Breath Hold Diving
Breath Hold Diving
ABSTRACT
WALTERSPACHER, S., T. SCHOLZ, K. TETZLAFF, and S. SORICHTER. Breath-Hold Diving: Respiratory Function on the Longer
Term. Med. Sci. Sports Exerc., Vol. 43, No. 7, pp. 1214–1219, 2011. Purpose: Extensive breath-hold (BH) diving imposes high
pulmonary stress by performing voluntary lung hyperinflation maneuvers (glossopharyngeal insufflation, GI), hyperinflating the lung
up to 50% of total lung capacity. Breath-hold durations of up to 10 min without oxygen support may also presume cerebral alterations
of respiratory drive. Little is known about the long-term effects of GI onto the pulmonary parenchyma and respiratory adaptation
BASIC SCIENCES
processes in this popular extreme sport. Methods: Lung function assessments and subsequent measures of pulmonary static compliance
were obtained for 5 min after GI in 12 elite competitive breath-hold divers (BHD) with a mean apnea diving performance of 6.6 yr.
Three-year follow-up measurements were performed in 4 BHD. Respiratory drive was assessed in steady-state measurements for
6% and 9% CO2 in ambient air. Results: Short-term pulmonary stress effects for static compliance during GI (13.75 LIkPaj1) could be
confirmed in these 12 divers without exhibiting permanent changes to the lungs’ distensibility (7.41 LIkPaj1) or lung function param-
eters as confirmed by the follow-up measurements and for 4 BHD after 3 yr (P 9 0.05). Respiratory drive was significantly reduced
in these BHD revealing a characteristic breathing pattern with a significant increase in V̇E and mouth occlusion pressure (P0.1) bet ween
free breathing and 6% CO2, as well as between 6% CO2 and 9% CO2 (all P G 0.001). Conclusion: BH diving with performance
of GI does not permanently alter pulmonary distensibility or impair ventilatory flows and volumes. A blunted response to elevated
CO2 concentrations could be demonstrated, which was supportive of the hypothesis that CO2 tolerance is a training effect due to BH
diving rather than being an inherited phenomenon. Key Words: LUNG COMPLIANCE, HYPERCAPNIA, GLOSSOPHARYNGEAL
INSUFFLATION, ADAPTATION, RESPIRATORY DRIVE
G
lossopharyngeal insufflation (GI) is a breathing detected in five of six BHD after performing GI in computed
technique that allows pumping air in to the lungs tomographic scans. No prospective lung function data have
by contractions of the upper pharyngeal muscles. been reported yet in elite competitive BHD.
It was initially adopted by patients experiencing respira- In the recent years, the boundaries of breath-hold dura-
tory insufficiency due to poliomyelitis (6,7) to increase off- tions (current world record = 11 min 35 s) and diving depths
respirator time. It has been reported more recently that (current word record = 214 m) have been continuously
competitive breath-hold divers (BHD) use GI to add air on pushed further (1), exposing BHD to both severe hypoxia
top of their fully inflated lungs to reach greater depths, store and hypercapnia during these challenges. Conflicting data
surplus oxygen, and add space for CO2 storage (21). How- exist whether excelling CO2 tolerance may be an inherited
ever, information about the short and possible long-term phenomenon (2,15) or an adaptation to frequent short-term
(patho)physiological effects of GI (21) is scarce. So far, hypercapnia as observed in other sports (8). Suggestions
there are only single reports on acute lung damage due to have been made that elite performance in BHD may be he-
BHD and GI (17,18,22). In a recent study by Chung et al. reditary, as shown in three BHD family members with di-
(4), asymptomatic signs of pneumomediastinum could be minished respiratory drive under hypercapnia (13,15); an
altered respiratory drive was also detected and postulated in
later studies (12,34).
We hypothesized that aging and constant performance of
Address for correspondence: Stephan Walterspacher, M.D., Department of
Pneumology, University Hospital Freiburg, Killianstr. 5, 79106 Freiburg, GI may alter pulmonary distensibility and therefore possibly
Germany; E-mail: [email protected]. induce long-term damage. In a previous study, we were able
Submitted for publication August 2010. to show a transient change in pulmonary static lung com-
Accepted for publication December 2010. pliance due to GI (34). Here, we performed a 3-yr follow-up
0195-9131/11/4307-1214/0 measurement in four divers from our preliminary study
MEDICINE & SCIENCE IN SPORTS & EXERCISEÒ group. Further, we measured pulmonary compliance during
Copyright Ó 2011 by the American College of Sports Medicine 5-min intervals in three consecutive sessions in a greater group
DOI: 10.1249/MSS.0b013e31820a4e0c of 12 experienced elite divers. To assess further adaptive
1214
Copyright © 2011 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
TABLE 1. Divers’ characteristics. measure for the comparison of lung volumes before and
BMI BSA BHD PB Static PB Depth during GI (VCGI).
