Physiological stress markers during breath-hold diving and SCUBA diving Marion Marlinge, Mathieu Coulange, Richard C. Fitzpatrick, Romain Delacroix, Alexie Gabarré, Nicolas Lainé, Jennifer Cautela, Pierre Louge, Alain Boussuges, Jean-Claude Rostain, et al. To cite this version: Marion Marlinge, Mathieu Coulange, Richard C. Fitzpatrick, Romain Delacroix, Alexie Gabarré, et al.. Physiological stress markers during breath-hold diving and SCUBA diving. Physiological Reports, Wiley, 2019, 7 (6), 10.14814/phy2.14033. hal-02620844 HAL Id: hal-02620844 https://hal.inrae.fr/hal-02620844 Submitted on 26 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License Physiological Reports ISSN 2051-817X ORIGINAL RESEARCH Physiological stress markers during breath-hold diving and SCUBA diving Marion Marlinge1,2, Mathieu Coulange1,3, Richard C. Fitzpatrick4, Romain Delacroix1,2,5, Alexie Gabarre1,2,5, Nicolas Laine2,3, Jennifer Cautela6, Pierre Louge6, Alain Boussuges1,7, Jean-Claude Rostain1,Regis Guieu1,2 & Fabrice C. Joulia1,8,* 1 C2VN, INSERM, INRA, Aix-Marseille Universite (AMU), Marseille, France 2 APHM: Assistance Publique des Hopitaux de Marseille, Marseille, France 3 Department of Hyperbaric Medicine, Sainte Marguerite University Hospital, Marseille, France 4 School of Medical Sciences, University of New South Wales, Sydney, New South Wales, Australia 5 Laboratory of Biochemistry, Timone University Hospital, Marseille, France 6 Department of Cardiology, North Hospital, Marseille, France 7 HIA Saint Anne, Toulon, France 8 UFR STAPS Universite de Toulon, La Garde, France Keywords Abstract Apnea, biological stress markers, copeptin, cortisol, hypoxemia, SCUBA. This study investigated the sources of physiological stress in diving by com- paring SCUBA dives (stressors: hydrostatic pressure, cold, and hyperoxia), Correspondence apneic dives (hydrostatic pressure, cold, physical activity, hypoxia), and dry Fabrice C. Joulia, UFR STAPS, Universitede static apnea (hypoxia only). We hypothesized that despite the hypoxia induces Toulon, Avenue de l’Universite, 83130 La by a long static apnea, it would be less stressful than SCUBA dive or apneic Garde, France. dives since the latter combined high pressure, physical activity, and cold expo- Tel: (+33) 4 94142614 sure. Blood samples were collected from 12SCUBA and 12 apnea divers before Fax: (+33) 4 94142597 E-mail: [email protected] and after dives. On a different occasion, samples were collected from the apneic group before and after a maximal static dry apnea. We measured Funding Information changes in levels of the stress hormones cortisol and copeptin in each situa- This study was supported by Aix-Marseille tion. To identify localized effects of the stress, we measured levels of the car- Universite and Assistance Publique des diac injury markers troponin (cTnI) and brain natriuretic peptide (BNP), the ^ Hopitaux de Marseille. muscular stress markers myoglobin and lactate), and the hypoxemia marker ischemia-modified albumin (IMA). Copeptin, cortisol, and IMA levels Received: 13 December 2018; Revised: 21 February 2019; Accepted: 26 February 2019 increased for the apneic dive and the static dry apnea, whereas they decreased for the SCUBA dive. Troponin, BNP, and myoglobin levels increased for the doi: 10.14814/phy2.14033 apneic dive, but were unchanged for the SCUBA dive and the static dry apnea. We conclude that hypoxia induced by apnea is the dominant trigger Physiol Rep, 7 (6), 2019, e14033, for the release of stress hormones and cardiac injury markers, whereas cold or https://doi.org/10.14814/phy2.14033 and hyperbaric exposures play a minor role. These results indicate that sub- jects should be screened carefully for pre-existing cardiac diseases before undertaking significant apneic maneuvers. Introduction there are similarities and differences in the mechanisms by which these different dives could physiologically stress SCUBA diving and apneic diving (breath-hold diving) the body. both involve immersion, increased hydrostatic pressure, SCUBA diving, while breathing air, is a physiological physical activity, and cold exposure. They are different in stressor through cold exposure, increased hydrostatic that apneic dives are hypoxic (and hypercapnic), whereas pressure, and hyperbaric inspired O2. SCUBA dives have SCUBA dives are hyperoxic through hyperbaric inspired been reported to induce increased levels of stress hor- air