Large Lungs in Divers*

Natural Selection or a Training Effect?

Yochai Adir, MD; Avi Shupak, MD; Arie Laor, MD; and Daniel Weiler-Ravell, MD, FCCP

Background: Normal spirometry is required for medical clearance of professional divers in many countries. Divers frequently have unusually large lung volumes associated with a low ratio of FEV1 to FVC (FEV1%), suggestive of obstructive airways disease. We retrospectively analyzed the records of divers in the Israeli Navy with a low FEV1% who fulfilled the criteria for large lungs, to determine whether this might be the effect of training or natural selection. We also investigated changes in pulmonary function in relation to diving experience. Methods: A total of 171 divers with FEV1% < 80% on simple spirometry were evaluated. We conducted a retrospective analysis of lung function data for those subjects who met the criteria for large lungs. Results: One hundred nine of 171 divers with low FEV1% met the criteria for large lungs and were included in the study. Their average age was 25 years (range, 18 to 44 years), and their mean diving experience was 7 years (range, 0 to 26 years). No difference was found in FVC values between experienced and inexperienced divers. The mean forced expiratory flow at 50% of vital capacity was significantly reduced in the most experienced group compared with the novice or less experienced divers. No difference was found in the diffusing capacity of the lung for carbon monoxide between experienced and inexperienced divers. Conclusions: We suggest that large lungs may represent part of the natural selection for diving, rather than a training effect. Prolonged diving experience may result in the development of small airways disease. (CHEST 2005; 128:224 228)
Key words: diving; large lungs; long-term effects Abbreviations: Dlco diffusing capacity of the lung for carbon monoxide; FEF50 forced expiratory flow at 50% of vital capacity; FEV1% ratio of FEV1 to FVC; RV residual volume; TLC total lung capacity

pulmonary function is essential for divers, N ormal not only to ensure that they will be able to maintain high levels of physical activity, but also to avoid pulmonary barotrauma due to air trapping. Normal spirometry is a prerequisite for medical certification of nonrecreational diver candidates and is part of the annual medical examination of commercial divers.1,2 Several cross-sectional studies37 have shown that divers frequently have unusually large lung volumes
*From the Israel Naval Medical Institute (Drs. Adir and Shupak), Israel Defense Forces Medical Corps, the Department of Internal Medicine (Dr. Laor), and the Division of Respiratory Physiology and Chest Disease (Dr. Weiler-Ravell), Carmel Medical Center, Haifa, Israel. Manuscript received January 28, 2004; revision accepted December 15, 2004. Reproduction of this article is prohibited without written permission from the American College of Chest Physicians (www.chestjournal. org/misc/reprints.shtml). Correspondence to: Yochai Adir, MD, Israel Naval Medical Institute, PO Box 8040, 31 080 Haifa, Israel; e-mail: adir-sh@ zahav.net.il
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and a low ratio of FEV1 to FVC (FEV1%), suggestive of obstructive airways disease or airflow limitation. However, when a low FEV1% represents true airflow limitation, FEV1 is reduced, and residual volume (RV) is often increased, also called air trapping. For a low FEV1% to represent large lungs, FEV1 must be at least normal, and RV has to be low. Because a reduced FEV1% might represent airflow limitation and/or air trapping, which increases the risk of pulmonary barotrauma and reduces exercise capacity during a dive, divers with reduced FEV1% are required to undergo complete pulmonary function studies to exclude obstructive airways disease. Crosbie et al4,5 were the first to describe the phenomenon of large lungs in divers. Their lung function studies demonstrated a large FVC and increased FEV1, as well as low FEV1% with no other evidence of air trapping or obstructive airways disease. It is not known whether the considerable increase observed in FVC is the result of adaptation due to a training effect of diving on the respiratory muscles or whether it is an effect of selecClinical Investigations