Age (kgImj2) (m2) (months) Apnea (s) (m)
The esophageal pressure method was used for the mea-
1a 25 18.2 1.76 60 340 35
2a 34 26.0 1.9 106 362 56
surement of pulmonary compliance. Esophageal pressure
3a 38 27.2 2.15 103 304 32 was used as a determinant of transpulmonary pressure. All
4a 37 24.6 2.1 120 421 64 measurements were performed in a sitting position with the
5 34 22.8 2.13 36 365 37
6 46 22.9 2.04 48 460 125 subjects breathing quietly through the spirometer. Pressure
7 33 19.0 1.77 120 383 38 curves were recorded using a conventional balloon catheter
8 43 25.0 2.03 108 414 50
9 24 22.1 1.94 12 395 35 (nSpireÒ GmbH, Oberthulba, Germany) placed in the mid
10 30 20.8 1.74 12 469 50 third part of the esophagus. The esophageal balloon was
11 46 23.7 2.08 120 450 65
12 38 22.8 1.77 30 345 56
filled with 1.5 mL of air over a three-way tap and a syringe
Mean 35 23.1 1.98 79 383 52 for optimal pressure transduction; for compliance measure-
SD 7.3 3 0.15 40.7 46.6 29.4 ments during GI, the balloon was filled with 0.5 mL of air to
BMI, body mass index; BHD, breath hold diving; PB, personal best.
a
avoid signal disturbances. No recordings were done during
Divers from previous measurements.
esophageal contractions. For correct assessment of pulmo-
nary compliance, a standardization of volume history has
effects to hypercapnia during continuation of competitive been calculated according to the resting lung volume meas-
BASIC SCIENCES
breath-hold diving, we also investigated the respiratory drive urements. Dynamic compliance (Cdyn) was registered during
using the steady-state method (5) in this unrelated group of quiet breathing at a respiratory rate between 10 minj1 and
divers in adherence to our and other previous studies. 5 minj1. At least 10 closed curves with clearly determined
points of reversal at the end of inspiration and expiration
were registered, and the mean value was calculated. Static
compliance (Cstat) was carried out during gentle passive
METHODS
noninterrupted expiration from total lung capacity (Cstatrest)
The study protocol was approved by the Ethics Committee or after GI (CstatGI). At least three technically acceptable
of the Albert-Ludwigs-University at Freiburg, Germany, curves had to be achieved for calculation of Cstatrest. For
and the study was performed in accordance with the ethical determination of Cstat, the slope of the curve was manually
standards set by the latest Declaration of Helsinki. All sub- adjusted for perfect fit at 50%–80% of the calculated lung
jects signed their informed consent before the study. For eli- volume (MasterLabÒ; Viasys) (14).
gibility, the BHD had to present actual training records with a Subsequent measurements of Cstat were done as follows:
minimum annual diving record exceeding of 100 dives and Cstat was measured before (Cstatrest), at GImax (CstatGI), and
participation in three competitions per year. Only male sub- each minute for 5 min (Cstat1–5min) in three sessions after
jects were investigated (Table 1) and recruited via Internet and GI. GI was always performed without previous hyperventi-
the local diving communities. lation. These measurements were performed according to the
Baseline spirometry was assessed using a constant vol- measurement of Cstatrest.
ume body plethysmograph (MasterLabÒ; Viasys, Höchberg, Mouth occlusion pressure at 0.1 s (P0.1), tidal breathing
Germany) according to current ATS/ERS guidelines (25,35). ventilation per minute (V̇E), and breathing frequency ( fb)
Reference values for forced expiratory flows and volumes were measured as an equivalent of respiratory drive. For P0.1
as well as static volumes were calculated according to the resting measurements (P0.1 rest), the subjects were asked
technique described by Matthys et al. (24). Maximal inspi- to breathe freely through a mouthpiece with a nose clip.
