Abstract
Historically, many studies investigating the pulmonary physiology of exercise (and biomedical research in general) were performed exclusively or predominantly with male research participants. This has led to an incomplete understanding of the pulmonary response to exercise. More recently, important sex-based differences with respect to the human respiratory system have been identified. The purpose of this review is to summarize current findings related to sex-based differences in the pulmonary physiology of exercise. To that end, we will discuss how morphological sex-based differences of the respiratory system affect the respiratory response to exercise. Moreover, we will discuss sex-based differences of the physiological integrative responses to exercise, and how all these differences can influence the regulation of breathing. We end with a brief discussion of pregnancy and menopause and the accompanying ventilatory changes observed during exercise.
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Abbreviations
- CO2 :
-
Carbon dioxide
- EIAH:
-
Exercise-induced arterial hypoxemia
- EMG:
-
Electromyography
- FEV1 :
-
Forced expiratory volume in one second
- FVC:
-
Forced vital capacity
- MSNA:
-
Muscle sympathetic nerve activity
- MVC:
-
Maximal voluntary contraction
- O2 :
-
Oxygen
- P aCO2 :
-
Arterial partial pressure of carbon dioxide
- P aO2 :
-
Arterial partial pressure of oxygen
- \(\dot{Q}\) :
-
Cardiac output
- SaO2 :
-
Arterial saturation of oxygen
- \(\dot{V}_{{\text{A}}}\) :
-
Alveolar ventilation
- \(\dot{V}\)O2max :
-
Maximal oxygen uptake
- W b :
-
Work of breathing
References
Aaron EA, Seow KC, Johnson BD, Dempsey JA (1992) Oxygen cost of exercise hyperpnea: implications for performance. J Appl Physiol 72:1818–1825. https://doi.org/10.1152/jappl.1992.72.5.1818
Archiza B, Welch JF, Geary CM et al (2018) Temporal characteristics of exercise-induced diaphragmatic fatigue. J Appl Physiol 124:906–914. https://doi.org/10.1152/japplphysiol.00942.2017
Archiza B, Reinhard PA, Welch JF, Sheel AW (2020) Sex differences in diaphragmatic fatigue: effects of hypoxia during inspiratory loading. J Physiol 599:1319–1333. https://doi.org/10.1113/JP280704
Behan M, Kinkead R (2011) Neuronal control of breathing: sex and stress hormones. Compr Physiol 1:2101–2139. https://doi.org/10.1002/cphy.c100027
Behan M, Wenninger JM (2008) Sex steroidal hormones and respiratory control. Respir Physiol Neurobiol 164:213–221. https://doi.org/10.1016/j.resp.2008.06.006
Bellemare F, Jeanneret A, Couture J (2003) Sex differences in thoracic dimensions and configuration. Am J Respir Crit Care Med 168:305–312. https://doi.org/10.1164/rccm.200208-876OC
Boccia G, Dardanello D, Tarperi C et al (2018) Women show similar central and peripheral fatigue to men after half-marathon. Eur J Sport Sci 18:695–704. https://doi.org/10.1080/17461391.2018.1442500
Bouwsema MM, Tedjasaputra V, Stickland MK (2017) Are there sex differences in the capillary blood volume and diffusing capacity response to exercise? J Appl Physiol 122:460–469. https://doi.org/10.1152/japplphysiol.00389.2016
Brinton RD, Thompson RF, Foy MR et al (2008) Progesterone receptors: form and function in brain. Front Neuroendocrinol 29:313–339
Campbell ML (2017) Dyspnea. Crit Care Nurs Clin N Am 29:461–470. https://doi.org/10.1016/j.cnc.2017.08.006
Carrick-Ranson G, Hastings JL, Bhella PS et al (2014) The effect of lifelong exercise dose on cardiovascular function during exercise. J Appl Physiol 116:736–745. https://doi.org/10.1152/japplphysiol.00342.2013
Carrick-Ranson G, Sloane NM, Howden EJ et al (2020) The effect of lifelong endurance exercise on cardiovascular structure and exercise function in women. J Physiol 598:2589–2605. https://doi.org/10.1113/JP278503