and often high O2 concentration N2/O2 mixes. Thus, mones prolactin (Anegg et al. 2002) and cortisol related ª 2019 The Authors. Physiological Reports published by Wiley Periodicals, Inc. on behalf of 2019 | Vol. 7 | Iss. 6 | e14033 The Physiological Society and the American Physiological Society Page 1 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Stress Hormone Release in Diving M. Marlinge et al. to immersion depth (Zarezadeh and Azarbayjani 2014). This study examines sources of physiological stress in These dives have been associated with transient endothe- diving as revealed by circulating stress markers. We com- lial dysfunction (Culic et al. 2014) likely mediated pared responses to three conditions; (1) dry static apnea through hyperbaric O2, and have been linked to reduced (hypoxia), (2) apneic dives (hypoxia, pressure, cold, activ- cognitive performance (Pourhashemi et al. 2016) and ity), and (3) SCUBA dives (hyperbaric O2, pressure, cold, stress cardiomyopathy (Baber et al. 2016). On the other activity). To identify additional stress effects of hydro- hand, improved well-being and reduced stress have been static pressure, cold and activity from hypoxic stress reported recently in recreational SCUBA divers (Beneton effects, we compared apneic dives with dry static apnea et al. 2017). performed on land at rest. To identify the relative stresses Spearfishing competitions and recreational apneic div- of hypoxic and hyperoxic conditions, we compared apneic ing commonly involve 4–5 h of immersion with repeated dives with SCUBA dives. We hypothesized that the com- voluntary dynamic apneic phases that can represent more bined stress factors of cold and pressure exposure associ- than 2 h of apnea and, in temperate climates, the water is ated with physical activities during SCUBA and apneic often cold. Apneic hypoxia combined with endurance dives would be more stressful compared to the hypoxia physical activity, cold exposure, and increased hydrostatic strictly induced by a long static apnea. pressures can exert intense physiological stresses on divers. For example, a release of S100B, a marker of cere- Materials and Methods bral stress, has been described after a single apnea fol- lowed by a black out (Liner and Andersson 2009) or Subjects preceded by hyperventilation and glossopharyngeal insuf- flations (Andersson et al. 2009) suggesting a brain stress Thirty-six volunteers recruited from three populations during breath hold diving. However, such a release of participated to this experiment. Twelve men (mean age S100B has not been observed after a maximal static apnea 37 Æ 8 years) who were experienced apneic divers were (Kjeld et al. 2015) suggesting that this cerebral stress recruited during the French Spearfishing Championship could also be related to other factors than hypoxia. Expo- (Saint Raphael, July 2014). Twelve men (mean age sition to high pressure of dives was known to induce 51 Æ 10 years) who were experienced SCUBA divers were brain injury (Tamaki et al. 2010), hemoptysis, and pneu- recruited from the military diving school of St Mandrier, momediastinum (Henckes et al. 2011) and is often associ- France. Eight men (mean age 48 Æ 4 years) who were ated with increased plasma markers of oxidative stress not divers were recruited from departmental staff to serve (Theunissen et al. 2013). as a control group. Participant characteristics are summa- Despite the popularity of spearfishing and breath-hold rized in Table 1. All subjects were nonsmokers, without diving worldwide, the stress effects of repeated voluntary medication, inflammatory, cardiovascular, or respiratory apnea are poorly understood and require investigation. disease. Subjects gave written informed consent prior to Commonly, voluntary apnea has been studied through the study, which was approved by the Aix-Marseille the cardiovascular adaptation of the diving reflex (Berg- University Human Research Ethics (South Marseille) and man et al. 1972; Andersson et al. 2004), which protects conducted in line with the principles of the Declaration the heart and brain against hypoxia (Breskovic et al. of Helsinki. 2011). However, the triggers, release and actions of stress hormones during breath-hold diving are poorly under- Protocol stood. Accurately measured levels of stress hormones and cardiac markers could provide a better understanding of Four studies were undertaken. The practicalities