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Relationship between sleep disordered breathing and heart rate turbulence in non-obese subjects

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Abstract

Heart rate turbulence (HRT) is regarded as a parameter of cardiac autonomic dysfunction. Several studies have suggested that patients with sleep disordered breathing (SDB) have an impaired HRT, which play a role in the relationship between SDB and risk of cardiovascular morbidity and mortality. However, the impact of SDB on HRT independent from obesity is still debatable. Data of eligible subjects who underwent sleep test and 24 h Holter electrocardiogram (ECG) recording from 2009–2012 were analyzed. HRT parameters, turbulence onset (TO), and turbulence slope (TS) in the 24 h recording, while awakening, and sleeping (TO-24 h, TO-awake, TO-sleep, TS-24 h, TS-awake, and TS-sleep, respectively) were compared across subjects with no-to-mild, moderate, and severe SDB. Univariable and multivariable regression analyses including TO or TS as a dependent variable were performed. Data from 41 subjects were evaluated. Compared with the no-to-mild and moderate SDB groups, in the severe SDB group, the TO-24 h and TO-awake were significantly greater, and the TS-24 h, TS-awake, and TS-sleep were significantly lower. In multivariable analyses, the apnea–hypopnea index (AHI) was correlated directly with TO-24 h (coefficient, 0.36; P = 0.03) and TO-awake (coefficient, 0.40; P = 0.01). SDB severity, as represented by AHI, is related to HRT impairments in non-obese subjects. SDB, independent from obesity, may affect cardiac autonomic dysfunction.

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References

  1. Kasai T, Floras JS, Bradley TD (2012) Sleep apnea and cardiovascular disease: a bidirectional relationship. Circulation 126:1495–1510

    Article  Google Scholar 

  2. Khoo MC, Kim TS, Berry RB (1999) Spectral indices of cardiac autonomic function in obstructive sleep apnea. Sleep 22:443–451

    Article  CAS  Google Scholar 

  3. Gami AS, Olson EJ, Shen WK, Wright RS, Ballman KV, Hodge DO, Herges RM, Howard DE, Somers VK (2013) Obstructive sleep apnea and the risk of sudden cardiac death: a longitudinal study of 10,701 adults. J Am Coll Cardiol 62:610–616

    Article  Google Scholar 

  4. Keller T, Hader C, De Zeeuw J, Rasche K (2007) Obstructive sleep apnea syndrome: the effect of diabetes and autonomic neuropathy. J Physiol Pharmacol 58(Suppl 5):313–318

    PubMed  Google Scholar 

  5. Ito R, Hamada H, Yokoyama A, Oshima M, Katayama H, Ohnishi H, Kadowaki T, Ishimaru S, Irifune K, Higaki J (2005) Successful treatment of obstructive sleep apnea syndrome improves autonomic nervous system dysfunction. Clin Exp Hypertens 27:259–267

    Article  Google Scholar 

  6. Szymanowska K, Piatkowska A, Nowicka A, Cofta S, Wierzchowiecki M (2008) Heart rate turbulence in patients with obstructive sleep apnea syndrome. Cardiol J 15:441–445

    PubMed  Google Scholar 

  7. Wiklund U, Olofsson BO, Franklin K, Blom H, Bjerle P, Niklasson U (2000) Autonomic cardiovascular regulation in patients with obstructive sleep apnoea: a study based on spectral analysis of heart rate variability. Clin Physiol 20:234–241

    Article  CAS  Google Scholar 

  8. La Rovere MT, Maestri R, Pinna GD, Sleight P, Febo O (2011) Clinical and haemodynamic correlates of heart rate turbulence as a non-invasive index of baroreflex sensitivity in chronic heart failure. Clin Sci (Lond) 121:279–284

    Article  Google Scholar 

  9. Balcioglu S, Arslan U, Turkoglu S, Ozdemir M, Cengel A (2007) Heart rate variability and heart rate turbulence in patients with type 2 diabetes mellitus with versus without cardiac autonomic neuropathy. Am J Cardiol 100:890–893

    Article  Google Scholar 

  10. Koyama J, Watanabe J, Yamada A, Koseki Y, Konno Y, Toda S, Shinozaki T, Miura M, Fukuchi M, Ninomiya M, Kagaya Y, Shirato K (2002) Evaluation of heart-rate turbulence as a new prognostic marker in patients with chronic heart failure. Circ J 66:902–907

