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Going to Extremes of Lung Physiology–Deep Breath-Hold Diving

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Going to Extremes of Lung Physiology–Deep Breath-Hold Diving fphys-12-710429 July 5, 2021 Time: 19:22 # 1 REVIEW published: 09 July 2021 doi: 10.3389/fphys.2021.710429 Going to Extremes of Lung Physiology–Deep Breath-Hold Diving Kay Tetzlaff1*, Frederic Lemaitre2, Christof Burgstahler1, Julian A. Luetkens3 and Lars Eichhorn4 1 Department of Sports Medicine, University Hospital of Tübingen, Tübingen, Germany, 2 Faculte des Sciences du Sport et de l’Education Physique, Universite de Rouen, Rouen, France, 3 Department of Radiology, University Hospital Bonn, Bonn, Germany, 4 Department of Anesthesiology and Intensive Care Medicine, University Hospital Bonn, Bonn, Germany Breath-hold diving involves environmental challenges, such as water immersion, hydrostatic pressure, and asphyxia, that put the respiratory system under stress. While training and inherent individual factors may increase tolerance to these challenges, the limits of human respiratory physiology will be reached quickly during deep breath-hold dives. Nonetheless, world records in deep breath-hold diving of more than 214 m of seawater have considerably exceeded predictions from human physiology. Investigations of elite breath-hold divers and their achievements revised our understanding of possible physiological adaptations in humans and revealed techniques Edited by: such as glossopharyngeal breathing as being essential to achieve extremes in breath- Costantino Balestra, hold diving performance. These techniques allow elite athletes to increase total lung Haute École Bruxelles-Brabant capacity and minimize residual volume, thereby reducing thoracic squeeze. However, (HE2B), Belgium the inability of human lungs to collapse early during descent enables respiratory gas Reviewed by: Enrico M. Camporesi, exchange to continue at greater depths, forcing nitrogen (N2) out of the alveolar space USF Health, United States to dissolve in body tissues. This will increase risk of N2 narcosis and decompression Giorgos K. Sakkas, University of Thessaly, Greece stress. Clinical cases of stroke-like syndromes after single deep breath-hold dives *Correspondence: point to possible mechanisms of decompression stress, caused by N2 entering the Kay Tetzlaff vasculature upon ascent from these deep dives. Mechanisms of neurological injury and [email protected] inert gas narcosis during deep breath-hold dives are still incompletely understood. This Specialty section: review addresses possible hypotheses and elucidates factors that may contribute to This article was submitted to pathophysiology of deep freediving accidents. Awareness of the unique challenges Environmental, Aviation and Space to pulmonary physiology at depth is paramount to assess medical risks of deep Physiology, a section of the journal breath-hold diving. Frontiers in Physiology Keywords: breath-hold diving, apnea, glossopharyngeal insufflation, decompression, narcosis, lung Received: 16 May 2021 Accepted: 16 June 2021 Published: 09 July 2021 INTRODUCTION Citation: Tetzlaff K, Lemaitre F, Breath-hold diving (synonyms: apnea diving, freediving, and skin diving) has been practiced by Burgstahler C, Luetkens JA and humans throughout history for leisure and commercial purposes, e.g., harvesting sea food or Eichhorn L (2021) Going to Extremes of Lung Physiology–Deep spearfishing. More recently breath-hold diving also became a competitive sports activity, inspired Breath-Hold Diving. by the famous competition between Italian freediver Enzo Maiorca, who breached the 50 m depth Front. Physiol. 12:710429. in 1960, and French freediver Jacques Mayol, who was the first to reach 100 m in 1976. These doi: 10.3389/fphys.2021.710429 achievements also raised interest by the scientific community, as they challenged the pertinent Frontiers in Physiology| www.frontiersin.org 1 July 2021| Volume 12| Article 710429 fphys-12-710429 July 5, 2021 Time: 19:22 # 2 Tetzlaff et al. Going to Extremes of Lung Physiology understanding of the depth limits of breath-hold diving. This total lung capacity (TLC) (Carey et al., 1956; Agostoni, 1965). review aims at elucidating the particular challenges of deep As intrathoracic gas will be compressed during a breath-hold human breath-hold diving to respiratory physiology, and to dive with increasing depth, volume halves at 10 m depth (2 atm highlight the serious medical risks associated with competitive absolute pressure), and will be reduced to one third of its initial freediving to great depths. volume at 20 m depth. Thus, in a subject with an RV of 20% of TLC, the critical lung volume will be reached at 40 m depth (5 atm absolute pressure) when the TLC is compressed to one fifth THE DIVING RESPONSE of its initial volume. Intrathoracic pressure will become lower than