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tion,8,9 although there are data relating high vital capacity to diving history.6,7 At the Israel Naval Medical Institute, we routinely perform spirometry as part of the annual medical fitness examination conducted on professional divers and as part of the prediving medical examination of diver candidates. Any diver or diver candidate with abnormal spirometry is required to undergo complete pulmonary function studies. We retrospectively analyzed the records of divers with a low FEV1% who fulfilled the criteria for large lungs in divers, to determine whether this might be the effect of training or natural selection. We also investigated changes in pulmonary function in those divers who were found to have large lungs in relation to diving experience. Materials and Methods
One hundred seventy-one divers with FEV1% 80% on simple spirometry (ST-250; Fukuda Sangyo; Chiba, Japan) during medical evaluation were referred for further investigation. Before testing, the spirometer was calibrated according to the recommendations of the American Thoracic Society.10 FVC, FEV1, and FEV1% were measured. The best result of at least three tests was used for evaluation. All of the pulmonary function tests were conducted in a single pulmonary function laboratory by the same technicians. Lung volumes (vital capacity, total lung capacity [TLC], RV, and RV/TLC ratio) were measured and calculated using a body plethysmograph (Bodyscreen II; Erich Jaeger; Wurzburg, Germany). Volumes and flows were corrected to body temperature and pressure, saturated. Single-breath diffusing capacity of the lung for carbon monoxide (Dlco) was measured according to the instructions of the manufacturer. Values were corrected for venous hemoglobin concentration. Dlco is expressed in standard temperature and pressure, dry. The criteria for large lungs were as follows: large FVC (FVC 100%), FEV1 90%, and no evidence of air trapping, as manifested by a ratio of RV to TLC 0.30.5 We conducted a retrospective analysis of lung function data for the nonsmoking divers who met these criteria. Comparison among groups was done by analysis of variance and linear regression analysis using SAS 6.03 (SAS Institute; Cary, NC). The scattergram was built with a 95% confidence interval.

Results Of the 171 divers with low FEV1%, 109 met the criteria for both large lungs and nonsmoking and were included in the study. The remaining 62 divers were excluded for the following reasons: 6 divers had large lungs but were smokers, and the other 56 divers had pulmonary function findings, suggestive of obstructive airflow limitation of unknown etiology. Twelve of these 56 divers were smokers. Thus, the 109 divers included in the study were healthy, nonsmoking males with no history, symptoms, or other evidence of obstructive airways disease. Physical examination and chest radiograph findings were normal in all subjects. Their average age was 25 years (range, 18 to 44 years), and their mean diving experience was 7 years (range, 0 to 26 years). This group was further divided into three subgroups according to age and diving experience (novice, less experienced, and experienced), and the results of the pulmonary function tests were analyzed for each subgroup (Table 1). No difference was found in FVC values between experienced and inexperienced divers. The mean forced expiratory flow at 50% of vital capacity (FEF50) was significantly reduced in the most experienced group compared with the novice or less experienced divers (p 0.05) [Fig 1]. No difference was found in the Dlco between experienced and inexperienced divers. Discussion During diving, the respiratory system must deal with increased gas density, the effects of immersion, and the use of breathing apparatus, all of which increase respiratory mechanical load.1117 Decompression stress and breathing high-oxygen concentrations can also have detrimental effects on pulmonary function.1113,18 Therefore, one of the major concerns that must be addressed when assessing pulmo-

Table 1Results of Lung Function Tests in the Diver Population*

Parameter Age range, yr No. Years diving FVC FEV1 FEF50 TLC RV ITGV Dlco All Divers 1844 109 7.03 7.2 118.24 13.6 101.56 9.6 69.18 15 110.75 12.93 113.25 31.16 113.54 22.06 94.68 16.89 Subgroup 1 1825 67 2.10 1.86 120.31 15.63 102.86 10.2 70.60 17.28 112.95 13.64 114.86 31.68 115.18 20.55 95.84 15.5 Subgroup 2 2635 28 11.82 2.99 113.78 7.90 99.10 6.64 68.92 10.78 105.6 11.32 109.57 32.5 111.62 23.8 84.75 18.39 Subgroup 3 3644 14 21.07 2.84 117.28 9.94 100.28 8.74 62.71 8.38 110.64 9.94 113.00 27.02 109.50 26.10 84.81 20.7

