Abstract
Numerous epidemiological studies have shown explicit sex and gender differences in the respiratory system under both physiological and pathological conditions. Here, we review the impact of sex steroids, with emphasis on androgens, upon the respiratory system in two endocrine hyperandrogenemic clinical scenarios: polycystic ovary syndrome and postmenopausal women. The primary sex hormones are testosterone in men and estrogens in women. Interestingly, in women, the plasma concentration of testosterone is much higher than estradiol; however, whether and how the excess of androgens may affect the respiratory system in women remain unclear. Hence, here we review some of the evidence that highlights the crucial role of androgens modulating respiratory physiology in these hyperandrogenemic endocrine conditions.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Ala-Fossi SL, Maenpaa J, Aine R, Punnonen R (1998) Ovarian testosterone secretion during perimenopause. Maturitas 29(3):239–245. https://doi.org/10.1016/s0378-5122(98)00034-6
Azziz R, Sanchez LA, Knochenhauer ES, Moran C, Lazenby J, Stephens KC, Taylor K, Boots LR (2004) Androgen excess in women: experience with over 1000 consecutive patients. J Clin Endocrinol Metab 89(2):453–462. https://doi.org/10.1210/jc.2003-031122
Azziz R, Carmina E, Dewailly D, Diamanti-Kandarakis E, Escobar-Morreale HF, Futterweit W, Janssen OE, Legro RS, Norman RJ, Taylor AE, Witchel SF (2006) Positions statement: criteria for defining polycystic ovary syndrome as a predominantly hyperandrogenic syndrome: an androgen excess society guideline. J Clin Endocrinol Metab 91(11):4237–4245. https://doi.org/10.1210/jc.2006-0178
Baptist AP, Hamad A, Patel MR (2014) Special challenges in treatment and self-management of older women with asthma. Ann Allergy Asthma Immunol 113(2):125–130. https://doi.org/10.1016/j.anai.2014.05.013
Becerra-Diaz M, Strickland AB, Keselman A, Heller NM (2018) Androgen and androgen receptor as enhancers of M2 macrophage polarization in allergic lung inflammation. J Immunol 201(10):2923–2933. https://doi.org/10.4049/jimmunol.1800352
Benza RL, Miller DP, Gomberg-Maitland M, Frantz RP, Foreman AJ, Coffey CS, Frost A, Barst RJ, Badesch DB, Elliott CG, Liou TG, McGoon MD (2010) Predicting survival in pulmonary arterial hypertension: insights from the registry to evaluate early and long-term pulmonary arterial hypertension disease management (REVEAL). Circulation 122(2):164–172. https://doi.org/10.1161/circulationaha.109.898122
Borg W, Shackleton CH, Pahuja SL, Hochberg RB (1995) Long-lived testosterone esters in the rat. Proc Natl Acad Sci U S A 92(5):1545–1549
Brahmbhatt Y, Gupta M, Hamrahian S (2019) Hypertension in premenopausal and postmenopausal women. Curr Hypertens Rep 21(10):74. https://doi.org/10.1007/s11906-019-0979-y
Brand JS, Chan MF, Dowsett M, Folkerd E, Wareham NJ, Luben RN, van der Schouw YT, Khaw KT (2011) Cigarette smoking and endogenous sex hormones in postmenopausal women. J Clin Endocrinol Metab 96(10):3184–3192. https://doi.org/10.1210/jc.2011-1165
Brittain EL, Talati M, Fessel JP, Zhu H, Penner N, Calcutt MW, West JD, Funke M, Lewis GD, Gerszten RE, Hamid R, Pugh ME, Austin ED, Newman JH, Hemnes AR (2016) Fatty acid metabolic defects and right ventricular lipotoxicity in human pulmonary arterial hypertension. Circulation 133(20):1936–1944. https://doi.org/10.1161/circulationaha.115.019351
Burger HG (2002) Androgen production in women. Fertil Steril 77(Suppl 4):S3–S5. https://doi.org/10.1016/s0015-0282(02)02985-0
Burger HG, Dudley EC, Hopper JL, Groome N, Guthrie JR, Green A, Dennerstein L (1999) Prospectively measured levels of serum follicle-stimulating hormone, estradiol, and the dimeric inhibins during the menopausal transition in a population-based cohort of women. J Clin Endocrinol Metab 84(11):4025–4030. https://doi.org/10.1210/jcem.84.11.6158