ratory vital capacity (VC) was considered as a baseline Ten airway occlusions occurred at random order 0.1 s after
RESPIRATORY ADAPTATION IN BREATH-HOLD DIVERS Medicine & Science in Sports & Exercised 1215
Copyright © 2011 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
the onset of inspiration in a computer-controlled fashion
(MasterLabÒ; Viasys), with the mean P0.1 being automati-
cally calculated (3). The effect of CO2 on respiratory drive
was measured using mixtures of 6% CO2 (P0.1 6%) and 9%
CO2 (P0.1 9%) in ambient air using the steady-state method
(5). Drive measurements under 6% and 9% CO2 were started
after reaching a steady state in V̇E and fb. P0.1 measurements
were performed analogous to the resting measurements.
Additionally, blood gas samples were drawn from the arte-
rialized ear lobe (cobas b221; Roche Diagnostics, Grenzach-
Wyhlen, Germany), and body surface area (BSA) was
calculated according to Mosteller’s (26) method.
Data were analyzed using SigmaPlotÒ 11.2 for WindowsÒ
(SSI, San Jose, CA). Results are expressed as means T SD
or as median (range) if data were not normally distributed.
FIGURE 1—Compliance follow-up measurements for five consecutive
All variables were tested for normal distribution and equal minutes. Rest, resting measurement; GI, glossopharnygeal insufflation;
variance. Paired t-tests (Student’s t-test or Mann–Whitney Cstat, static compliance. CstatGI is significantly different from all other
measurements (P G 0.001).
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Copyright © 2011 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
TABLE 4. Blood gas samples.
Ambient Air Ambient Air + 6% CO2 Ambient Air + 9% CO2
PaO2 (mm Hg) PaCO2 (mm Hg) pH PaO2 (mm Hg) PaCO2 (mm Hg) pH PaO2 (mm Hg) PaCO2 (mm Hg) pH
1 80.8 41 7.381 87.3 48.2 7.336 110.1 64.6 7.251
2 — — — — — — — — —
3 81.4 37.4 7.413 102.2 52.2 7.33 115.9 66.4 7.267
4 78.1 35.9 7.429 — — — 112.9 59.1 7.279
5 85.4 37.4 7.422 107.3 45.7 7.371 113.9 63.3 7.28
6 76.1 29.3 7.482 125.3 42.8 7.379 — — —
7 96 27.3 7.512 72.4 47.8 7.357 — — —
8 77.9 37.8 7.422 97.7 45 7.378 119.4 61.8 7.295
9 89.1 35.1 7.421 104.6 47.1 7.349 114.2 59.8 7.279
10 80.8 28.5 7.441 106 47.2 7.328 114.1 58.7 7.264
11 74.1 37.5 7.409 94.4 47.1 7.339 122.2 62.2 7.264
12 80.2 42.2 7.364 97.6 51.9 7.317 112.1 65.2 7.25
Mean 81.81 35.40 7.43 99.48 47.50 7.35 114.98 62.34 7.27
SD 6.27 4.97 0.04 13.82 2.87 0.02 3.73 2.77 0.01
PaCO2, arterial partial pressure of carbon dioxide; PaO2, arterial partial pressure of oxygen.
hyperinflating up to 50% above total lung capacity (23). compliance has been shown not to be age dependent so that
BASIC SCIENCES
Our study in 12 elite BHD for the first time shows that significant aging effects can be neglected (14).
persistent competitive breath-hold diving using the GI tech- In magnetic resonance imaging during GI maneuvers, full
nique does not impose deleterious long-term effects onto reversibility of the transient hyperinflation with herniation
the pulmonary parenchyma. The increase seen in ventilatory of the lung beneath the sternum and enlargement of the
volumes may rather indicate a training effect of GI. Further, costodiaphragmatic angle had been shown previously (11).
the investigation of respiratory drive regarding CO2 re- This is in line with the findings of velocity encoding cine
sponse supported the evidence that increased tolerance of magnetic resonance imaging of the main pulmonary artery
high-level CO2 resembles a training effect rather than an showing a complete reversibility of hemodynamic parame-
inherited phenomenon. ters mimicking pulmonary hypertension during GI (10).