ambient pressure and therefore pressure of body tissues and A major challenge for humans inherent to the aquatic blood. With further descent beyond RV the distensibility limit environment is the lack of oxygen, as mammals cannot breathe of the blood-containing structures in the chest may be reached, under water. Thus, oxygen depletion relies on air inhaled into resulting in possible fluid extravasation and pulmonary trauma the lungs before breath-holding, and intrinsic oxygen stores including alveolar damage and intra-alveolar bleeding. bound in blood to hemoglobin, in muscle to myoglobin and The classical concept that the RV/TLC ratio determined the in smaller amounts also physically dissolved in plasma. Diving maximum breath-holding diving depth had been consistent with mammals have developed a major physiological adaptation to early research in professional Japanese and Korean diving women withstand asphyxia for prolonged dive duration called the diving harvesting seafood in the Sea of Japan and Yellow Sea. Teruoka response. This fundamental mechanism enabling organisms to (1932) was the first to extensively study the so called Japanese maintain life during asphyxia has been demonstrated in many “Ama” women divers and documented maximum diving depths terrestrial species and involves both bradycardia and peripheral of up to 25 m, although anecdotally reported dives were up vasoconstriction. In humans, the diving response is characterized to 45 m. A study in US Navy submarine escape training tank by a synergistic sympathetic and parasympathetic activiation and instructors reported larger TLC and vital capacity compared to catecholamine increase (Heusser et al., 2009; Eichhorn et al., laboratory control personnel, supporting the concept that a lower 2017), redistribution of blood flow to maintain adequate oxygen RV/TLC ratio was beneficial to achieve greater freediving depths supply to hypoxia sensible organs (Joulia et al., 2009; Eichhorn (Carey et al., 1956). Divers had 14.6% higher than predicted et al., 2018), and reduced heart rate (Perini et al., 2008; Costalat vital capacity; a longitudinal follow-up over 1 year attributed et al., 2021). More recently, active contraction of the spleen the higher VC to training adaptation rather than a selection has also been attributed to the human diving response without effect. Song et al.(1963) measured RV and TLC in Korean diving clear relationship. woman and controls and determined an average ratio of 25% that The human diving response is highly variable and can allowed dives to approx. 30 m. There was no significant difference be modified by physiological as well as emotional factors. between divers and controls, however, diving women tended to Elite breath-hold divers have developed certain adaptions to have a lower RV/TLC ratio per corresponding age group. repeated apnea training, such as greater tolerance to hypoxia Subsequent reports confirmed that subjects achieving record and hypercapnia, and a more pronounced diving response. For depths had favorable individual RV/TLC ratios, allowing them some factors like the blunted chemosensitivity to hypercapnia to go deeper than predicted. US Navy diver Robert Croft had a a possible genetic predisposition has been discussed while TLC of 9.1 L and an RV of 1.3 L providing a ratio that would apnea training may modify these or other physiologic and enable him to dive safely up to 60 m depth (Schaefer et al., 1968). psychophysical factors (Bain et al., 2018). In fact, the predicted values according to his age, height and sex Trained freedivers achieve average breath-hold times of 5 min would have amounted to 6.9 and 2 L for TLC and RV,respectively, under resting conditions (Hansel et al., 2009), allowing them allowing him to hardly reach 30 m. Thus, favorably low RV/TLC in theory to reach great depths with assisted descent using a ratios enabled certain individuals to reach record depths that ballast, and ascending with lifting bags. In fact, total dive time for exceeded the depth range of 30–40 m known from professional documented world record dives were less than 5 min. Maximum breath-hold divers. achievable breath hold time is not determining the maximal However, Robert Croft reached 66 m depth in 1968 and French diving depth, but physiological factors (lung size and compliance, freediver Jacques Mayol became the first to break the 70 m limit in cardiac fitness), blood redistribution, economization of diving the same year. These achievements alerted physiologists that the movements, equalization techniques, mental strength and other concept of RV/TLC determining maximum breath-hold diving factors influence the risk for serious hypoxemia upon ascent and depth needed to be refined. are therefore affecting the maximum diving depth. THORACIC BLOOD SHIFT THE RV/TLC RATIO Although the anatomy of the human lung,
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