Burger HG, Dudley EC, Cui J, Dennerstein L, Hopper JL (2000) A prospective longitudinal study of serum testosterone, dehydroepiandrosterone sulfate, and sex hormone-binding globulin levels through the menopause transition. J Clin Endocrinol Metab 85(8):2832–2838. https://doi.org/10.1210/jcem.85.8.6740
Burger HG, MacLennan AH, Huang KE, Castelo-Branco C (2012) Evidence-based assessment of the impact of the WHI on women’s health. Climacteric 15(3):281–287. https://doi.org/10.3109/13697137.2012.655564
Campbell B, Bui DS, Simpson JA, Lodge CJ, Lowe AJ, Bowatte G, Leynaert B, Gomez Real F, Thomas PS, Giles GG, Johns DP, Garcia-Aymerich J, Hopper JL, Jarvis D, Abramson MJ, Walters EH, Perret JL, Dharmage SC (2020) Early age at natural menopause is related to lower post-bronchodilator lung function: a longitudinal population-based study. Ann Am Thorac Soc 17:429. https://doi.org/10.1513/AnnalsATS.201902-180OC
Cevrioglu AS, Fidan F, Unlu M, Yilmazer M, Orman A, Fenkci IV, Serteser M (2004) The effects of hormone therapy on pulmonary function tests in postmenopausal women. Maturitas 49(3):221–227. https://doi.org/10.1016/j.maturitas.2004.01.009
Chapman DG, Irvin CG, Kaminsky DA, Forgione PM, Bates JH, Dixon AE (2014) Influence of distinct asthma phenotypes on lung function following weight loss in the obese. Respirology 19(8):1170–1177. https://doi.org/10.1111/resp.12368
Chu MC, Cosper P, Orio F, Carmina E, Lobo RA (2006) Insulin resistance in postmenopausal women with metabolic syndrome and the measurements of adiponectin, leptin, resistin, and ghrelin. Am J Obstet Gynecol 194(1):100–104. https://doi.org/10.1016/j.ajog.2005.06.073
Collins LC, Peiris A (1993) Bronchospasm secondary to replacement estrogen therapy. Chest 104(4):1300–1302. https://doi.org/10.1378/chest.104.4.1300
Collins LC, Hoberty PD, Walker JF, Fletcher EC, Peiris AN (1995) The effect of body fat distribution on pulmonary function tests. Chest 107(5):1298–1302. https://doi.org/10.1378/chest.107.5.1298
Davis WA, Knuiman M, Kendall P, Grange V, Davis TM (2004) Glycemic exposure is associated with reduced pulmonary function in type 2 diabetes: the Fremantle diabetes study. Diabetes Care 27(3):752–757. https://doi.org/10.2337/diacare.27.3.752
Deslypere JP, Verdonck L, Vermeulen A (1985) Fat tissue: a steroid reservoir and site of steroid metabolism. J Clin Endocrinol Metab 61(3):564–570. https://doi.org/10.1210/jcem-61-3-564
Dixon AE, Pratley RE, Forgione PM, Kaminsky DA, Whittaker-Leclair LA, Griffes LA, Garudathri J, Raymond D, Poynter ME, Bunn JY, Irvin CG (2011) Effects of obesity and bariatric surgery on airway hyperresponsiveness, asthma control, and inflammation. J Allergy Clin Immunol 128(3):508–515.e501–502. https://doi.org/10.1016/j.jaci.2011.06.009
Dumesic DA, Oberfield SE, Stener-Victorin E, Marshall JC, Laven JS, Legro RS (2015) Scientific statement on the diagnostic criteria, epidemiology, pathophysiology, and molecular genetics of polycystic ovary syndrome. Endocr Rev 36(5):487–525. https://doi.org/10.1210/er.2015-1018
Ehrmann DA, Barnes RB, Rosenfield RL, Cavaghan MK, Imperial J (1999) Prevalence of impaired glucose tolerance and diabetes in women with polycystic ovary syndrome. Diabetes Care 22(1):141–146
El Khoudary SR, Santoro N, Chen HY, Tepper PG, Brooks MM, Thurston RC, Janssen I, Harlow SD, Barinas-Mitchell E, Selzer F, Derby CA, Jackson EA, McConnell D, Matthews KA (2016) Trajectories of estradiol and follicle-stimulating hormone over the menopause transition and early markers of atherosclerosis after menopause. Eur J Prev Cardiol 23(7):694–703. https://doi.org/10.1177/2047487315607044
