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Epicardial fat accumulation is an independent marker of impaired heart rate recovery in obese patients with obstructive sleep apnea

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Abstract

Background

Sympathetic nervous system activation plays a pivotal role in obese patients with obstructive sleep apnea (OSA), contributing to increased cardiovascular risk. Epicardial adipose tissue (EAT) activates cardiac autonomic nervous system. Our main study objective was to investigate effects of these autonomic dysfunction factors on post-exercise heart rate recovery (HRR).

Methods

36 patients, referred for clinical assessment of obesity (BMI > 30 kg/m2), underwent overnight polysomnography, transthoracic echocardiography and cardiopulmonary exercise testing.

Results

Compared to non-OSA patients, OSA patients were older and displayed reduced body weight-indexed peak VO2. Cardiac output at peak exercise was similar among groups. Peak exercise arterio-venous oxygen content difference D[a-v]O2 was lower in OSA patients. In univariate linear analysis, age, AHI, EAT thickness, peak VO2 and diabetes were associated with blunted HRR. Multiple linear regression analysis showed that increased EAT thickness, AHI and diabetes were independently associated with lower HRR. For identical AHI value and diabetes status, HRR significantly decreased by 61.7% for every 1 mm increase of EAT volume (p = 0.011). If HRR was treated as a categorical variable, EAT [odds ratio (OR) 1.78 (95% confidence interval [CI] 1.19–2.66); p = 0.005], and type 2 diabetes [OR 8.97 (95% CI 1.16–69.10); p = 0.035] were the only independent predictors of blunted HRR.

Conclusions

Aerobic capacity and peak exercise D[a-v]O2 are impaired in obese OSA patients, suggesting abnormal peripheral oxygen extraction. EAT thickness is an independent marker of post-exercise HRR, which is a noninvasive marker of autonomic nerve dysfunction accompanying poor cardiovascular prognosis in obese patients.

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References

  1. Guarino D, Nannipieri M, Iervasi G, Taddei S, Bruno RM (2017) The role of the autonomic nervous system in the pathophysiology of obesity. Front Physiol 8:665. https://doi.org/10.3389/fphys.2017.00665

    Article  PubMed  PubMed Central  Google Scholar 

  2. Baguet JP, Barone-Rochette G, Tamisier R, Levy P, Pépin JL (2012) Mechanisms of cardiac dysfunction in obstructive sleep apnea. Nat Rev Cardiol 9:679–688. https://doi.org/10.1038/nrcardio.2012.141

    Article  CAS  Google Scholar 

  3. Parati G, Lombardi C, Castagna F, Mattaliano P, Filardi PP, Agostoni P, Italian Society of Cardiology (SIC) (2016) Heart failure and sleep disorders. Nat Rev Cardiol 13:389–403. https://doi.org/10.1038/nrcardio.2016.71

    Article  CAS  PubMed  Google Scholar 

  4. Floras JS (2018) Sleep apnea and cardiovascular disease: an enigmatic risk factor. Circ Res 122:1741–1764. https://doi.org/10.1161/CIRCRESAHA.118.310783

    Article  CAS  PubMed  Google Scholar 

  5. Tafelmeier M, Weizenegger T, Ripfel S et al (2018) Postoperative complications after elective coronary artery bypass grafting surgery in patients with sleep-disordered breathing. Clin Res Cardiol 107:1148–1159. https://doi.org/10.1007/s00392-018-1289-0

    Article  PubMed  Google Scholar 

  6. Reuter H, Herkenrath S, Treml M et al (2018) Sleep-disordered breathing in patients with cardiovascular diseases cannot be detected by ESS, STOP-BANG, and Berlin questionnaires. Clin Res Cardiol 107:1071–1078. https://doi.org/10.1007/s00392-018-1282-7

    Article  PubMed  Google Scholar 

  7. Omran H, Bitter T, Horstkotte D, Oldenburg O, Fox H (2018) Characteristics and circadian distribution of cardiac arrhythmias in patients with heart failure and sleep-disordered breathing. Clin Res Cardiol 107:965–974. https://doi.org/10.1007/s00392-018-1269-4