Carter SL, Rennie CD, Hamilton SJ, Tarnopolsky MA (2001) Changes in skeletal muscle in males and females following endurance training. Can J Physiol Pharmacol 79:386–392. https://doi.org/10.1139/cjpp-79-5-386
Choi HM, Stebbins CL, Nho H et al (2012) Skeletal muscle metaboreflex is enhanced in postmenopausal women. Eur J Appl Physiol 112:2671–2678. https://doi.org/10.1007/s00421-011-2245-0
Costello JT, Bieuzen F, Bleakley CM (2014) Where are all the female participants in sports and exercise medicine research? Eur J Sport Sci 14:847–851. https://doi.org/10.1080/17461391.2014.911354
Davenport MH, Skow RJ, Steinback CD (2016) Maternal responses to aerobic exercise in pregnancy. Clin Obstet Gynecol 59:541–551. https://doi.org/10.1097/GRF.0000000000000201
De Souza MJ, Maguire MS, Rubin KR, Maresh CM (1990) Effects of menstrual phase and amenorrhea on exercise performance in runners. Med Sci Sports Exerc 22:575–580
Dempsey JA, Wagner PD (1999) Exercise-induced arterial hypoxemia. J Appl Physiol 87:1997–2006
Dempsey JA, Hanson PG, Henderson KS (1984) Exercise-induced arterial hypoxaemia in healthy human subjects at sea level. J Physiol 355:161–175. https://doi.org/10.1113/jphysiol.1984.sp015412
Dempsey JA, Foster H, Ainsworth D (1995) Regulation of hyperpnea, hyperventilation and respiratory muscle recruitment during exercise. In: AI P (ed) Regulation of breathing. Marcel Dekker, New York, pp 1065–1134
Derchak PA, Sheel AW, Morgan BJ, Dempsey JA (2002) Effects of expiratory muscle work on muscle sympathetic nerve activity. J Appl Physiol 92:1539–1552. https://doi.org/10.1152/japplphysiol.00790.2001
Dominelli PB, Sheel AW (2012) Experimental approaches to the study of the mechanics of breathing during exercise. Respir Physiol Neurobiol 180:147–161. https://doi.org/10.1016/j.resp.2011.10.005
Dominelli PB, Sheel AW (2019) Exercise-induced arterial hypoxemia; some answers, more questions. Appl Physiol Nutr Metab 44:571–579. https://doi.org/10.1139/apnm-2018-0468
Dominelli PB, Guenette JA, Wilkie SS et al (2011) Determinants of expiratory flow limitation in healthy women during exercise. Med Sci Sports Exerc 43:1666–1674. https://doi.org/10.1249/mss.0b013e318214679d
Dominelli PB, Foster GE, Dominelli GS et al (2013) Exercise-induced arterial hypoxaemia and the mechanics of breathing in healthy young women. J Physiol 591:3017–3034. https://doi.org/10.1113/jphysiol.2013.252767
Dominelli PB, Molgat-Seon Y, Bingham D et al (2015a) Dysanapsis and the resistive work of breathing during exercise in healthy men and women. J Appl Physiol 119:1105–1113. https://doi.org/10.1152/japplphysiol.00409.2015
Dominelli PB, Render JN, Molgat-Seon Y et al (2015b) Oxygen cost of exercise hyperpnoea is greater in women compared with men. J Physiol 593:1965–1979. https://doi.org/10.1113/jphysiol.2014.285965
Dominelli PB, Archiza B, Ramsook AH et al (2017a) Effects of respiratory muscle work on respiratory and locomotor blood flow during exercise. Exp Physiol 102:1535–1547. https://doi.org/10.1113/EP086566
Dominelli PB, Molgat-Seon Y, Griesdale DEG et al (2017b) Exercise-induced quadriceps muscle fatigue in men and women: effects of arterial oxygen content and respiratory muscle work. J Physiol 595:5227–5244. https://doi.org/10.1113/JP274068
Dominelli PB, Ripoll JG, Cross TJ et al (2018) Sex differences in large conducting airway anatomy. J Appl Physiol 125:960–965. https://doi.org/10.1152/japplphysiol.00440.2018
Dominelli PB, Katayama K, Vermeulen TD et al (2019) Work of breathing influences muscle sympathetic nerve activity during semi-recumbent cycle exercise. Acta Physiol. https://doi.org/10.1111/apha.13212