Engstrom G, Wollmer P, Valind S, Hedblad B, Janzon L (2001) Blood pressure increase between 55 and 68 years of age is inversely related to lung function: longitudinal results from the cohort study ‘Men born in 1914’. J Hypertens 19(7):1203–1208. https://doi.org/10.1097/00004872-200107000-00004
Engstrom G, Hedblad B, Nilsson P, Wollmer P, Berglund G, Janzon L (2003) Lung function, insulin resistance and incidence of cardiovascular disease: a longitudinal cohort study. J Intern Med 253(5):574–581. https://doi.org/10.1046/j.1365-2796.2003.01138.x
Feher T, Bodrogi L (1982) A comparative study of steroid concentrations in human adipose tissue and the peripheral circulation. Clin Chim Acta 126(2):135–141
Franchi AM, Gimeno MF, Gimeno AL (1985) Estradiol −17-beta enhances the formation of (3H)-PGF2 alpha from (3H)-PGE2 in the uterus isolated from ovariectomized rats. Prostaglandins 29(5):773–783. https://doi.org/10.1016/0090-6980(85)90137-6
Gallagher PE, Li P, Lenhart JR, Chappell MC, Brosnihan KB (1999) Estrogen regulation of angiotensin-converting enzyme mRNA. Hypertension 33(1 Pt 2):323–328. https://doi.org/10.1161/01.hyp.33.1.323
Gomez Real F, Svanes C, Bjornsson EH, Franklin KA, Gislason D, Gislason T, Gulsvik A, Janson C, Jogi R, Kiserud T, Norback D, Nystrom L, Toren K, Wentzel-Larsen T, Omenaas E (2006) Hormone replacement therapy, body mass index and asthma in perimenopausal women: a cross sectional survey. Thorax 61(1):34–40. https://doi.org/10.1136/thx.2005.040881
Goodpaster BH, Park SW, Harris TB, Kritchevsky SB, Nevitt M, Schwartz AV, Simonsick EM, Tylavsky FA, Visser M, Newman AB (2006) The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci 61(10):1059–1064. https://doi.org/10.1093/gerona/61.10.1059
Guo Z, Benten WP, Krucken J, Wunderlich F (2002) Nongenomic testosterone calcium signaling. Genotropic actions in androgen receptor-free macrophages. J Biol Chem 277(33):29600–29607
Hakala K, Stenius-Aarniala B, Sovijarvi A (2000) Effects of weight loss on peak flow variability, airways obstruction, and lung volumes in obese patients with asthma. Chest 118(5):1315–1321. https://doi.org/10.1378/chest.118.5.1315
Han W, Li J, Tang H, Sun L (2017) Treatment of obese asthma in a mouse model by simvastatin is associated with improving dyslipidemia and decreasing leptin level. Biochem Biophys Res Commun 484(2):396–402. https://doi.org/10.1016/j.bbrc.2017.01.135
Hayatbakhsh MR, Najman JM, O'Callaghan MJ, Williams GM, Paydar A, Clavarino A (2011) Association between smoking and respiratory function before and after menopause. Lung 189(1):65–71. https://doi.org/10.1007/s00408-010-9269-9
Hickson DA, Burchfiel CM, Petrini MF, Liu J, Campbell-Jenkins BW, Bhagat R, Marshall GD (2011) Leptin is inversely associated with lung function in African Americans, independent of adiposity: the Jackson heart study. Obesity (Silver Spring, Md) 19(5):1054–1061. https://doi.org/10.1038/oby.2010.240
Hopkins E, Sharma S (2020) Physiology, functional residual capacity. In: StatPearls. StatPearls Publishing, Treasure Island (FL)
Htet TD, Teede HJ, de Courten B, Loxton D, Real FG, Moran LJ, Joham AE (2017) Asthma in reproductive-aged women with polycystic ovary syndrome and association with obesity. Eur Respir J 49(5):1601334. https://doi.org/10.1183/13993003.01334-2016
Huang A, Brennan K, Azziz R (2010) Prevalence of hyperandrogenemia in the polycystic ovary syndrome diagnosed by the National Institutes of Health 1990 criteria. Fertil Steril 93(6):1938–1941. https://doi.org/10.1016/j.fertnstert.2008.12.138
Imai Y, Kuba K, Rao S, Huan Y, Guo F, Guan B, Yang P, Sarao R, Wada T, Leong-Poi H, Crackower MA, Fukamizu A, Hui CC, Hein L, Uhlig S, Slutsky AS, Jiang C, Penninger JM (2005) Angiotensin-converting enzyme 2 protects from severe acute lung failure. Nature 436(7047):112–116. https://doi.org/10.1038/nature03712