*Divers were arbitrarily classified into three groups according to their age and diving experience: novice, less experienced, and experienced divers. All values are percentage of predicted of normal. Values are given as mean SD, unless otherwise indicated. ITGV intrathoracic gas volume. p 0.05.
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Figure 1. A scattergram describing the relation between diving experience expressed in years of diving and the FEF50 of the diver population. The upper and lower lines represent the 95% confidence interval.

nary fitness to dive is whether specific lung diseases might predispose the diver to injuries unique to the diving environment. Lung function testing is a useful tool to discover clinically occult pulmonary abnormalities. This is the rationale for screening professional divers by referring those with abnormal spirometry results (FEV1, FVC, and FEV1% below predicted values) for further evaluation to exclude pulmonary disease.19 Obstructive lung disease and, in particular, asthma are the most common lung diseases that must be excluded in divers,20 due to concern about the possible occurrence of pulmonary barotrauma and arterial gas embolism as a result of air trapping.2123 Moreover, breathing cold, dry air during diving, as well as the greater demands made on the respiratory system underwater due to the physical exertion required, can lead to bronchospasm.14 In our diving population, asthma and other obstructive airways disease associated with air trapping are contraindications to commence or continue diving. However, an earlier study by Crosbie at al5 described a diver population in whom, despite abnormal spirometry manifesting as a low FEV1%, further evaluation revealed no evidence of obstructive airways disease. These divers had elevated FVC and TLC, a normal FEV1, and no air trapping (normal RV/TLC). Crosbie and colleagues4,5 named this phenomenon divers large lungs. It was shown that in divers up to the age of 30 years, FVC increased with years of diving and with increased diving depth.4,5 In contrast to this, there was no change in FEV1. This resulted in a large FVC and a decrease in the FEV1%, with no
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evidence of air trapping. It was noted, however, that in divers 30 years old, FVC declined despite continued diving, even when age was taken into account.4,5 This decrease may be related to divinginduced structural changes in the lung beyond the reduction in the elastic recoil of normal lungs due to aging. The phenomenon of increased FVC in divers may be attributed to a number of factors. Breathing dense air via breathing apparatus during diving results in increased inspiratory and expiratory resistance, leading to an increase in the work of breathing. The physical stress imposed by the underwater environment, together with the increased work of breathing, produces a breathing pattern characterized by high tidal volumes, which is maintained for prolonged periods.14 A previous study9 demonstrated that inspiratory muscle strength training near TLC and conditioning of the accessory muscles of the neck and chest wall may be important in expanding the chest at large lung volumes, and can cause a shift in the optimal length of the inspiratory muscles such that larger forces can be generated at a shorter muscle length. A change in lung compliance and an increase in alveolar size can lead to a shift of the volume-pressure curve of the lung and chest wall and an increase in TLC.24 As opposed to those studies,4,5,9,24 others raised the question whether the considerable increase observed in FVC is indeed the result of adaptation due to a training effect of diving on the respiratory muscles, or whether it is advantageous for the novice diver, helping him in the selection process toward becoming a professional
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diver. Divers quickly learn that breathing with high tidal volumes enables them to work for a longer time when using self-contained gas supplies. It is possible that large lungs (an increased FVC at the expense of a reduced RV) may be due to hypertrophy of the thoracic wall and diaphragm muscles. This might be a training effect of breathing against an increased respiratory load. In turn, the stronger respiratory muscles might facilitate overcoming the increased work of breathing during diving. The characteristics of our diver population are similar to those reported in the literature.6 But in contrast to others, we did not find a correlation between large FVC and diving experience. This supports the notion that there is a natural selection for professional divers, and that the increase in FVC is not due to a training effect on the respiratory muscles. The present study indicates that increased diving experience correlates with reduced expiratory flows at low lung volumes, possibly indicating pathological changes in the lung periphery, suggesting small airways disease. This is in agreement with previous investigations of the long-term effects of diving on pulmonary function.6,7,25 Tetzlaff et al26 found that divers had lower midexpiratory flow values at 25% of vital capacity than control subjects, and that their midexpiratory flows at 25% and 50% of vital capacity were inversely related to years of diving. Skogstad et al27 demonstrated that professional divers initially belong to a selected group having a large FVC, and that exposure to the diving environment mostly affects small airway conductance. These changes were related to breathing hyperbaric air, venous gas microembolism during decompression, and hyperoxic exposure, and they may lead to small airways