Eckberg DL, Nerhed C, Wallin BG (1985) Respiratory modulation of muscle sympathetic and vagal cardiac outflow in man. J Physiol 365:181–196. https://doi.org/10.1113/jphysiol.1985.sp015766
Ekström M, Schiöler L, Grønseth R et al (2017) Absolute values of lung function explain the sex difference in breathlessness in the general population. Eur Respir J 49:1–9. https://doi.org/10.1183/13993003.02047-2016
Ettinger SM, Silber DH, Collins BG et al (1996) Influences of gender on sympathetic nerve responses to static exercise. J Appl Physiol 80:245–251. https://doi.org/10.1152/jappl.1996.80.1.245
Ferretti G, Fagoni N, Taboni A et al (2017) The physiology of submaximal exercise: the steady state concept. Respir Physiol Neurobiol 246:76–85
Forster HV, Haouzi P, Dempsey JA (2012) Control of breathing during exercise. Compr Physiol 2:743–777. https://doi.org/10.1002/cphy.c100045
García-Martínez D, Torres-Tamayo N, Torres-Sanchez I et al (2016) Morphological and functional implications of sexual dimorphism in the human skeletal thorax. Am J Phys Anthropol 161:467–477. https://doi.org/10.1002/ajpa.23051
Gargaglioni LH, Marques DA, Patrone LGA (2019) Sex differences in breathing. Comp Biochem Physiol Part A Mol Integr Physiol 238:1–26. https://doi.org/10.1016/j.cbpa.2019.110543
Geary CM, Welch JF, McDonald MR et al (2019) Diaphragm fatigue and inspiratory muscle metaborflex in men and women matched for absolute diaphragmatic work during pressure-threshold loading. J Physiol 597:4797–4808. https://doi.org/10.1113/jp278380
Gilroy RJ, Mangura BT, Lavietes MH (1988) Rib cage and abdominal volume displacements during breathing in pregnancy. Am Rev Respir Dis 137:668–672. https://doi.org/10.1164/ajrccm/137.3.668
Glace BW, Kremenic IJ, McHugh MP (2013) Sex differences in central and peripheral mechanisms of fatigue in cyclists. Eur J Appl Physiol 113:1091–1098. https://doi.org/10.1007/s00421-012-2516-4
Green M, Mead J, Turner MJ (1974) Variability of maximum expiratory flow-volume curves. J Appl Physiol 37:67–74
Guenette JA, Diep TT, Koehle MS et al (2004) Acute hypoxic ventilatory response and exercise-induced arterial hypoxemia in men and women. Respir Physiol Neurobiol 143:37–48. https://doi.org/10.1016/j.resp.2004.07.004
Guenette JA, Witt JD, McKenzie DC et al (2007) Respiratory mechanics during exercise in endurance-trained men and women. J Physiol 581:1309–1322. https://doi.org/10.1113/jphysiol.2006.126466
Guenette JA, Romer LM, Querido JS et al (2010) Sex differences in exercise-induced diaphragmatic fatigue in endurance-trained athletes. J Appl Physiol 109:35–46. https://doi.org/10.1152/japplphysiol.01341.2009
Guenette JA, Jensen D, Webb KA et al (2011) Sex differences in exertional dyspnea in patients with mild COPD: physiological mechanisms. Respir Physiol Neurobiol 177:218–227. https://doi.org/10.1016/j.resp.2011.04.011
Hamson DK, Jones BA, Watson NV (2004) Distribution of androgen receptor immunoreactivity in the brainstem of male rats. Neuroscience 127:797–803. https://doi.org/10.1016/j.neuroscience.2004.06.006
Harms CA, McClaran SR, Nickele GA et al (1998) Exercise-induced arterial hypoxaemia in healthy young women. J Physiol 507:619–628. https://doi.org/10.1111/j.1469-7793.1998.619bt.x
Harms CA, Wetter TJ, Croix CMST et al (2000) Effects of respiratory muscle work on exercise performance. J Appl Physiol 89:131–138
Harms CA, Babcock MA, McClaran SR et al (1997) Respiratory muscle work compromises leg blood flow during maximal exercise. J Appl Physiol 82:1573–1583. https://doi.org/10.1152/jappl.1997.82.5.1573
Hong YS, Park HY, Chang Y et al (2021) Stages of menopause and abnormal lung function: a cross-sectional study of middle-aged women. Menopause. https://doi.org/10.1097/GME.0000000000001779