Institute of Medicine (U.S.). Committee on Understanding the Biology of Sex and Gender Differences (2001) Exploring the biological contributions to human health: does sex matter? The National Academies Press, Washington, DC. https://doi.org/10.17226/10028
Israili ZH, Hall WD (1992) Cough and angioneurotic edema associated with angiotensin-converting enzyme inhibitor therapy. A review of the literature and pathophysiology. Ann Intern Med 117(3):234–242. https://doi.org/10.7326/0003-4819-117-3-234
Ivanova MM, Mazhawidza W, Dougherty SM, Minna JD, Klinge CM (2009) Activity and intracellular location of estrogen receptors alpha and beta in human bronchial epithelial cells. Mol Cell Endocrinol 305(1–2):12–21. https://doi.org/10.1016/j.mce.2009.01.021
Javed AA, Mayhew AJ, Shea AK, Raina P (2019) Association between hormone therapy and muscle mass in postmenopausal women: a systematic review and meta-analysis. JAMA Netw Open 2(8):e1910154. https://doi.org/10.1001/jamanetworkopen.2019.10154
Jones RL, Nzekwu MM (2006) The effects of body mass index on lung volumes. Chest 130(3):827–833. https://doi.org/10.1378/chest.130.3.827
Judd HL, Lucas WE, Yen SS (1974) Effect of oophorectomy on circulating testosterone and androstenedione levels in patients with endometrial cancer. Am J Obstet Gynecol 118(6):793–798. https://doi.org/10.1016/0002-9378(74)90490-6
Kalidhindi RSR, Katragadda R, Beauchamp KL, Pabelick CM, Prakash YS, Sathish V (2019) Androgen receptor-mediated regulation of intracellular calcium in human airway smooth muscle cells. Cell Physiol Biochem 53(1):215–228. https://doi.org/10.33594/000000131
Kaunitz AM, Pinkerton JV, Manson JE (2020) Hormone therapy and sarcopenia: implications for the prevention of frailty as women age. Menopause 27:496. https://doi.org/10.1097/gme.0000000000001541
Keefe CC, Goldman MM, Zhang K, Clarke N, Reitz RE, Welt CK (2014) Simultaneous measurement of thirteen steroid hormones in women with polycystic ovary syndrome and control women using liquid chromatography-tandem mass spectrometry. PLoS One 9(4):e93805. https://doi.org/10.1371/journal.pone.0093805
Kelsey TW, Wright P, Nelson SM, Anderson RA, Wallace WH (2011) A validated model of serum anti-mullerian hormone from conception to menopause. PLoS One 6(7):e22024. https://doi.org/10.1371/journal.pone.0022024
Khalil RA (2013) Estrogen, vascular estrogen receptor and hormone therapy in postmenopausal vascular disease. Biochem Pharmacol 86(12):1627–1642. https://doi.org/10.1016/j.bcp.2013.09.024
Kluft C, Leuven JA, Helmerhorst FM, Krans HM (2002) Pro-inflammatory effects of oestrogens during use of oral contraceptives and hormone replacement treatment. Vasc Pharmacol 39(3):149–154. https://doi.org/10.1016/s1537-1891(02)00304-x
Krommidas G, Kostikas K, Papatheodorou G, Koutsokera A, Gourgoulianis KI, Roussos C, Koulouris NG, Loukides S (2010) Plasma leptin and adiponectin in COPD exacerbations: associations with inflammatory biomarkers. Respir Med 104(1):40–46. https://doi.org/10.1016/j.rmed.2009.08.012
Kruszynska A, Slowinska-Srzednicka J (2017) Anti-Mullerian hormone (AMH) as a good predictor of time of menopause. Prz Menopauzalny 16(2):47–50. https://doi.org/10.5114/pm.2017.68591
Lambrinoudaki I, Brincat M, Erel CT, Gambacciani M, Moen MH, Schenck-Gustafsson K, Tremollieres F, Vujovic S, Rees M, Rozenberg S (2010) EMAS position statement: managing obese postmenopausal women. Maturitas 66(3):323–326. https://doi.org/10.1016/j.maturitas.2010.03.025
Lavie M, Fisher D, Vilozni D, Forschmidt R, Sarouk I, Kanety H, Hemi R, Efrati O, Modan-Moses D (2015) Glucose intolerance in cystic fibrosis as a determinant of pulmonary function and clinical status. Diabetes Res Clin Pract 110(3):276–284. https://doi.org/10.1016/j.diabres.2015.10.007