disease in experienced divers. To test whether the development of small airways disease is correlated with morphologic abnormalities, Reuter et al28 compared divers and nondiver control subjects using high-resolution CT scanning. They did not find radiologic evidence of the development of small airways disease in divers. The question of whether diving causes a reduction in diffusion capacity is still a controversial issue. Some studies found no correlation between changes in Dlco and age or diving parameters, whereas others reported reduced Dlco in experienced divers.29 32 The pathogenesis of this reduction in pulmonary gas transfer function is not clear. Shortterm exposure to deep saturation diving causes a reduction in diffusion capacity, which may recover with time.33 This has been attributed to low-level oxygen toxicity occurring as a result of breathing increased partial pressures of oxygen at depth and to the effects of venous gas emboli on the pulmonary
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microcirculation.33,34 Animal studies35,36 demonstrated that venous gas embolism encountered during decompression after hyperbaric exposure may cause an inflammatory response and capillary endothelial damage in the pulmonary microcirculation. It seems that repetitive inflammatory responses and injury may cause irreversible damage to the alveolarcapillary membrane. Our results show that there was no significant change in diffusion capacity between the experienced diver populations compared with novice divers. The average depth and bottom times for our diver population were 25 to 35 m of seawater for 30 to 40 min, respectively, occurring mostly during dives using compressed air. Because the decompression requirement and the inert gas load are low, and the exposure to relatively high oxygen partial pressures in these dives is too short to result in lung injury, this may explain our findings. In summary, our findings lead us to concur with previous authors that in a diving population, a low FEV1% does not necessarily indicate obstructive airways disease, but may simply reflect the phenomenon of divers large lungs. We suggest that large lungs represent part of the natural selection for diving, rather than a training effect. Prolonged diving experience may result in the development of small airways disease. References
1 Gorman D, Veale A. SPUMS policy on asthma and fitness for diving. SPUMS J 1995; 25:213215 2 UK Sport Diving Medical Committee. Medical standards. Available at: http://www.uksdmc.co.uk. Accessed June 16, 2005 3 Hong SK, Rahn H, Kang DH, et al. Diving pattern, lung volumes, and alveolar gas of the Korean diving woman (ama). J Appl Physiol 1963; 18:457 465 4 Crosbie WA, Clarke MB, Cox RAF, et al. Physical characteristics and ventilatory function of 404 commercial divers working in the North Sea. Br J Ind Med 1977; 34:19 25 5 Crosbie WA, Reed JW, Clarke MC. Functional characteristics of the large lungs found in commercial divers. J Appl Physiol 1979; 46:639 645 6 Davey IS, Cotes JE, Reed JW. Relationship of ventilatory capacity to hyperbaric exposure in divers. J Appl Physiol 1984; 56:16551658 7 Watt SJ. Effect of commercial diving on ventilatory function. Br J Ind Med 1985; 42:59 62 8 Bouhuys A, Beck GJ. Large lungs in divers [letter]? J Appl Physiol 1979; 47:1136 1137 9 Clanton TL, Dixon GF, Drake J, et al. Effects of swim training on lung volumes and inspiratory muscle conditioning. J Appl Physiol 1987; 62:39 46 10 Standardization of spirometry, 1994 update. American Thoracic Society. Am J Respir Crit Care Med 1995; 152:1107 1136 11 Brubakk AO, Neuman TS, eds. Bennett and Elliotts physiology and medicine of diving. 5th ed. Edinburgh, Scotland: Saunders, 2003
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12 Edmonds C, Lowry C, Pennefather J, et al, eds. Diving and subaquatic medicine. 4th ed. London, UK: Arnold, 2002 13 Bove AA, ed. Bove and Davis diving medicine. 3rd ed. Philadelphia, PA: W.B. Saunders Company, 1997 14 Lundgren CEG, Miller JN, eds. The lung at depth: lung biology in health and disease (vol 132). New York, NY: Marcel Dekker, 1999 15 Arborelius M Jr, Balldin UI, Lilja B, et al. Hemodynamic changes in man during immersion with the head above water. Aerospace Med 1972; 43:592598 16 Robertson CH Jr, Engle CM, Bradley ME. Lung volumes in man immersed to the neck: dilution and plethysmographic techniques. J Appl Physiol 1978; 44:679 682 17 Morrison JB, Butt WS, Florio JT, et al. Effects of increased O2-N2 pressure and breathing apparatus on respiratory function. Undersea Biomed Res 1976; 3:217234 18 Thorsen E, Aanderud L, Aasen TB. Effects of a standard hyperbaric oxygen treatment protocol on pulmonary function. Eur Respir J 1998; 12:14421445 19 Jenkins C, Anderson SD, Wong R, et al. Compressed air diving and respiratory disease: a discussion document of the Thoracic Society of Australia and New Zealand. Med J Aust 1993; 158:275279 20 Glen S, White S, Douglas J. Medical supervision of sport diving in Scotland: reassessing the need for routine medical examinations. Br J Sports Med 2000; 34:375378 21 Neuman TS, Bove AA, OConnor RD, et al. Asthma and diving. Ann Allergy 1994; 73:344 350 22 Colebatch HJH, Ng CKY. Decreased pulmonary distensibility and pulmonary barotrauma in divers. Respir Physiol 1991; 86:293303 23 British Thoracic Society Fitness to Dive Group, Subgroup of the British Thoracic Society Standards of Care Committee. British Thoracic Society guidelines on respiratory aspects of fitness for diving. Thorax 2003; 58:313 24 Calder IM, Sweetnham K, Chan KK, et al. Relation of alveolar size to forced vital capacity in professional divers. Br J Ind Med 1987; 44:467 469