Hopkins SR, Barker RC, Brutsaert TD et al (2000) Pulmonary gas exchange during exercise in women: effects of exercise type and work increment. J Appl Physiol 89:721–730. https://doi.org/10.1152/jappl.2000.89.2.721
Howden EJ, Perhonen M, Peshock RM et al (2015) Females have a blunted cardiovascular response to one year of intensive supervised endurance training. J Appl Physiol 75321:37–46. https://doi.org/10.1152/japplphysiol.00092.2015
Howell FR, Richards TG (1955) The determination of pressure-volume changes in the femoral tree of the cat in relation to vascular tonus and the resistance offered to blood flow. J Physiol 130:414–426. https://doi.org/10.1113/jphysiol.1955.sp005415
Hunter SK (2016) Sex differences in fatigability of dynamic contractions. Exp Physiol 101:250–255. https://doi.org/10.1113/EP085370
Hunter SK, Critchlow A, Shin IS, Enoka RM (2004) Fatigability of the elbow flexor muscles for a sustained submaximal contraction is similar in men and women matched for strength. J Appl Physiol 96:195–202. https://doi.org/10.1152/japplphysiol.00893.2003
Hunter SK, Butler JE, Todd G et al (2006) Supraspinal fatigue does not explain the sex difference in muscle fatigue of maximal contractions. J Appl Physiol 101:1036–1044. https://doi.org/10.1152/japplphysiol.00103.2006
Jensen D, Wolfe LA, Slatkovska L et al (2005) Effects of human pregnancy on the ventilatory chemoreflex response to carbon dioxide. Am J Physiol Regul Integr Comp Physiol 288:1369–1375. https://doi.org/10.1152/ajpregu.00862.2004
Jensen D, Webb KA, O’Donnell DE (2007) Chemical and mechanical adaptations of the respiratory system at rest and during exercise in human pregnancy. Appl Physiol Nutr Metab 32:1239–1250. https://doi.org/10.1139/H07-120
Jensen D, Webb KA, Davies GAL, O’Donnell DE (2008) Mechanical ventilatory constraints during incremental cycle exercise in human pregnancy: implications for respiratory sensation. J Physiol 586:4735–4750. https://doi.org/10.1113/jphysiol.2008.158154
Jensen D, Ofir D, O’Donnell DE (2009) Effects of pregnancy, obesity and aging on the intensity of perceived breathlessness during exercise in healthy humans. Respir Physiol Neurobiol 167:87–100. https://doi.org/10.1016/j.resp.2009.01.011
Johnson BD, Saupe KW, Dempsey JA (1992) Mechanical constraints on exercise hyperpnea in endurance athletes. J Appl Physiol 73:874–886. https://doi.org/10.1152/jappl.1992.73.3.874
Jolley C (2014) Sex differences in the perception of breathlessness: insights from measurements of neural respiratory drive. Exp Physiol 99:346–347. https://doi.org/10.1113/expphysiol.2013.076968
Katayama K, Smith JR, Goto K et al (2018) Elevated sympathetic vasomotor outflow in response to increased inspiratory muscle activity during exercise is less in young women compared with men. Exp Physiol 103:570–580. https://doi.org/10.1113/EP086817
Kiely C, Rocha J, O’Connor E et al (2015) Influence of menopause and type 2 diabetes on pulmonary oxygen uptake kinetics and peak exercise performance during cycling. Am J Physiol Regul Integr Comp Physiol 309:R875–R883. https://doi.org/10.1152/ajpregu.00258.2015
Killian KJ, Summers E, Jones NL, Campbell EJ (1992) Dyspnea and leg effort during incremental cycle ergometry. Am Rev Respir Dis 145:1339–1345. https://doi.org/10.1164/ajrccm/145.6.1339
Killick R, Wang D, Hoyos CM et al (2013) The effects of testosterone on ventilatory responses in men with obstructive sleep apnea: a randomised, placebo-controlled trial. J Sleep Res 22:331–336. https://doi.org/10.1111/jsr.12027