Lawlor DA, Ebrahim S, Smith GD (2004) Associations of measures of lung function with insulin resistance and type 2 diabetes: findings from the British Women’s heart and health study. Diabetologia 47(2):195–203. https://doi.org/10.1007/s00125-003-1310-6
Legro RS, Kunselman AR, Dodson WC, Dunaif A (1999) Prevalence and predictors of risk for type 2 diabetes mellitus and impaired glucose tolerance in polycystic ovary syndrome: a prospective, controlled study in 254 affected women. J Clin Endocrinol Metab 84(1):165–169. https://doi.org/10.1210/jcem.84.1.5393
Levy P, Kohler M, McNicholas WT, Barbe F, McEvoy RD, Somers VK, Lavie L, Pepin JL (2015) Obstructive sleep apnoea syndrome. Nat Rev Dis Primers 1:15015. https://doi.org/10.1038/nrdp.2015.15
Lizneva D, Suturina L, Walker W, Brakta S, Gavrilova-Jordan L, Azziz R (2016) Criteria, prevalence, and phenotypes of polycystic ovary syndrome. Fertil Steril 106(1):6–15. https://doi.org/10.1016/j.fertnstert.2016.05.003
Lundblad LK, Thompson-Figueroa J, Leclair T, Sullivan MJ, Poynter ME, Irvin CG, Bates JH (2005) Tumor necrosis factor-alpha overexpression in lung disease: a single cause behind a complex phenotype. Am J Respir Crit Care Med 171(12):1363–1370. https://doi.org/10.1164/rccm.200410-1349OC
Luther RR, Stein HH, Glassman HN, Kleinert HD (1989) Renin inhibitors: specific modulators of the renin-angiotensin system. Arzneimittelforschung 39(1):1–5
Macsali F, Real FG, Omenaas ER, Bjorge L, Janson C, Franklin K, Svanes C (2009) Oral contraception, body mass index, and asthma: a cross-sectional Nordic-Baltic population survey. J Allergy Clin Immunol 123(2):391–397. https://doi.org/10.1016/j.jaci.2008.10.041
Margolis KL, Bonds DE, Rodabough RJ, Tinker L, Phillips LS, Allen C, Bassford T, Burke G, Torrens J, Howard BV (2004) Effect of oestrogen plus progestin on the incidence of diabetes in postmenopausal women: results from the Women’s Health Initiative hormone trial. Diabetologia 47(7):1175–1187. https://doi.org/10.1007/s00125-004-1448-x
Marshall RP (2003) The pulmonary renin-angiotensin system. Curr Pharm Des 9(9):715–722. https://doi.org/10.2174/1381612033455431
Massaro D, Massaro GD (2004) Estrogen regulates pulmonary alveolar formation, loss, and regeneration in mice. Am J Physiol Lung Cell Mol Physiol 287(6):L1154–L1159. https://doi.org/10.1152/ajplung.00228.2004
Massaro GD, Mortola JP, Massaro D (1995) Sexual dimorphism in the architecture of the lung's gas-exchange region. Proc Natl Acad Sci U S A 92(4):1105–1107. https://doi.org/10.1073/pnas.92.4.1105
Mehari A, Afreen S, Ngwa J, Setse R, Thomas AN, Poddar V, Davis W, Polk OD, Hassan S, Thomas AV (2015) Obesity and pulmonary function in African Americans. PLoS One 10(10):e0140610. https://doi.org/10.1371/journal.pone.0140610
Meldrum DR, Davidson BJ, Tataryn IV, Judd HL (1981) Changes in circulating steroids with aging in postmenopausal women. Obstet Gynecol 57(5):624–628
Memoalia J, Anjum B, Singh N, Gupta M (2018) Decline in pulmonary function tests after menopause. J Menopausal Med 24(1):34–40. https://doi.org/10.6118/jmm.2018.24.1.34
Moawad AH, River LP, Kilpatrick SJ (1982) The effect of estrogen and progesterone on beta-adrenergic receptor activity in rabbit lung tissue. Am J Obstet Gynecol 144(5):608–613. https://doi.org/10.1016/0002-9378(82)90235-6
Mohsenin V (2003) Effects of gender on upper airway collapsibility and severity of obstructive sleep apnea. Sleep Med 4(6):523–529. https://doi.org/10.1016/s1389-9457(03)00168-0
Montano LM, Espinoza J, Flores-Soto E, Chavez J, Perusquia M (2014) Androgens are bronchoactive drugs that act by relaxing airway smooth muscle and preventing bronchospasm. J Endocrinol 222(1):1–13. https://doi.org/10.1530/joe-14-0074