In a preceding study, we showed a transient change in In contrast to our previous findings on the time course of
pulmonary static lung compliance due to GI indicating high pulmonary static compliance after GI (n = 5 divers) (34),
stress to the lung tissue during hyperinflation (34). Extreme here we did not observe a statistically significant differ-
transpulmonary pressures during GI up to 109 cm H2O (23) ence between measurements of Cstat at baseline and Cstat
and hyperinflation may lead to parenchymal changes in the after 1 min (Cstat1min). Looking at absolute values in the
lung tissue as seen in pulmonary barotraumas during me- current group of 12 divers, a higher mean value of Cstat1min
chanical ventilation on the intensive care unit (28). The cur- was observed (7.41 LIkPaj1 (n = 12) vs 5.36 LIkPaj1 (n = 5),
rent findings in the follow-up measurements of four divers all P 9 0.05). The lack of difference between Cstat at GI and
constantly performing BHD with GI revealed no changes to Cstat1min may therefore be due to the higher sample size in
their lungs’ distensibility (Table 3). All resting values of Cstat the current study. The absolute value for Cstat at GI, how-
and Cdyn were within the normal range; also, pulmonary ever, was close to our previous data (13.75 LIkPaj1 (n = 12)
vs 13.21 LIkPaj1 (n = 5)).
In the group of four divers who were available for a 3-yr
follow-up pulmonary function testing, mean ventilatory
volumes had increased over time (Table 3). This somewhat
unexpected finding was in line with earlier studies that re-
ported positive effects on lung volumes from GI after a 5-wk
training in competitive swimmers and a cross-sectional
study comparing lung volumes between novice and more
experienced BHD (20,27). We had anticipated to find a de-
cline in forced expiratory volumes, should GI cause delete-
rious effects to the airways and lung tissue on the longer
term. Indeed, in scuba divers who were of comparable age
to our BHD, a decrease in forced expiratory volume in 1 s
of about 100 mL was found after a 3-yr follow-up that was
attributable to the effects of diving exposure (33). Although
the sample size of the group of BHD who were available
FIGURE 2—Steady-state measurement of respiratory drive using 6% for follow-up was rather small, the lack of a deleterious
and 9% CO2 in ambient air (fb, breathing frequency; VE, tidal volume;
BSA, body surface area; P0.1, mouth occlusion pressure). For statistical effect was in line with the findings in the larger group of
significance levels, please refer to the results section. BHD we investigated here. The mean breath-hold diving
RESPIRATORY ADAPTATION IN BREATH-HOLD DIVERS Medicine & Science in Sports & Exercised 1217
Copyright © 2011 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
performance of 6.6 yr, with the maximum being 10 yr, does cannot be the only determination of a successful BHD.
further support the evidence that the stress on the pulmonary However, low-response subjects might be prone to excel
parenchyma is transient and reversible. It should be em- in breath-hold diving or related sports. This is in line with
phasized that long-term effects may occur in divers with findings of reduced ventilatory responses in other sports
more extreme exposures such as very deep diving, which such as underwater hockey (8) or tank instructors (30).
causes numerous other effects on the body and the lungs Whether GI has additional enhancing effects on CO2 tol-
(21). In our BHD, no subject except for diver 6 reached erance may be speculated but is not supported by the cur-
depth levels beyond 70 m (Table 1). However, the current rent study.
results do indicate that extensive use of GI for breath-hold A limitation of the present study is the lack of a control
diving at more shallow depths can be considered a safe group. However, data from our previous study may serve as
procedure regarding possible long-term damage to the pul- control because the study setup was identical except for the
monary parenchyma. measurement of respiratory drive under 9% CO2 and normal
A reduced respiratory drive has been shown previously data may be considered from the studies by Grassi et al. (15)
in studies measuring ventilatory response in hyperoxia and and Lambertsen (19) using the same technique. For pulmo-
hypercapnia (16) and during immersion accompanied by nary compliance, current reference values exist and may be
both hyperoxia and hypercapnia (9). For the first time and in referred to (14). Moreover, the follow-up was only possible
line with findings of Grassi et al. (15) in three elite BHD in a limited number of four subjects who were willing to
BASIC SCIENCES
family members, we could show a blunted response to CO2 undergo all of the demanding procedures again. The lack of
using a steady-state CO2 challenge in ambient air in a greater an impairment in lung function as an indicator of damage
group of 12 unrelated elite BHD (5). On the contrary, ven- due to GI was in accordance with the cross-sectional data of
tilatory response to inhaled CO2 was shown to be signifi- samples of BHD with long-lasting GI experience published
cantly different when monozygous and dizygous twins were by us and others. However, this was the first study with a
studied, revealing that personality factors seemed to influ- longitudinal design to provide long-term pulmonary data
ence the frequency response to CO2 (2). In this even larger in individual elite BHD subjects. We cannot exclude, how-
group, we could now show a blunted response to 6% and 9% ever, that there are deleterious effects in susceptible subjects
CO2 in ambient air with a characteristic breathing pattern who may give up BHD or escape clinical investigation.