Layton AM, Garber CE, Thomashow BM et al (2011) Exercise ventilatory kinematics in endurance trained and untrained men and women. Respir Physiol Neurobiol 178:223–229. https://doi.org/10.1016/j.resp.2011.06.009
Lee SY, Chien DK, Huang CH et al (2017) Dyspnea in pregnancy. Taiwan J Obstet Gynecol 56:432–436. https://doi.org/10.1016/j.tjog.2017.04.035
LoMauro A, Aliverti A, Frykholm P et al (2019) Adaptation of lung, chest wall, and respiratory muscles during pregnancy: preparing for birth. J Appl Physiol 127:1640–1650. https://doi.org/10.1152/japplphysiol.00035.2019
Luo YM, Li RF, Jolley C et al (2011) Neural respiratory drive in patients with COPD during exercise tests. Respiration 81:294–301. https://doi.org/10.1159/000317136
Lynch NA, Ryan AS, Berman DM et al (2002) Comparison of VO2max and disease risk factors between perimenopausal and postmenopausal women. Menopause 9:456–462. https://doi.org/10.1097/00042192-200211000-00012
MacNutt MJ, De Souza MJ, Tomczak SE et al (2012) Resting and exercise ventilatory chemosensitivity across the menstrual cycle. J Appl Physiol 112:737–747. https://doi.org/10.1152/japplphysiol.00727.2011
Mann LM, Granger EA, Chan JS et al (2020) Minimizing airflow turbulence in women lowers the work of breathing to levels similar to men. J Appl Physiol 129:410–418. https://doi.org/10.1152/japplphysiol.00347.2020
Martin PG, Rattey J (2007) Central fatigue explains sex differences in muscle fatigue and contralateral cross-over effects of maximal contractions. Pflugers Arch Eur J Physiol 454:957–969. https://doi.org/10.1007/s00424-007-0243-1
Martin TR, Castile RG, Fredberg JJ et al (1987) Airway size is related to sex but not lung size in normal adults. J Appl Physiol 63:2042–2047. https://doi.org/10.1152/jappl.1987.63.5.2042
McClaran SR, Harms CA, Pegelow DF, Dempsey JA (1998) Smaller lungs in women affect exercise hyperpnea. J Appl Physiol 84:1872–1881. https://doi.org/10.1152/jappl.1998.84.6.1872
McCloskey DI (1981) Corollary discharges: motor commands to perception. In: Brookhart JM, Mountcastle VB (eds) The nervous system: handbook of physiology. American Physiological Society, Bethesda, pp 1415–1447
Mead J (1980) Dysanapsis in normal lungs assessed by the relationship between maximal flow, static recoil, and vital capacity. Am Rev Respir Dis 121:339–342. https://doi.org/10.1164/arrd.1980.121.2.339
Mendonca CT, Schaeffer MR, Riley P, Jensen D (2014) Physiological mechanisms of dyspnea during exercise with external thoracic restriction: role of increased neural respiratory drive. J Appl Physiol 116:570–581. https://doi.org/10.1152/japplphysiol.00950.2013
Mercuro G, Saiu F, Deidda M et al (2006) Impairment of physical exercise capacity in healthy postmenopausal women. Am Heart J 151:923–927. https://doi.org/10.1016/j.ahj.2005.06.027
Miller MR, Hankinson J, Brusasco V et al (2005) Standardisation of spirometry. Eur Respir J 26:319–338. https://doi.org/10.1183/09031936.05.00034805
Mitchell RA, Schaeffer MR, Ramsook AH et al (2018) Sex differences in respiratory muscle activation patterns during high-intensity exercise in healthy humans. Respir Physiol Neurobiol 247:57–60. https://doi.org/10.1016/j.resp.2017.09.002
Molgat-Seon Y, Dominelli PB, Ramsook AH et al (2018a) The effects of age and sex on mechanical ventilatory constraint and dyspnea during exercise in healthy humans. J Appl Physiol 124:1092–1106. https://doi.org/10.1152/japplphysiol.00608.2017
Molgat-Seon Y, Dominelli PB, Ramsook AH et al (2018b) Effects of age and sex on inspiratory muscle activation patterns during exercise. Med Sci Sports Exerc 50:1882–1891. https://doi.org/10.1249/MSS.0000000000001648
Molgat-Seon Y, Dominelli PB, Guenette JA, Sheel AW (2019) Modelling the effects of age and sex on the resistive and viscoelastic components of the work of breathing during exercise. Exp Physiol 104:1737–1745. https://doi.org/10.1113/EP087956