Morani A, Barros RP, Imamov O, Hultenby K, Arner A, Warner M, Gustafsson JA (2006) Lung dysfunction causes systemic hypoxia in estrogen receptor beta knockout (ERbeta−/−) mice. Proc Natl Acad Sci U S A 103(18):7165–7169. https://doi.org/10.1073/pnas.0602194103
Murdoch JR, Lloyd CM (2010) Chronic inflammation and asthma. Mutat Res 690(1–2):24–39. https://doi.org/10.1016/j.mrfmmm.2009.09.005
National Institutes of Health (1998) Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults--the evidence report. Obes Res 6(Suppl 2):51s–209s
Nielsen HC (1985) Androgen receptors influence the production of pulmonary surfactant in the testicular feminization mouse fetus. J Clin Invest 76(1):177–181. https://doi.org/10.1172/jci111943
Nielsen HC, Zinman HM, Torday JS (1982) Dihydrotestosterone inhibits fetal rabbit pulmonary surfactant production. J Clin Invest 69(3):611–616. https://doi.org/10.1172/jci110488
North American Menopause Society (2018) The 2017 hormone therapy position statement of the North American menopause society. Menopause 25(11):1362–1387. https://doi.org/10.1097/gme.0000000000001241
Patrone C, Cassel TN, Pettersson K, Piao YS, Cheng G, Ciana P, Maggi A, Warner M, Gustafsson JA, Nord M (2003) Regulation of postnatal lung development and homeostasis by estrogen receptor beta. Mol Cell Biol 23(23):8542–8552. https://doi.org/10.1128/mcb.23.23.8542-8552.2003
Perger E, Mattaliano P, Lombardi C (2019) Menopause and sleep apnea. Maturitas 124:35–38. https://doi.org/10.1016/j.maturitas.2019.02.011
Peters MC, McGrath KW, Hawkins GA, Hastie AT, Levy BD, Israel E, Phillips BR, Mauger DT, Comhair SA, Erzurum SC, Johansson MW, Jarjour NN, Coverstone AM, Castro M, Holguin F, Wenzel SE, Woodruff PG, Bleecker ER, Fahy JV (2016) Plasma interleukin-6 concentrations, metabolic dysfunction, and asthma severity: a cross-sectional analysis of two cohorts. Lancet Respir Med 4(7):574–584. https://doi.org/10.1016/s2213-2600(16)30048-0
Peters U, Suratt BT, Bates JHT, Dixon AE (2018) Beyond BMI: obesity and lung disease. Chest 153(3):702–709. https://doi.org/10.1016/j.chest.2017.07.010
Quinkler M, Sinha B, Tomlinson JW, Bujalska IJ, Stewart PM, Arlt W (2004) Androgen generation in adipose tissue in women with simple obesity--a site-specific role for 17beta-hydroxysteroid dehydrogenase type 5. J Endocrinol 183(2):331–342. https://doi.org/10.1677/joe.1.05762
Raghavan D, Jain R (2016) Increasing awareness of sex differences in airway diseases. Respirology 21(3):449–459. https://doi.org/10.1111/resp.12702
Rannevik G, Jeppsson S, Johnell O, Bjerre B, Laurell-Borulf Y, Svanberg L (1995) A longitudinal study of the perimenopausal transition: altered profiles of steroid and pituitary hormones, SHBG and bone mineral density. Maturitas 21(2):103–113. https://doi.org/10.1016/0378-5122(94)00869-9
Real FG, Svanes C, Omenaas ER, Anto JM, Plana E, Jarvis D, Janson C, Neukirch F, Zemp E, Dratva J, Wjst M, Svanes K, Leynaert B, Sunyer J (2008) Lung function, respiratory symptoms, and the menopausal transition. J Allergy Clin Immunol 121(1):72–80.e73. https://doi.org/10.1016/j.jaci.2007.08.057
Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC, Kotchen JM, Ockene J (2002) Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women’s Health Initiative randomized controlled trial. JAMA 288(3):321–333
Rotterdam ESHRE/ASRM-Sponsored PCOS Consensus Workshop Group (2004) Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome. Fertil Steril 81(1):19–25
Roy AK, Lavrovsky Y, Song CS, Chen S, Jung MH, Velu NK, Bi BY, Chatterjee B (1999) Regulation of androgen action. Vitam Horm 55:309–352
Sagun G, Gedik C, Ekiz E, Karagoz E, Takir M, Oguz A (2015) The relation between insulin resistance and lung function: a cross sectional study. BMC Pulm Med 15:139. https://doi.org/10.1186/s12890-015-0125-9
