Cardiovascular magnetic resonance assessment of acute cardiovascular effects of voluntary apnoea in elite divers

L Eichhorn, J Doerner, J A Luetkens, J M Lunkenheimer, R C Dolscheid-Pommerich, F Erdfelder, R Fimmers, J Nadal, B Stoffel-Wagner, H H Schild, A Hoeft, B Zur, C P Naehle, L Eichhorn, J Doerner, J A Luetkens, J M Lunkenheimer, R C Dolscheid-Pommerich, F Erdfelder, R Fimmers, J Nadal, B Stoffel-Wagner, H H Schild, A Hoeft, B Zur, C P Naehle

Abstract

Background: Prolonged breath holding results in hypoxemia and hypercapnia. Compensatory mechanisms help maintain adequate oxygen supply to hypoxia sensitive organs, but burden the cardiovascular system. The aim was to investigate human compensatory mechanisms and their effects on the cardiovascular system with regard to cardiac function and morphology, blood flow redistribution, serum biomarkers of the adrenergic system and myocardial injury markers following prolonged apnoea.

Methods: Seventeen elite apnoea divers performed maximal breath-hold during cardiovascular magnetic resonance imaging (CMR). Two breath-hold sessions were performed to assess (1) cardiac function, myocardial tissue properties and (2) blood flow. In between CMR sessions, a head MRI was performed for the assessment of signs of silent brain ischemia. Urine and blood samples were analysed prior to and up to 4 h after the first breath-hold.

Results: Mean breath-hold time was 297 ± 52 s. Left ventricular (LV) end-systolic, end-diastolic, and stroke volume increased significantly (p < 0.05). Peripheral oxygen saturation, LV ejection fraction, LV fractional shortening, and heart rate decreased significantly (p < 0.05). Blood distribution was diverted to cerebral regions with no significant changes in the descending aorta. Catecholamine levels, high-sensitivity cardiac troponin, and NT-pro-BNP levels increased significantly, but did not reach pathological levels.

Conclusion: Compensatory effects of prolonged apnoea substantially burden the cardiovascular system. CMR tissue characterisation did not reveal acute myocardial injury, indicating that the resulting cardiovascular stress does not exceed compensatory physiological limits in healthy subjects. However, these compensatory mechanisms could overly tax those limits in subjects with pre-existing cardiac disease. For divers interested in competetive apnoea diving, a comprehensive medical exam with a special focus on the cardiovascular system may be warranted.

Trial registration: This prospective single-centre study was approved by the institutional ethics committee review board. It was retrospectively registered under ClinicalTrials.gov (Trial registration: NCT02280226 . Registered 29 October 2014).

Keywords: Apnoea; CMR; Cardiac function; Catecholamine; Hypoxia; hs-cT.

Conflict of interest statement

Ethics approval and consent to participate

This prospective single-centre study was registered under Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Illustration of the study protocol (CMR: cardiovascular magnetic resonance)
Fig. 2
Fig. 2
Left ventricular changes during apnoea. a) LV volumes: left ventricular volumes. b) LVEF: left ventricular ejection fraction, c) HR: heart rate, d) LVCO: left ventricular cardiac output (*p = < 0.05; **p = < 0.01; ***p = < 0.001; ****p = < 0.0001). Values are expressed as mean ± standard deviation
Fig. 3
Fig. 3
Representative image showing a progressive LV dilation over the course of apnoea in diastolic heart phase (subject 12)
Fig. 4
Fig. 4
Correlation of a) ΔHR (Apnoeaearly – Apnoealate) with ΔLVSV (Apnoeaearly – Apnoealate, panel and b) ΔLVEDV (Apnoeaearly – Apnoealate, panel respectively, using Spearman’s rank correlation (ΔHR with ΔLVSV: − 0.637, p = 0.008; ΔHR with ΔLVEDV: -0.592923; p = 0.0155). HR: heart rate, LVSV: left ventricular stroke volume; LVEDV: left ventricular end-diastolic volume
Fig. 5
Fig. 5
Stroke volumes of common carotid arteries during course ao apnoea. SV-CCA: stroke volume in common carotid arteries. Values are expressed as mean ± SD
Fig. 6
Fig. 6
Serum parameters of a) epinephrine, b) norepinephrine, c) NT pro-BNP and d) high sensitive Troponin (hsTrop) under apnoea