Nardone M, Teixeira AL, Incognito AV et al (2020) Within-breath sympathetic baroreflex sensitivity is modulated by lung volume but unaffected by acute intermittent hypercapnic hypoxia in men. Am J Physiol Heart Circ Physiol 319:H213–H221. https://doi.org/10.1152/ajpheart.00296.2020
Nielsen HB (2003) Arterial desaturation during exercise in man: implication for O2 uptake and work capacity. Scand J Med Sci Sport 13:339–358
O’Donnell DE, Milne KM, James MD et al (2020) Dyspnea in COPD: new mechanistic insights and management implications. Adv Ther 37:41–60. https://doi.org/10.1007/s12325-019-01128-9
Ofir D, Laveneziana P, Webb KA et al (2008) Sex differences in the perceived intensity of breathlessness during exercise with advancing age. J Appl Physiol 104:1583–1593. https://doi.org/10.1152/japplphysiol.00079.2008
Olfert IM, Balouch J, Kleinsasser A et al (2004) Does gender affect human pulmonary gas exchange during exercise? J Physiol 557:529–541. https://doi.org/10.1113/jphysiol.2003.056887
Porter MM, Stuart S, Boij M, Lexell J (2002) Capillary supply of the tibialis anterior muscle in young, healthy, and moderately active men and women. J Appl Physiol 92:1451–1457. https://doi.org/10.1152/japplphysiol.00744.2001
Powers SK, Dodd S, Lawler J et al (1988) Incidence of exercise induced hypoxemia in elite endurance athletes at sea level. Eur J Appl Physiol Occup Physiol 58:298–302. https://doi.org/10.1007/BF00417266
Powers SK, Lawler J, Dempsey JA et al (1989) Effects of incomplete pulmonary gas exchange on V̇O2max. J Appl Physiol 66:2491–2495. https://doi.org/10.1152/jappl.1989.66.6.2491
Rankin J, Dempsey JA (1967) Respiratory muscles and the mechanisms of breathing. Am J Phys Med 46:198–244
Real FG, Svanes C, Omenaas ER et al (2008) Lung function, respiratory symptoms, and the menopausal transition. J Allergy Clin Immunol. https://doi.org/10.1016/j.jaci.2007.08.057
Reilly CC, Ward K, Jolley CJ et al (2011) Neural respiratory drive, pulmonary mechanics and breathlessness in patients with cystic fibrosis. Thorax 66:240–246. https://doi.org/10.1136/thx.2010.142646
Richards JC, McKenzie DC, Warburton DER et al (2004) Prevalence of exercise-induced arterial hypoxemia in healthy women. Med Sci Sport Exerc 36:1514–1521. https://doi.org/10.1249/01.MSS.0000139898.30804.60
Ripoll JG, Guo W, Andersen KJ et al (2020) Sex differences in paediatric airway anatomy. Exp Physiol. https://doi.org/10.1113/ep088370
Romer LM, Polkey MI (2008) Exercise-induced respiratory muscle fatigue: implications for performance. J Appl Physiol 104:879–888. https://doi.org/10.1152/japplphysiol.01157.2007
Romer LM, Haverkamp HC, Lovering AT et al (2006) Effect of exercise-induced arterial hypoxemia on quadriceps muscle fatigue in healthy humans. Am J Physiol Integr Comp Physiol 290:R365–R375. https://doi.org/10.1152/ajpregu.00332.2005
Schaeffer MR, Mendonca CT, Levangie MC et al (2014) Physiological mechanisms of sex differences in exertional dyspnoea: role of neural respiratory motor drive. Exp Physiol 99:427–441. https://doi.org/10.1113/expphysiol.2013.074880
Schwartz J, Katz SA, Fegley RW, Tockman MS (1988) Sex and race differences in the development of lung function. Am Rev Respir Dis 138:1415–1421. https://doi.org/10.1164/ajrccm/140.3.855a
Sheel AW, Guenette JA (2008) Mechanics of breathing during exercise in men and women: sex versus body size differences? Exerc Sport Sci Rev 36:128–134. https://doi.org/10.1097/jes.0b013e31817be7f0
Sheel AW, Richards JC, Foster GE, Guenette JA (2004) Sex differences in respiratory exercise physiology. Sport Med 34:567–579. https://doi.org/10.2165/00007256-200434090-00002