    Article  Google Scholar 

  11. Moore RK, Groves DG, Barlow PE, Fox KA, Shah A, Nolan J, Kearney MT (2006) Heart rate turbulence and death due to cardiac decompensation in patients with chronic heart failure. Eur J Heart Fail 8:585–590

    Article  Google Scholar 

  12. Pinnacchio G, Lanza GA, Stazi A, Careri G, Coviello I, Mollo R, Crea F (2015) Determinants of heart rate turbulence in individuals without apparent heart disease and in patients with stable coronary artery disease. Europace 17:1855–1861

    Article  Google Scholar 

  13. Schmidt G, Malik M, Barthel P, Schneider R, Ulm K, Rolnitzky L, Camm AJ, Bigger JT Jr, Schomig A (1999) Heart-rate turbulence after ventricular premature beats as a predictor of mortality after acute myocardial infarction. Lancet 353:1390–1396

    Article  CAS  Google Scholar 

  14. Makikallio TH, Barthel P, Schneider R, Bauer A, Tapanainen JM, Tulppo MP, Schmidt G, Huikuri HV (2005) Prediction of sudden cardiac death after acute myocardial infarction: role of Holter monitoring in the modern treatment era. Eur Heart J 26:762–769

    Article  Google Scholar 

  15. Disertori M, Mase M, Rigoni M, Nollo G, Ravelli F (2016) heart rate turbulence is a powerful predictor of cardiac death and ventricular arrhythmias in postmyocardial infarction and heart failure patients: a systematic review and meta-analysis. Circ Arrhythm Electrophysiol 9:e004610

    Article  Google Scholar 

  16. Yang A, Schafer H, Manka R, Andrie R, Schwab JO, Lewalter T, Luderitz B, Tasci S (2005) Influence of obstructive sleep apnea on heart rate turbulence. Basic Res Cardiol 100:439–445

    Article  CAS  Google Scholar 

  17. Aytemir K, Deniz A, Yavuz B, Ugur Demir A, Sahiner L, Ciftci O, Tokgozoglu L, Can I, Sahin A, Oto A (2007) Increased myocardial vulnerability and autonomic nervous system imbalance in obstructive sleep apnea syndrome. Respir Med 101:1277–1282

    Article  Google Scholar 

  18. Erdem A, Dogan OT, Yontar OC, Epozturk K, Ozlu MF, Ozturk S, Ayhan SS, Erdem FH, Yazici M, Akkurt I, Talay F (2013) The pure effects of obstructive sleep apnea syndrome on cardiac autonomic functions: heart rate turbulence analysis. Eur Rev Med Pharmacol Sci 17:2778–2783

    CAS  PubMed  Google Scholar 

  19. Mrowka R, Persson PB, Theres H, Patzak A (2000) Blunted arterial baroreflex causes "pathological" heart rate turbulence. Am J Physiol Regul Integr Comp Physiol 279:R1171–1175

    Article  CAS  Google Scholar 

  20. Indumathy J, Pal GK, Pal P, Ananthanarayanan PH, Parija SC, Balachander J, Dutta TK (2015) Decreased baroreflex sensitivity is linked to sympathovagal imbalance, body fat mass and altered cardiometabolic profile in pre-obesity and obesity. Metabolism 64:1704–1714

    Article  CAS  Google Scholar 

  21. Fidan-Yaylali G, Yaylali YT, Erdogan C, Can B, Senol H, Gedik-Topcu B, Topsakal S (2016) The association between central adiposity and autonomic dysfunction in obesity. Med Princ Pract 25:442–448

    Article  Google Scholar 

  22. Erdem A, Uenishi M, Matsumoto K, Kucukdurmaz Z, Kato R, Sahin S, Yazici M (2012) Cardiac autonomic function in metabolic syndrome: a comparison of ethnic Turkish and Japanese patients. J Interv Card Electrophysiol 35:253–258

    Article  Google Scholar 

  23. Avsar A, Acarturk G, Melek M, Kilit C, Celik A, Onrat E (2007) Cardiac autonomic function evaluated by the heart rate turbulence method was not changed in obese patients without co-morbidities. J Korean Med Sci 22:629–632

    Article  Google Scholar 

  24. Bauer A, Malik M, Schmidt G, Barthel P, Bonnemeier H, Cygankiewicz I, Guzik P, Lombardi F, Muller A, Oto A, Schneider R, Watanabe M, Wichterle D, Zareba W (2008) Heart rate turbulence: standards of measurement, physiological interpretation, and clinical use: International Society for Holter and Noninvasive Electrophysiology Consensus. J Am Coll Cardiol 52:1353–1365