References

    1. Chen L, Sica AL, Greenberg H, Scharf SM. Role of hypoxemia and hypercapnia in acute cardiovascular response to periodic apneas in sedated pigs. Respir Physiol. 1998;111:257–269. doi: 10.1016/S0034-5687(98)00007-3.
    1. O’Donnell CP, King ED, Schwartz AR, Robotham JL, Smith PL. Relationship between blood pressure and airway obstruction during sleep in the dog. J Appl Physiol. 1994;77:1819–1828. doi: 10.1152/jappl.1994.77.4.1819.
    1. Eichhorn L, Erdfelder F, Kessler F, Doerner J, Thudium MO, Meyer R, et al. Evaluation of near-infrared spectroscopy under apnea-dependent hypoxia in humans. J Clin Monit Comput. 2015;29:749–757. doi: 10.1007/s10877-015-9662-2.
    1. Eichhorn L, Kessler F, Böhnert V, Erdfelder F, Reckendorf A, Meyer R, et al. A model to simulate clinically relevant hypoxia in humans. J Vis Exp JoVE. 2016:e54933.
    1. Heusser K, Dzamonja G, Tank J, Palada I, Valic Z, Bakovic D, et al. Cardiovascular regulation during apnea in elite divers. Hypertension. 2009;53:719–724. doi: 10.1161/HYPERTENSIONAHA.108.127530.
    1. Overgaard K, Friis S, Pedersen RB, Lykkeboe G. Influence of lung volume, glossopharyngeal inhalation and P(ET) O2 and P(ET) CO2 on apnea performance in trained breath-hold divers. Eur J Appl Physiol. 2006;97:158–164. doi: 10.1007/s00421-006-0156-2.
    1. Willie CK, Ainslie PN, Drvis I, MacLeod DB, Bain AR, Madden D, et al. Regulation of brain blood flow and oxygen delivery in elite breath-hold divers. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab. 2015;35:66–73. doi: 10.1038/jcbfm.2014.170.
    1. Lindholm P, Lundgren CE. The physiology and pathophysiology of human breath-hold diving. J Appl Physiol. 2009;106:284–292. doi: 10.1152/japplphysiol.90991.2008.
    1. Perini R, Tironi A, Gheza A, Butti F, Moia C, Ferretti G. Heart rate and blood pressure time courses during prolonged dry apnoea in breath-hold divers. Eur J Appl Physiol. 2008;104:1–7. doi: 10.1007/s00421-008-0771-1.
    1. Marabotti C, Piaggi P, Menicucci D, Passera M, Benassi A, Bedini R, et al. Cardiac function and oxygen saturation during maximal breath-holding in air and during whole-body surface immersion. Diving Hyperb Med. 2013;43:131–137.
    1. Gopal AS, King DL, King DL, Keller AM, Rigling R. Left ventricular volume and endocardial surface area by three-dimensional echocardiography: comparison with two-dimensional echocardiography and nuclear magnetic resonance imaging in normal subjects. J Am Coll Cardiol. 1993;22:258–270. doi: 10.1016/0735-1097(93)90842-O.
    1. Sprinkart AM, Luetkens JA, Träber F, Doerner J, Gieseke J, Schnackenburg B, et al. Gradient spin Echo (GraSE) imaging for fast myocardial T2 mapping. J Cardiovasc Magn Reson. 2015;17:12.
    1. Mosteller RD. Simplified calculation of body-surface area. N Engl J Med. 1987;317:1098.
    1. Lewis RP, Sandler H. Relationship between changes in left ventricular dimensions and the ejection fraction in man. Circulation. 1971;44:548–557. doi: 10.1161/01.CIR.44.4.548.
    1. Hoeft A, Sonntag H, Stephan H, Kettler D. The influence of anesthesia on myocardial oxygen utilization efficiency in patients undergoing coronary bypass surgery. Anesth Analg. 1994;78:857–866. doi: 10.1213/00000539-199405000-00006.
    1. Eichhorn L, Erdfelder F, Kessler F, Dolscheid-Pommerich RC, Zur B, Hoffmann U, et al. Influence of apnea-induced hypoxia on catecholamine release and cardiovascular dynamics. Int J Sports Med. 2017;38:85–91.