focusing on increased V̇E with steady fb (Fig. 2). This was Further, a selection bias cannot be ruled out because of the
also observed in a study by Ivancev et al. (16) using a ramp recruitment method of the divers via Internet and the local
protocol for inducing hypercapnia with hyperoxia (29). Our diving communities.
unrelated BHD revealed the same blunted response to CO2 In conclusion, the present study is the first prospective
when normalized for BSA as shown by Grassi et al. (15) follow-up on BHD lung function. The main finding was that
with an average of 9 LIminj1Imj2 for divers at 52 torr repeated GI in elite BHD does not permanently alter pul-
PETCO2 versus 12 LIminj1Imj2 in control subjects and in monary distensibility because all changes to the pulmonary
the study by Lambertsen (19) with 31 LIminj1 at 50 mm Hg compliance remain transient and lung function parameters
PETCO2. Schaefer (31) demonstrated two different ventila- remain stable. Also, respiratory drive measurements revealed
tory response types classifying a high-response group (higher a distinct pattern of blunted ventilatory response to elevated
tidal volume, higher breathing frequency) and a low-response CO2 concentrations indicating this phenomenon being asso-
group for resting breathing and under various CO2 concen- ciated with BH training rather than being inherited.
trations in normal subjects. The low-response breathing pat-
tern was also seen in tank instructors and divers and may
therefore serve as an adaptation marker to elevated CO2 There was no special funding supporting this study.
concentrations (32). The same type of low response is seen in All authors declare no conflict of interest regarding this study.
The authors thank all divers for their participation.
BHD. We therefore postulate that breath-hold diving results The results of the present study do not constitute endorsement
in a trainable adaptation to increased CO2 levels; genetics by the American College of Sports Medicine.
REFERENCES
1. AIDA - Worldwide Federation for breath-hold diving [Internet]. 5. Clark TJ. The measurement of ventilatory response to CO2. Br J
Lausanne (Switzerland): AIDA; [cited 2010 Nov 12]. Available Dis Chest. 1968;62(3):113–25.
from: http://www.aida-international.org/. 6. Dail CW. FGlossopharyngeal breathing_ by paralyzed patients: a
2. Arkinstall WW, Nirmel K, Klissouras V, Milic-Emili J. Genetic preliminary report. Calif Med. 1951;75(3):217–8.
differences in the ventilatory response to inhaled CO2. J Appl 7. Dail CW, Affeldt JE, Collier CR. Clinical aspects of glossophar-
Physiol. 1974;36(1):6–11. yngeal breathing; report of use by one hundred postpoliomyelitic
3. ATS/ERS. Statement on respiratory muscle testing. Am J Respir patients. J Am Med Assoc. 1955;158(6):445–9.
Crit Care Med. 2002;166(4):518–624. 8. Davis FM, Graves MP, Guy HJ, Prisk GK, Tanner TE. Carbon
4. Chung SC, Seccombe LM, Jenkins CR, Frater CJ, Ridley LJ, dioxide response and breath-hold times in underwater hockey
Peters MJ. Glossopharyngeal insufflation causes lung injury in players. Undersea Biomed Res. 1987;14(6):527–34.
trained breath-hold divers. Respirology. 2010;15(5):813–7. 9. Delapille P, Verin E, Tourny-Chollet C, Pasquis P. Ventilatory
Copyright © 2011 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
responses to hypercapnia in divers and non-divers: effects of glossopharyngeal insufflation and exsufflation beyond normal
posture and immersion. Eur J Appl Physiol. 2001;86(1):97–103. lung volumes in competitive breath-hold divers. J Appl Physiol.