    Article  Google Scholar 

  25. Sawada Y, Ohtomo N, Tanaka Y, Tanaka G, Yamakoshi K, Terachi S, Shimamoto K, Nakagawa M, Satoh S, Kuroda S, Iimura O (1997) New technique for time series analysis combining the maximum entropy method and non-linear least squares method: its value in heart rate variability analysis. Med Biol Eng Comput 35:318–322

    Article  CAS  Google Scholar 

  26. Fujiwara Y, Kurokawa S, Asakura Y, Wakao Y, Nishiwaki K, Komatsu T (2007) Correlation between heart rate variability and haemodynamic fluctuation during induction of general anaesthesia: comparison between linear and non-linear analysis. Anaesthesia 62:117–121

    Article  CAS  Google Scholar 

  27. Nishimura A, Kasai T, Tamura H, Yamato A, Yasuda D, Nagasawa K, Okubo M, Narui K, Mori Y (2015) Relationship between sleep disordered breathing and diabetic retinopathy: Analysis of 136 patients with diabetes. Diabetes Res Clin Pract 109:306–311

    Article  Google Scholar 

  28. Sumida K, Hoshino J, Suwabe T, Kasai T, Hayami N, Mise K, Kawada M, Imafuku A, Hiramatsu R, Hasegawa E, Yamanouchi M, Sawa N, Narui K, Takaichi K, Ubara Y (2015) Sleep-disordered breathing in patients with polycystic liver and kidney disease referred for transcatheter arterial embolization. Clin J Am Soc Nephrol 10:949–956

    Article  Google Scholar 

  29. Hida W, Shindoh C, Miki H, Kikuchi Y, Okabe S, Taguchi O, Takishima T, Shirato K (1993) Prevalence of sleep apnea among Japanese industrial workers determined by a portable sleep monitoring system. Respiration 60:332–337

    Article  CAS  Google Scholar 

  30. Yagi H, Nakata S, Tsuge H, Yasuma F, Noda A, Morinaga M, Tagaya M, Nakashima T (2009) Significance of a screening device (Apnomonitor 5) for sleep apnea syndrome. Auris Nasus Larynx 36:176–180

    Article  Google Scholar 

  31. Collop NA, Anderson WM, Boehlecke B, Claman D, Goldberg R, Gottlieb DJ, Hudgel D, Sateia M, Schwab R and Portable Monitoring Task Force of the American Academy of Sleep M (2007) Clinical guidelines for the use of unattended portable monitors in the diagnosis of obstructive sleep apnea in adult patients. Portable monitoring task force of the American Academy of Sleep Medicine. J Clin Sleep Med 3:737–747

    Google Scholar 

  32. Cygankiewicz I (2013) Heart rate turbulence. Prog Cardiovasc Dis 56:160–171

    Article  Google Scholar 

  33. Carlson JT, Hedner J, Elam M, Ejnell H, Sellgren J, Wallin BG (1993) Augmented resting sympathetic activity in awake patients with obstructive sleep apnea. Chest 103:1763–1768

    Article  CAS  Google Scholar 

  34. Cooper VL, Bowker CM, Pearson SB, Elliott MW, Hainsworth R (2004) Effects of simulated obstructive sleep apnoea on the human carotid baroreceptor-vascular resistance reflex. J Physiol 557:1055–1065

    Article  CAS  Google Scholar 

  35. Carlson JT, Hedner JA, Sellgren J, Elam M, Wallin BG (1996) Depressed baroreflex sensitivity in patients with obstructive sleep apnea. Am J Respir Crit Care Med 154:1490–1496

    Article  CAS  Google Scholar 

  36. Bonsignore MR, Parati G, Insalaco G, Marrone O, Castiglioni P, Romano S, Di Rienzo M, Mancia G, Bonsignore G (2002) Continuous positive airway pressure treatment improves baroreflex control of heart rate during sleep in severe obstructive sleep apnea syndrome. Am J Respir Crit Care Med 166:279–286

    Article  Google Scholar 

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Research grants from the Okinaka Memorial Institute for Medical Research.

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Correspondence to Takatoshi Kasai.

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Drs. Kasai, and Tomita are affiliated with a department endowed by Philips Respironics, ResMed, Teijin Home Healthcare, and Fukuda Denshi.

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Kikuchi, T., Kasai, T., Tomita, Y. et al. Relationship between sleep disordered breathing and heart rate turbulence in non-obese subjects. Heart Vessels 34, 1801–1810 (2019). https://doi.org/10.1007/s00380-019-01430-0

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