    1. Pingitore A, Gemignani A, Menicucci D, Di Bella G, De Marchi D, Passera M, et al. Cardiovascular response to acute hypoxemia induced by prolonged breath holding in air. Am J Physiol Heart Circ Physiol. 2008;294:H449–H455. doi: 10.1152/ajpheart.00607.2007.
    1. Batinic T, Utz W, Breskovic T, Jordan J, Schulz-Menger J, Jankovic S, et al. Cardiac magnetic resonance imaging during pulmonary hyperinflation in apnea divers. Med Sci Sports Exerc. 2011;43:2095–2101. doi: 10.1249/MSS.0b013e31821ff294.
    1. Cross TJ, Kavanagh JJ, Breskovic T, Johnson BD, Dujic Z. Dynamic cerebral autoregulation is acutely impaired during maximal apnoea in trained divers. PLoS One. 2014;9:e87598. doi: 10.1371/journal.pone.0087598.
    1. Laurino M, Menicucci D, Mastorci F, Allegrini P, Piarulli A, Scilingo EP, et al. Mind-body relationships in elite apnea divers during breath holding: a study of autonomic responses to acute hypoxemia. Front Neuroengineering. 2012;5:4. doi: 10.3389/fneng.2012.00004.
    1. Costalat G, Pichon A, Joulia F, Lemaître F. Modeling the diving bradycardia: toward an “oxygen-conserving breaking point”? Eur J Appl Physiol. 2015;115:1475–1484. doi: 10.1007/s00421-015-3129-5.
    1. Hoeft A, Korb H, Hellige G, Sonntag H, Kettler D. The energetics and economics of the cardiac pump function. Anaesthesist. 1991;40:465–478.
    1. Schipke JD. Cardiac efficiency. Basic Res Cardiol. 1994;89:207–240.
    1. Palada I, Obad A, Bakovic D, Valic Z, Ivancev V, Dujic Z. Cerebral and peripheral hemodynamics and oxygenation during maximal dry breath-holds. Respir Physiol Neurobiol. 2007;157:374–381. doi: 10.1016/j.resp.2007.02.002.
    1. Eichhorn L, Erdfelder F, Kessler F, Dolscheid-Pommerich RC, Zur B, Hoffmann U, et al. Influence of apnea-induced hypoxia on catecholamine release and cardiovascular dynamics. Int J Sports Med. 2016;
    1. Nakagawa O, Ogawa Y, Itoh H, Suga S, Komatsu Y, Kishimoto I, et al. Rapid transcriptional activation and early mRNA turnover of brain natriuretic peptide in cardiocyte hypertrophy. Evidence for brain natriuretic peptide as an “emergency” cardiac hormone against ventricular overload. J Clin Invest. 1995;96:1280–1287. doi: 10.1172/JCI118162.
    1. Sato Y, Yamada T, Taniguchi R, Nagai K, Makiyama T, Okada H, et al. Persistently increased serum concentrations of cardiac troponin T in patients with idiopathic dilated cardiomyopathy are predictive of adverse outcomes. Circulation. 2001;103:369–374. doi: 10.1161/01.CIR.103.3.369.
    1. Andersson JPA, Linér MH, Rünow E, Schagatay EKA. Diving response and arterial oxygen saturation during apnea and exercise in breath-hold divers. J Appl Physiol. 2002;93:882–886. doi: 10.1152/japplphysiol.00863.2001.
    1. Andersson JPA, Evaggelidis L. Arterial oxygen saturation and diving response during dynamic apneas in breath-hold divers. Scand J Med Sci Sports. 2009;19:87–91. doi: 10.1111/j.1600-0838.2008.00777.x.
    1. Foster GE, Sheel AW. The human diving response, its function, and its control. Scand J Med Sci Sports. 2005;15:3–12. doi: 10.1111/j.1600-0838.2005.00440.x.
    1. Bisogni V, Pengo MF, Maiolino G, Rossi GP. The sympathetic nervous system and catecholamines metabolism in obstructive sleep apnoea. J Thorac Dis. 2016;8:243–254.
    1. Busch DR, Lynch JM, Winters ME, McCarthy AL, Newland JJ, Ko T, et al. Cerebral blood flow response to hypercapnia in children with obstructive sleep apnea syndrome. Sleep. 2016;39:209–216. doi: 10.5665/sleep.5350.