Sharp JT, Henry JP, Sweany SK, Meadows WR, Pietras RJ (1964) The total work of breathing in normal and obese men. J Clin Invest 43:728–739. https://doi.org/10.1172/jci104957
Shore SA, Schwartzman IN, Mellema MS, Flynt L, Imrich A, Johnston RA (2005) Effect of leptin on allergic airway responses in mice. J Allergy Clin Immunol 115(1):103–109. https://doi.org/10.1016/j.jaci.2004.10.007
Sideleva O, Suratt BT, Black KE, Tharp WG, Pratley RE, Forgione P, Dienz O, Irvin CG, Dixon AE (2012) Obesity and asthma: an inflammatory disease of adipose tissue not the airway. Am J Respir Crit Care Med 186(7):598–605. https://doi.org/10.1164/rccm.201203-0573OC
Sluijmer AV, Heineman MJ, Koudstaal J, Theunissen PH, de Jong FH, Evers JL (1998) Relationship between ovarian production of estrone, estradiol, testosterone, and androstenedione and the ovarian degree of stromal hyperplasia in postmenopausal women. Menopause 5(4):207–210
Soriguer F, Rubio-Martin E, Fernandez D, Valdes S, Garcia-Escobar E, Martin-Nunez GM, Esteva I, Almaraz MC, Rojo-Martinez G (2012) Testosterone, SHBG and risk of type 2 diabetes in the second evaluation of the Pizarra cohort study. Eur J Clin Investig 42(1):79–85. https://doi.org/10.1111/j.1365-2362.2011.02559.x
Straub RH (2007) The complex role of estrogens in inflammation. Endocr Rev 28(5):521–574. https://doi.org/10.1210/er.2007-0001
Svanes O, Bertelsen RJ, Lygre SHL, Carsin AE, Anto JM, Forsberg B, Garcia-Garcia JM, Gullon JA, Heinrich J, Holm M, Kogevinas M, Urrutia I, Leynaert B, Moratalla JM, Le Moual N, Lytras T, Norback D, Nowak D, Olivieri M, Pin I, Probst-Hensch N, Schlunssen V, Sigsgaard T, Skorge TD, Villani S, Jarvis D, Zock JP, Svanes C (2018) Cleaning at home and at work in relation to lung function decline and airway obstruction. Am J Respir Crit Care Med 197(9):1157–1163. https://doi.org/10.1164/rccm.201706-1311OC
Svensson PA, Gabrielsson BG, Jernas M, Gummesson A, Sjoholm K (2008) Regulation of human aldoketo reductase 1C3 (AKR1C3) gene expression in the adipose tissue. Cell Mol Biol Lett 13(4):599–613. https://doi.org/10.2478/s11658-008-0025-6
Szymczak J, Milewicz A, Thijssen JH, Blankenstein MA, Daroszewski J (1998) Concentration of sex steroids in adipose tissue after menopause. Steroids 63(5–6):319–321
Tam A, Wadsworth S, Dorscheid D, Man SF, Sin DD (2014) Estradiol increases mucus synthesis in bronchial epithelial cells. PLoS One 9(6):e100633. https://doi.org/10.1371/journal.pone.0100633
Tchernof A, Mansour MF, Pelletier M, Boulet MM, Nadeau M, Luu-The V (2015) Updated survey of the steroid-converting enzymes in human adipose tissues. J Steroid Biochem Mol Biol 147:56–69. https://doi.org/10.1016/j.jsbmb.2014.11.011
Tchernof A, Brochu D, Maltais-Payette I, Mansour MF, Marchand GB, Carreau AM, Kapeluto J (2018) Androgens and the regulation of adiposity and body fat distribution in humans. Compr Physiol 8(4):1253–1290. https://doi.org/10.1002/cphy.c170009
Tehrani FR, Solaymani-Dodaran M, Azizi F (2009) A single test of anti-mullerian hormone in late reproductive-aged women is a good predictor of menopause. Menopause 16(4):797–802. https://doi.org/10.1097/gme.0b013e318193e95d
Triebner K, Matulonga B, Johannessen A, Suske S, Benediktsdottir B, Demoly P, Dharmage SC, Franklin KA, Garcia-Aymerich J, Gullon Blanco JA, Heinrich J, Holm M, Jarvis D, Jogi R, Lindberg E, Moratalla Rovira JM, Muniozguren Agirre N, Pin I, Probst-Hensch N, Puggini L, Raherison C, Sanchez-Ramos JL, Schlunssen V, Sunyer J, Svanes C, Hustad S, Leynaert B, Gomez Real F (2017) Menopause is associated with accelerated lung function decline. Am J Respir Crit Care Med 195(8):1058–1065. https://doi.org/10.1164/rccm.201605-0968OC
Trigunaite A, Dimo J, Jorgensen TN (2015) Suppressive effects of androgens on the immune system. Cell Immunol 294(2):87–94. https://doi.org/10.1016/j.cellimm.2015.02.004