10. Eichinger M, Puderbach M, Smith H, et al. Magnetic resonance- 2007;102(3):841–6.
compatible-spirometry: principle, technical evaluation and appli- 24. Matthys H, Zaiss A, Theissen J, Virchow J, Werner P. Def-
cation. Eur Respir J. 2007;30(5):972–9. initions, predicted values and measures for diagnosis of ob-
11. Eichinger M, Walterspacher S, Scholz T, et al. Lung hyperinfla- structive, restrictive as well as combined ventilatory disorders for
tion: foe or friend? Eur Respir J. 2008;32(4):1113–6. clinical lung function diagnostics. Atemw-Lungenkrkh. 1995;21(3):
12. Ferretti G. Extreme human breath-hold diving. Eur J Appl Physiol. 130–8.
2001;84(4):254–71. 25. Miller MR, Hankinson J, Brusasco V, et al. Standardisation of
13. Ferretti G, Costa M, Ferrigno M, et al. Alveolar gas composition spirometry. Eur Respir J. 2005;26(2):319–38.
and exchange during deep breath-hold diving and dry breath holds 26. Mosteller RD. Simplified calculation of body-surface area. N Engl
in elite divers. J Appl Physiol. 1991;70(2):794–802. J Med. 1987;317(17):1098.
14. Galetke W, Feier C, Muth T, Ruehle K, Borsch-Galetke E, 27. Nygren-Bonnier M, Gullstrand L, Klefbeck B, Lindholm P. Effects
Randerath W. Reference values for dynamic and static pulmonary of glossopharyngeal pistoning for lung insufflation in elite swim-
compliance in men. Respir Med. 2007;101(8):1783–9. mers. Med Sci Sports Exerc. 2007;39(5):836–41.
15. Grassi B, Ferretti G, Costa M, et al. Ventilatory responses to hy- 28. Petersen GW, Baier H. Incidence of pulmonary barotrauma in a
percapnia and hypoxia in elite breath-hold divers. Respir Physiol. medical ICU. Crit Care Med. 1983;11(2):67–9.
1994;97(3):323–32. 29. Read DJ. A clinical method for assessing the ventilatory response
16. Ivancev V, Palada I, Valic Z, et al. Cerebrovascular reactivity to to carbon dioxide. Australas Ann Med. 1967;16(1):20–32.
hypercapnia is unimpaired in breath-hold divers. J Physiol. 2007; 30. Schaefer KE. The Role of Carbon Dioxide in the Physiology of
582(Pt 2):723–30. Human Diving. Washington (DC): National Academy of Science;
BASIC SCIENCES
17. Jacobson FL, Loring SH, Ferrigno M. Pneumomediastinum after 1955. p. 131–9.
lung packing. Undersea Hyperb Med. 2006;33(5):313–6. 31. Schaefer KE. Respiratory pattern and respiratory response to CO2.
18. Kiyan E, Aktas S, Toklu AS. Hemoptysis provoked by voluntary J Appl Physiol. 1958;13(1):1–4.
diaphragmatic contractions in breath-hold divers. Chest. 2001; 32. Schaefer KE. Effect of prolonged diving training. In: Lambertsen,
120(6):2098–100. CJ, Greenbaum, LJ, editors. Proceedings Second Symposium on
19. Lambertsen CJ. Carbon dioxide and respiration in acid–base ho- Underwater Physiology. Washington (DC): National Academy of
meostasis. Anesthesiology. 1960;21642–51. Sciences; 1963. p. 271–8.
20. Lemaitre F, Clua E, Andreani B, Castres I, Chollet D. Ventilatory 33. Skogstad M, Thorsen E, Haldorsen T. Lung function over the first
function in breath-hold divers: effect of glossopharyngeal insuf- 3 years of a professional diving career. Occup Environ Med.
flation. Eur J Appl Physiol. 2010;108(4):741–7. 2000;57(6):390–5.
21. Lindholm P, Lundgren CEG. The physiology and pathophysiology 34. Tetzlaff K, Scholz T, Walterspacher S, et al. Characteristics
of human breath-hold diving. J Appl Physiol. 2009;106(1):284–92. of the respiratory mechanical and muscle function of com-
22. Liner MH, Andersson JPA. Pulmonary edema after competitive petitive breath-hold divers. Eur J Appl Physiol. 2008;103(4):
breath-hold diving. J Appl Physiol. 2008;104(4):986–90. 469–75.
23. Loring SH, O’Donnell CR, Butler JP, Lindholm P, Jacobson F, 35. Wanger J, Clausen JL, Coates A, et al. Standardisation of the
Ferrigno M. Transpulmonary pressures and lung mechanics with measurement of lung volumes. Eur Respir J. 2005;26(3):511–22.
RESPIRATORY ADAPTATION IN BREATH-HOLD DIVERS Medicine & Science in Sports & Exercised 1219
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