    1. Alex R, Bhave G, Al-Abed MA, Bashaboyina A, Iyer S, Watenpaugh DE, et al. An investigation of simultaneous variations in cerebral blood flow velocity and arterial blood pressure during sleep apnea. Conf Proc Annu Int Conf IEEE Eng Med Biol Soc IEEE Eng Med Biol Soc Annu Conf. 2012;2012:5634–5637.
    1. Gilmartin GS, Tamisier R, Curley M, Weiss JW. Ventilatory, hemodynamic, sympathetic nervous system, and vascular reactivity changes after recurrent nocturnal sustained hypoxia in humans. Am J Physiol Heart Circ Physiol. 2008;295:H778–H785. doi: 10.1152/ajpheart.00653.2007.
    1. Mohsenin V. Obstructive sleep apnea and hypertension: a critical review. Curr Hypertens Rep. 2014;16:482. doi: 10.1007/s11906-014-0482-4.
    1. Kasai T, Bradley TD. Obstructive sleep apnea and heart failure: pathophysiologic and therapeutic implications. J Am Coll Cardiol. 2011;57:119–127. doi: 10.1016/j.jacc.2010.08.627.
    1. Geovanini GR, Gowdak LHW, Pereira AC, Danzi-Soares NJ, LOC D, Poppi NT, et al. OSA and depression are common and independently associated with refractory angina in patients with coronary artery disease. Chest. 2014;146:73–80. doi: 10.1378/chest.13-2885.
    1. Nieto FJ, Young TB, Lind BK, Shahar E, Samet JM, Redline S, et al. Association of sleep-disordered breathing, sleep apnea, and hypertension in a large community-based study. Sleep heart health study. JAMA. 2000;283:1829–1836. doi: 10.1001/jama.283.14.1829.
    1. Drager LF, Polotsky VY, O’Donnell CP, Cravo SL, Lorenzi-Filho G, Machado BH. Translational approaches to understanding metabolic dysfunction and cardiovascular consequences of obstructive sleep apnea. Am J Physiol Heart Circ Physiol. 2015;309:H1101–H1111. doi: 10.1152/ajpheart.00094.2015.
    1. Kolb JC, Ainslie PN, Ide K, Poulin MJ. Protocol to measure acute cerebrovascular and ventilatory responses to isocapnic hypoxia in humans. Respir Physiol Neurobiol. 2004;141:191–199. doi: 10.1016/j.resp.2004.04.014.
    1. Ivancev V, Bakovic D, Obad A, Breskovic T, Palada I, Joyner MJ, et al. Effects of indomethacin on cerebrovascular response to hypercapnea and hypocapnea in breath-hold diving and obstructive sleep apnea. Respir Physiol Neurobiol. 2009;166:152–158. doi: 10.1016/j.resp.2009.03.001.
    1. Shaikh ZF, Jaye J, Ward N, Malhotra A, de Villa M, Polkey MI, et al. Patent foramen ovale in severe obstructive sleep apnea: clinical features and effects of closure. Chest. 2013;143:56–63. doi: 10.1378/chest.12-0334.
    1. Rimoldi SF, Ott S, Rexhaj E, de Marchi SF, Allemann Y, Gugger M, et al. Patent foramen Ovale closure in obstructive sleep apnea improves blood pressure and cardiovascular FunctionNovelty and significance. Hypertension. 2015;66:1050–1057. doi: 10.1161/HYPERTENSIONAHA.115.06303.
    1. Smart D, Mitchell S, Wilmshurst P, Turner M, Banham N. Joint position statement on persistent foramen ovale (PFO) and diving. South Pacific underwater medicine society (SPUMS) and the United Kingdom sports diving medical committee (UKSDMC) Diving Hyperb Med. 2015;45:129–131.
    1. Lafère P, Balestra C, Caers D, Germonpré P. Patent Foramen Ovale (PFO), personality traits, and iterative decompression sickness. Retrospective analysis of 209 cases. Front Psychol. 2017;8:1328. doi: 10.3389/fpsyg.2017.01328.

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