Uhal BD, Kim JK, Li X, Molina-Molina M (2007) Angiotensin-TGF-beta 1 crosstalk in human idiopathic pulmonary fibrosis: autocrine mechanisms in myofibroblasts and macrophages. Curr Pharm Des 13(12):1247–1256. https://doi.org/10.2174/138161207780618885
Valderhaug TG, Hertel JK, Nordstrand N, Dale PO, Hofso D, Hjelmesaeth J (2015) The association between hyperandrogenemia and the metabolic syndrome in morbidly obese women. Diabetol Metab Syndr 7:46. https://doi.org/10.1186/s13098-015-0040-5
Vidaillac C, Yong VFL, Jaggi TK, Soh MM, Chotirmall SH (2018) Gender differences in bronchiectasis: a real issue? Breathe (Sheff) 14(2):108–121. https://doi.org/10.1183/20734735.000218
Villa MP, Bernardi F, Burnaccini M, Tura A, Martelli M, Mazzanti L, Bergamaschi R, Cacciari E (1990) Bronchial reactivity and sex hormone: study in a Turner’s population. Pediatr Pulmonol 9(4):199–205. https://doi.org/10.1002/ppul.1950090403
Wen J, Wang J, Tang X, Deng S, Dai J, Li X, Cai W (2019) DHT deteriorates the progression of monocrotaline-induced pulmonary arterial hypertension: effects of endogenous and exogenous androgen. Am J Transl Res 11(9):5752–5763
Yanes LL, Reckelhoff JF (2011) Postmenopausal hypertension. Am J Hypertens 24(7):740–749. https://doi.org/10.1038/ajh.2011.71
Yanes LL, Romero DG (2009) Dihydrotestosterone stimulates aldosterone secretion by H295R human adrenocortical cells. Mol Cell Endocrinol 303(1–2):50–56. https://doi.org/10.1016/j.mce.2008.12.020
Yanes LL, Sartori-Valinotti JC, Iliescu R, Romero DG, Racusen LC, Zhang H, Reckelhoff JF (2009) Testosterone-dependent hypertension and upregulation of intrarenal angiotensinogen in Dahl salt-sensitive rats. Am J Physiol Renal Physiol 296(4):F771–F779. https://doi.org/10.1152/ajprenal.90389.2008
Yilmaz I (2019) Angiotensin-converting enzyme inhibitors induce cough. Turk Thorac J 20(1):36–42. https://doi.org/10.5152/TurkThoracJ.2018.18014
Zawadski JK, Dunaif A (1992) Diagnostic criteria for polycystic ovary syndrome: towards a rational approach. In: Dunaif A, Givens JR, Haseltine FP, Merrian GR (eds) Polycystic ovary syndrome. Blackwell Scientific Publications, Boston, pp 377–384
Zhu D, Chung HF, Pandeya N, Dobson AJ, Cade JE, Greenwood DC, Crawford SL, Avis NE, Gold EB, Mitchell ES, Woods NF, Anderson D, Brown DE, Sievert LL, Brunner EJ, Kuh D, Hardy R, Hayashi K, Lee JS, Mizunuma H, Giles GG, Bruinsma F, Tillin T, Simonsen MK, Adami HO, Weiderpass E, Canonico M, Ancelin ML, Demakakos P, Mishra GD (2018) Relationships between intensity, duration, cumulative dose, and timing of smoking with age at menopause: a pooled analysis of individual data from 17 observational studies. PLoS Med 15(11):e1002704. https://doi.org/10.1371/journal.pmed.1002704
Zierau L, Meteran H, Backer V, Lindenberg S, Skytthe A, Thomsen SF (2019) The risk of asthma is increased among women with polycystic ovary syndrome: a twin study. ERJ Open Res 5(3):00018. https://doi.org/10.1183/23120541.00018-2018
Acknowledgments
This study was supported by the National Institute of General Medical Sciences of the National Institutes of Health under Award Number P20GM121334. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2021 This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply
About this chapter
Cite this chapter
Yanes Cardozo, L.L., Rezq, S., Pruett, J.E., Garla, V.V., Romero, D.G. (2021). Androgen Excess in Women and the Respiratory System. In: Silveyra, P., Tigno, X.T. (eds) Sex-Based Differences in Lung Physiology. Physiology in Health and Disease. Springer, Cham. https://doi.org/10.1007/978-3-030-63549-7_14
Download citation
DOI: https://doi.org/10.1007/978-3-030-63549-7_14
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-63548-0
Online ISBN: 978-3-030-63549-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)