    Article  PubMed  Google Scholar 

  8. Desteghe L, Hendriks JML, McEvoy RD et al (2018) The why, when and how to test for obstructive sleep apnea in patients with atrial fibrillation. Clin Res Cardiol 107:617–631. https://doi.org/10.1007/s00392-018-1248-9

    Article  PubMed  Google Scholar 

  9. Strotmann J, Fox H, Bitter T et al (2018) Characteristics of sleep-disordered breathing in patients with atrial fibrillation and preserved left ventricular ejection fraction. Clin Res Cardiol 107:120–129. https://doi.org/10.1007/s00392-017-1163-5

    Article  PubMed  Google Scholar 

  10. Nakamura S, Asai K, Kubota Y, Murai K et al (2015) Impact of sleep-disordered breathing and efficacy of positive airway pressure on mortality in patients with chronic heart failure and sleep-disordered breathing: a meta-analysis. Clin Res Cardiol 104:208–216. https://doi.org/10.1007/s00392-014-0774-3

    Article  PubMed  Google Scholar 

  11. Cholidou KG, Manali ED, Kapsimalis F et al (2015) Heart rate recovery post 6-minute walking test in obstructive sleep apnea: cycle ergometry versus 6-minute walking test in OSA patients. Clin Res Cardiol 103:805–815. https://doi.org/10.1007/s00392-014-0721-3

    Article  Google Scholar 

  12. Okutucu S, Karakulak UN, Aytemir K, Oto A (2011) Heart rate recovery: a practical clinical indicator of abnormal cardiac autonomic function. Expert Rev Cardiovasc Ther 9:1417–1430. https://doi.org/10.1586/erc.11.149

    Article  PubMed  Google Scholar 

  13. Qiu S, Cai X, Sun Z et al (2017) Heart rate recovery and risk of cardiovascular events and all-cause mortality: a meta-analysis of prospective cohort studies. J Am Heart Assoc 6:e005505. https://doi.org/10.1161/JAHA.117.005505

    Article  PubMed  PubMed Central  Google Scholar 

  14. Arab C, Vanderlei LCM, da Silva Paiva L et al (2018) Cardiac autonomic modulation impairments in advanced breast cancer patients. Clin Res Cardiol 107:924–936. https://doi.org/10.1007/s00392-018-1264-9

    Article  PubMed  Google Scholar 

  15. Maeder MT, Ammann P, Schoch OD et al (2010) Determinants of postexercise heart rate recovery in patients with the obstructive sleep apnea syndrome. Chest 137:310–317. https://doi.org/10.1378/chest.09-1424

    Article  PubMed  Google Scholar 

  16. Kline CE, Crowley EP, Ewing GB et al (2013) Blunted heart rate recovery is improved following exercise training in overweight adults with obstructive sleep apnea. Int J Cardiol 67:1610–1615. https://doi.org/10.1016/j.ijcard.2012.04.108

    Article  Google Scholar 

  17. Gaborit B, Sengenes C, Ancel P, Jacquier A, Dutour A (2017) Role of epicardial adipose tissue in health and disease: a matter of fat? Compr Physiol 7:1051–1082. https://doi.org/10.1002/cphy.c160034

    Article  Google Scholar 

  18. Kim MK, Tanaka K, Kim MJ et al (2010) Epicardial fat tissue: relationship with cardiorespiratory fitness in men. Med Sci Sports Exerc 42:463–469. https://doi.org/10.1249/MSS.0b013e3181b8b1f0

    Article  PubMed  Google Scholar 

  19. Sengul C, Duman D (2011) The association of epicardial fat thickness with blunted heart rate recovery in patients with metabolic syndrome. Tohoku J Exp Med 224:257–262