Sheel AW, Guenette JA, Yuan R et al (2009) Evidence for dysanapsis using computed tomographic imaging of the airways in older ex-smokers. J Appl Physiol 107:1622–1628. https://doi.org/10.1152/japplphysiol.00562.2009
Sheel AW, Boushel R, Dempsey JA (2018) Competition for blood flow distribution between respiratory and locomotor muscles: implications for muscle fatigue. J Appl Physiol 125:820–831
Smith JR, Rosenkranz SK, Harms CA (2014) Dysanapsis ratio as a predictor for expiratory flow limitation. Respir Physiol Neurobiol 198:25–31. https://doi.org/10.1016/j.resp.2014.04.001
Smith JR, Brown KR, Murphy JD, Harms CA (2015) Does menstrual cycle phase affect lung diffusion capacity during exercise? Respir Physiol Neurobiol 205:99–104. https://doi.org/10.1016/j.resp.2014.10.014
Smith JR, Cross TJ, Van Iterson EH et al (2018) Resistive and elastic work of breathing in older and younger adults during exercise. J Appl Physiol 125:190–197. https://doi.org/10.1152/japplphysiol.01105.2017
Spina RJ, Miller TR, Bogenhagen WH et al (1996) Gender-related differences in left ventricular filling dynamics in older subjects after endurance exercise training. J Gerontol Ser A Biol Sci Med Sci 51:232–237. https://doi.org/10.1093/gerona/51A.3.B232
St. Croix CM, Satoh M, Morgan BJ et al (1999) Role of respiratory motor output in within-breath modulation of muscle sympathetic nerve activity in humans. Circ Res 85:457–469. https://doi.org/10.1161/01.RES.85.5.457
St Croix CM, Morgan BJ, Wetter TJ, Dempsey JA (2000) Fatiguing inspiratory muscle work causes reflex sympathetic activation in humans. J Physiol 529:493–504. https://doi.org/10.1111/j.1469-7793.2000.00493.x
Taylor JL, Gandevia SC (2001) Transcranial magnetic stimulation and human muscle fatigue. Muscle Nerve 24:18–29. https://doi.org/10.1002/1097-4598(200101)24:1%3c18::AID-MUS2%3e3.0.CO;2-D
Taylor JL, Todd G, Gandevia SC (2006) Evidence for a supraspinal contribution to human muscle fatigue. Clin Exp Pharmacol Physiol 33:400–405
Thurlbeck WM (1982) Postnatal human lung growth. Thorax 37:564–571. https://doi.org/10.1136/thx.37.8.564
Torres-Tamayo N, García-Martínez D, Lois Zlolniski S et al (2018) 3D analysis of sexual dimorphism in size, shape and breathing kinematics of human lungs. J Anat 232:227–237. https://doi.org/10.1111/joa.12743
Triebner K, Johannessen A, Puggini L et al (2016) Menopause as a predictor of new-onset asthma: a longitudinal Northern European population study. J Allergy Clin Immunol 137:50-57.e6. https://doi.org/10.1016/j.jaci.2015.08.019
Welch JF, Archiza B, Guenette JA et al (2018) Sex differences in diaphragmatic fatigue: the cardiovascular response to inspiratory resistance. J Physiol 596:4017–4032. https://doi.org/10.1113/JP275794
Welle S, Tawil R, Thornton CA (2008) Sex-related differences in gene expression in human skeletal muscle. PLoS ONE. https://doi.org/10.1371/journal.pone.0001385
Whittenberger JL, McGregor M, Berglund E, Borst HG (1960) Influence of state of inflation of the lung on pulmonary vascular resistance. J Appl Physiol 15:878–882. https://doi.org/10.1152/jappl.1960.15.5.878
Yacyshyn AF, Nettleton J, McNeil CJ (2018) The effects of sex and motoneuron pool on central fatigue. Med Sci Sports Exerc 50:1061–1069. https://doi.org/10.1249/MSS.0000000000001536
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Archiza, B., Leahy, M.G., Kipp, S. et al. An integrative approach to the pulmonary physiology of exercise: when does biological sex matter?. Eur J Appl Physiol 121, 2377–2391 (2021). https://doi.org/10.1007/s00421-021-04690-9
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DOI: https://doi.org/10.1007/s00421-021-04690-9