocturnal continuous positive airway pressure decreases daytime sympathetic traffic in obstructive sleep apnea. , 1999, Circulation.

[85]  R. Berry,et al.  Cardiac autonomic control in obstructive sleep apnea: effects of long-term CPAP therapy. , 2001, American journal of respiratory and critical care medicine.

[86]  Jun Lu,et al.  Critical Role of Dorsomedial Hypothalamic Nucleus in a Wide Range of Behavioral Circadian Rhythms , 2003, The Journal of Neuroscience.

[87]  P. Lavie,et al.  Power spectrum analysis and heart rate variability in Stage 4 and REM sleep: evidence for state‐specific changes in autonomic dominance , 1993, Journal of sleep research.

[88]  Salvatore Smirne,et al.  The impact of cyclic alternating pattern on heart rate variability during sleep in healthy young adults , 2000, Clinical Neurophysiology.

[89]  K. Miki,et al.  Functional role of diverse changes in sympathetic nerve activity in regulating arterial pressure during REM sleep. , 2011, Sleep.

[90]  P. Cistulli,et al.  Obstructive sleep apnea in obese noninsulin-dependent diabetic patients: effect of continuous positive airway pressure treatment on insulin responsiveness. , 1994, The Journal of clinical endocrinology and metabolism.

[91]  M. A. Arias,et al.  CPAP decreases plasma levels of soluble tumour necrosis factor-α receptor 1 in obstructive sleep apnoea , 2008, European Respiratory Journal.

[92]  C. Saper,et al.  Sleep State Switching , 2010, Neuron.

[93]  Liborio Parrino,et al.  Cyclic alternating pattern (CAP): the marker of sleep instability. , 2012, Sleep medicine reviews.

[94]  G. Billman Heart Rate Variability – A Historical Perspective , 2011, Front. Physio..

[95]  T Kobayashi,et al.  Augmented very low frequency component of heart rate variability during obstructive sleep apnea. , 1996, Sleep.

[96]  M. Terzano,et al.  The cyclic alternating pattern as a physiologic component of normal NREM sleep. , 1985, Sleep.

[97]  David Watts Apnea , 1997, The Lancet.

[98]  R. Berg,et al.  A Systematic Review and Meta-analysis , 2010 .

[99]  A Malliani,et al.  Sympathovagal balance: a reappraisal. , 1998, Circulation.

[100]  C. Negrão,et al.  Sleep-related changes in hemodynamic and autonomic regulation in human hypertension , 2009, Journal of hypertension.

[101]  A. Porta,et al.  Cardiac autonomic control in Brugada syndrome patients during sleep: the effects of sleep disordered breathing. , 2013, International journal of cardiology.

[102]  Douglas Tapper,et al.  Sleep apnea. , 2018, Otolaryngologic clinics of North America.

[103]  S. Redline,et al.  Sleep disturbances: time to join the top 10 potentially modifiable cardiovascular risk factors? , 2011, Circulation.

[104]  B. O. Genc,et al.  Analysis of 24-hour heart rate variations in patients with epilepsy receiving antiepileptic drugs , 2011, Epilepsy & Behavior.

[105]  M. Esler Clinical application of noradrenaline spillover methodology: delineation of regional human sympathetic nervous responses. , 1993, Pharmacology & toxicology.

[106]  T. Tomson,et al.  Carbamazepine affects autonomic cardiac control in patients with newly diagnosed epilepsy , 2003, Epilepsy Research.

[107]  F. Abboud,et al.  Sympathetic-nerve activity during sleep in normal subjects. , 1993, The New England journal of medicine.

[108]  E. Hon,et al.  The fetal electrocardiogram , 1965 .

[109]  I. Churchill-Davidson,et al.  Oxygenation in radiotherapy. II. Clinical application. , 1957, The British journal of radiology.

[110]  W Szelenberger,et al.  Nonlinear dynamics of the cardiovascular parameters in sleep and sleep apnea. In memory of Alberto Malliani (1935-2006)--a brave heart and beautiful mind. , 2006, Journal of physiology and pharmacology : an official journal of the Polish Physiological Society.

[111]  M Malik,et al.  Short- and long-term assessment of heart rate variability for risk stratification after acute myocardial infarction. , 1996, The American journal of cardiology.

[112]  R. Backs,et al.  Effects of obstructive sleep apnea on autonomic cardiac control during sleep , 2009, Sleep and Breathing.

[113]  Lino Nobili,et al.  Quantitative analysis of sleep EEG microstructure in the time–frequency domain , 2004, Brain Research Bulletin.

[114]  Alberto Porta,et al.  Short-Term Complexity of Cardiac Autonomic Control during Sleep: REM as a Potential Risk Factor for Cardiovascular System in Aging , 2011, PloS one.

[115]  Sabine Van Huffel,et al.  Autonomic effects of refractory epilepsy on heart rate variability in children: influence of intermittent vagus nerve stimulation , 2011, Developmental medicine and child neurology.

[116]  D. T. Kaplan,et al.  Aging and the complexity of cardiovascular dynamics. , 1991, Biophysical journal.

[117]  Heikki Huikuri,et al.  Sleep stage dependent patterns of nonlinear heart rate dynamics in postmenopausal women , 2007, Autonomic Neuroscience.

[118]  L. Berkman,et al.  A multivariate analysis of health-related practices: a nine-year mortality follow-up of the Alameda County Study. , 1982, American journal of epidemiology.

[119]  J. Kurths,et al.  The application of methods of non-linear dynamics for the improved and predictive recognition of patients threatened by sudden cardiac death. , 1996, Cardiovascular research.

[120]  C. Brooks,et al.  Functional significance of coactivation of vagal and sympathetic cardiac nerves. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[121]  O. Devinsky,et al.  Decrease of sympathetic cardiovascular modulation after temporal lobe epilepsy surgery. , 2002, Brain : a journal of neurology.

[122]  G. Billman The LF/HF ratio does not accurately measure cardiac sympatho-vagal balance , 2013, Front. Physio..

[123]  V. Somers,et al.  Sympathetic nerve activity in obstructive sleep apnoea. , 2003, Acta physiologica Scandinavica.

[124]  Raffaele Ferri,et al.  Heart rate variability during sleep in children with partial epilepsy , 2002, Journal of sleep research.

[125]  E. Lindberg,et al.  Heart rate variability during sleep and sleep apnoea in a population based study of 387 women , 2009, Clinical physiology and functional imaging.