Physiology, pathophysiology and (mal)adaptations to chronic apnoeic training: a state-of-the-art review

Abstract

Breath-hold diving is an activity that humans have engaged in since antiquity to forage for resources, provide sustenance and to support military campaigns. In modern times, breath-hold diving continues to gain popularity and recognition as both a competitive and recreational sport. The continued progression of world records is somewhat remarkable, particularly given the extreme hypoxaemic and hypercapnic conditions, and hydrostatic pressures these athletes endure. However, there is abundant literature to suggest a large inter-individual variation in the apnoeic capabilities that is thus far not fully understood. In this review, we explore developments in apnoea physiology and delineate the traits and mechanisms that potentially underpin this variation. In addition, we sought to highlight the physiological (mal)adaptations associated with consistent breath-hold training. Breath-hold divers (BHDs) are evidenced to exhibit a more pronounced diving-response than non-divers, while elite BHDs (EBHDs) also display beneficial adaptations in both blood and skeletal muscle. Importantly, these physiological characteristics are documented to be primarily influenced by training-induced stimuli. BHDs are exposed to unique physiological and environmental stressors, and as such possess an ability to withstand acute cerebrovascular and neuronal strains. Whether these characteristics are also a result of training-induced adaptations or genetic predisposition is less certain. Although the long-term effects of regular breath-hold diving activity are yet to be holistically established, preliminary evidence has posed considerations for cognitive, neurological, renal and bone health in BHDs. These areas should be explored further in longitudinal studies to more confidently ascertain the long-term health implications of extreme breath-holding activity.

Keywords: Apnoea; Bone health; Breath-hold diving; Haematology; Skeletal muscle; Spleen.

Fig. 1

Schematic representation depicting: (i) pre-apnoeic strategies evidenced to contribute towards attaining longer apnoeic durations, (ii) the role of resting characteristics on apnoeic capabilities and (iii) the physiological modifications induced during static apnoeic attempts and their role in influencing apnoeic length. Arrows up (↑) and down (↓) within the framed box indicate an increase or decrease of the associated variable. Dotted arrow lines (▪▪▪▪▪▪) indicate the link between pre-apnoeic strategies/resting characteristics and apnoeic durations. Abbreviations: BR beetroot juice, CBF cerebral blood flow, CD capillary density, CHO carbohydrates, CO₂  carbon dioxide, GI glossopharyngeal insufflation, Hb haemoglobin, Hct haematocrit, HR heart rate, IDM involuntary diaphragmatic movements, MAP mean arterial pressure, Mb myoglobin, MCV mean cell volume, MIT mitochondria, O₂  oxygen, PNA parasympathetic nervous system, R₉₅  diffusion distance, RV residual volume, SF sharing factor, SNA sympathetic nervous system, TLC total lung capacity, VC vital capacity. Supporting literature is denoted by the numbers, where; 1 = Asmussen and Kristiansson (1968), 2 = Ayers et al. (1972), 3 = Bae et al. (2003), 4 = Baković et al. (2003), 5 = Bakovic et al. (2013), 6 = Chicco et al. (2014), 7 = Dujic et al. (2008), 8 = Eichhorn et al. (2017), 9 = Eichhorn et al. (2018), 10 = Elia et al. (2019b), 11 = Elia et al. (2021b), 12 = Engan et al. (2012), 13 = Espersen et al. (2002), 14 = Ferretti (2001), 15 = Fredén et al. (1978), 16 = Gardner (1996), 17 = Ghiani et al. (2016), 18 = Hayashi et al. (1997), 19 = Heistad et al. (1968), 20 = Heusser et al. (2009), 21 = Hoiland et al. (2017), 22 = Ilardo et al. (2018), 23 = Joulia et al. (2009), 24 = Kjeld et al. (2018), 25 = Kutti et al. (1977), 26 = Kyhl et al. (2016), 27 = Landsberg (1975), 28 = Lemaitre et al. (2015), 29 = Lin (1982), 30 = Lindholm et al. (2007), 31 = Loring et al. (2007), 32 = Olsson et al. (1976), 33 = Overgaard et al. (2006), 34 = Palada et al. (2007), 35 = Patrician and Schagatay (2017), 36 = Paulev et al. (1990), 37 = Richardson et al. (2005), 38 = Schagatay and Holm (1996), 39 = Schagatay and Lodin-Sundström (2014), 40 = Schagatay et al. (2012), 41 = Shamsuzzaman et al. (2014), 42 = Steinback et al. (2010), 43 = Sterba and Lundgren (1988), 44 = Vestergaard and Larsson (2019), 45 = Whittaker and Irvin (2007)

Fig. 2

Schematic representation depicting current knowledge concerning the (mal)adaptations associated with long-term exposures to apnoea-related activities. Abbreviations: BMC, bone mineral content; BMD, bone mineral density; CD, capillary density; CKD, chronic kidney disease; Hb, haemoglobin; Mb, myoglobin; MIT, mitochondria; RBC, red blood cell; RTC, reticulocyte; R₉₅ , diffusion distance. Supporting literature is denoted by the numbers, where; 1 = Bae et al. (2003), 2 = Bouten et al. (2019), 3 = Doerner et al. (2018), 4 = Elia et al. (2019b), 5 = Elia et al. (2020), 6 = Engan et al. (2013), 7 = Fernandez et al. (2017), 8 = Hwang et al. (2006), 9 = Johansson and Schagatay (2012), 10 = Kjeld et al. (2018), 11 = Kohshi et al. (2014), 12 = Nygren-Bonnier et al. (2007), 13 = Oh et al. (2017), 14 = Potkin and Uzsler (2006), 15 = Seo et al. (2018), 16 = Tanaka et al. (2016).  Figure created with BioRender.com