25 Thorsen E, Segadal K, Kambestad B, et al. Divers lung function: small airways disease? Br J Ind Med 1990; 47:519 523 26 Tetzlaff K, Friege L, Reuter M, et al. Expiratory flow limitation in compressed air divers and oxygen divers. Eur Respir J 1998; 12:895 899 27 Skogstad M, Thorsen E, Haldorsen T. Lung function over the first 3 years of a professional diving career. Occup Environ Med 2000; 57:390 395 28 Reuter M, Tetzlaff K, Steffens JC, et al. Functional and high-resolution computed tomographic studies of divers lungs. Scand J Work Environ Health 1999; 25:6774 29 Dujic Z, Eterovic D, Denoble P, et al. Effect of a single air dive on pulmonary diffusing capacity in professional divers. J Appl Physiol 1993; 74:55 61 30 Hyacinthe R, Broussolle B. Effets pulmonaires au long cours de lhyperoxie chez le nageur de combat. Med Aeronaut Spat Med Subaquatique Hyperbare 1979; 72:322324 31 Thorsen E, Risberg J, Segadal K, et al. Effects of venous gas microemboli on pulmonary gas transfer function. Undersea Hyperb Med 1995; 22:347353 32 Bermon S, Magnie M-N, Dolisi C, et al. Decreased pulmonary diffusing capacity of divers over a 6-year period. Eur J Appl Physiol 1997; 76:170 173 33 Thorsen E, Segadal K, Myrseth E, et al. Pulmonary mechanical function and diffusion capacity after deep saturation dives. Br J Ind Med 1990; 47:242247 34 Thorsen E, Segadal K, Reed JW, et al. Contribution of hyperoxia to reduced pulmonary function after deep saturation dives. J Appl Physiol 1993; 75:657 662 35 Flick MR, Perel A, Staub NC. Leukocytes are required for increased lung microvascular permeability after microembolization in sheep. Circ Res 1981; 48:344 351 36 Ohkuda K, Nakahara K, Binder A, et al. Venous air emboli in sheep: reversible increase in lung microvascular permeability. J Appl Physiol 1981; 51:887 894

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