    Article  Google Scholar 

  20. Akoumianakis I, Antoniades C (2017) The interplay between adipose tissue and the cardiovascular system: is fat always bad? Cardiovasc Res 113:999–1008. https://doi.org/10.1093/cvr/cvx111

    Article  CAS  PubMed  Google Scholar 

  21. Mariani S, Fiore D, Barbaro G et al (2013) Association of epicardial fat thickness with the severity of obstructive sleep apnea in obese patients. Int J Cardiol 167:2244–2249. https://doi.org/10.1016/j.ijcard.2012.06.011

    Article  PubMed  Google Scholar 

  22. Barone-Rochette G, Vivodtzev I, Tamisier R et al (2015) Left ventricular remodeling and epicardial fat volume in obese patients with severe obstructive sleep apnea treated by continuous positive airway pressure. Int J Cardiol 179:218–219. https://doi.org/10.1016/j.ijcard.2014.11.023

    Article  PubMed  Google Scholar 

  23. Mendelson M, Marillier M, Bailly S et al (2018) Maximal exercise capacity in patients with obstructive sleep apnoea syndrome: a systematic review and meta-analysis. Eur Respir J 51 Pii: 1702697. https://doi.org/10.1183/13993003.02697-2017

  24. Hoyos CM, Melehan KL, Liu PY, Grunstein RR, Phillips CL (2015) Does obstructive sleep apnea cause endothelial dysfunction? A critical review of the literature. Sleep Med Rev 20:15–26. https://doi.org/10.1016/j.smrv.2014.06.003

    Article  PubMed  Google Scholar 

  25. Wang J, Yu W, Gao M, Zhang F, Gu C, Yu Y, Wei Y (2015) Impact of obstructive sleep apnea syndrome on endothelial function, arterial stiffening, and serum inflammatory markers: An updated meta-analysis and metaregression of 18 studies. J Am Heart Assoc 4:e002454. https://doi.org/10.1161/JAHA.115.002454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Gea J, Casadevall C, Pascual S, Orozco-Levi M, Barreiro E (2012) Respiratory diseases and muscle dysfunction. Expert Rev Respir Med 6:75–90. https://doi.org/10.1586/ers.11.81

    Article  CAS  PubMed  Google Scholar 

  27. Hargens TA, Guill SG, Zedalis D, Gregg JM, Nickols-Richardson SM, Herbert WG (2008) Attenuated heart rate recovery following exercise testing in overweight young men with untreated obstructive sleep apnea. Sleep 31:104–110

    Article  Google Scholar 

  28. Zhou Q, Zhang L, Wang K et al (2014) Effect of interconnection between cervical vagus trunk, epicardial fat pad on sinus node function, and atrial fibrillation. Pacing Clin Electrophysiol 37:356–363. https://doi.org/10.1111/pace.12265

    Article  PubMed  Google Scholar 

  29. Parisi V, Rengo G, Perrone-Filardi P et al (2016) Increased epicardial adipose tissue volume correlates with cardiac sympathetic denervation in patients with heart failure. Circ Res 118:1244–1253. https://doi.org/10.1161/CIRCRESAHA.115.307765

    Article  CAS  PubMed  Google Scholar 

  30. Trayhurn P (2013) Hypoxia and adipose tissue function and dysfunction in obesity. Physiol Rev 93:1–21. https://doi.org/10.1152/physrev.00017.2012

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by a grant from the Clinical Research and Innovation Unit (DRCI) of the University Hospital of Martinique (2016).

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Correspondence to Remi Neviere.

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The authors report no relationships that could be construed as a conflict of interest.

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Astrid Montfort and Jocelyn Inamo equally contributed to this work.

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Monfort, A., Inamo, J., Fagour, C. et al. Epicardial fat accumulation is an independent marker of impaired heart rate recovery in obese patients with obstructive sleep apnea. Clin Res Cardiol 108, 1226–1233 (2019). https://doi.org/10.1007/s00392-019-01454-6

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  • DOI: https://doi.org/10.1007/s00392-019-01454-6

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