Treating exercise-associated low testosterone and its related symptoms

References

• Wheeler GD, Wall SR, Belcastro AN, et al. Reduced serum testosterone and prolactin levels in male distance runners. JAMA. 1984 Jul 27;252(4):514–516. PubMed PMID: 6429357; eng.
   PubMed Web of Science ®Google Scholar
• McColl EM, Wheeler GD, Gomes P, et al. The effects of acute exercise on pulsatile LH release in high-mileage male runners. Clin Endocrinol (Oxf). 1989; Nov31(5):617–621. PubMed PMID: 2627755; eng.
   PubMed Web of Science ®Google Scholar
• Wheeler GD, Singh M, Pierce WD, et al. Endurance training decreases serum testosterone levels in men without change in luteinizing hormone pulsatile release. J Clin Endocrinol Metab. 1991 Feb;72(2):422–425. PubMed PMID: 1899423; eng.
   PubMed Web of Science ®Google Scholar
• Hackney AC, Fahrner CL, Gulledge TP. Basal reproductive hormonal profiles are altered in endurance trained men. J Sports Med Phys Fitness. 1998 Jun;38(2):138–141. PubMed PMID: 9763799; eng.
   PubMed Web of Science ®Google Scholar
• Hackney AC, Fahrner CL, Stupnicki R. Reproductive hormonal responses to maximal exercise in endurance-trained men with low resting testosterone levels. Exp Clin Endocrinol Diabetes. 1997;1055:291–295. PubMed PMID: 9354858; eng
   PubMed Web of Science ®Google Scholar
• Hackney AC, Sinning WE, Bruot BC. Hypothalamic-pituitary-testicular axis function in endurance-trained males. Int J Sports Med. 1990 Aug;11(4):298–303. PubMed PMID: 2228360; eng.
   PubMed Web of Science ®Google Scholar
• Hackney AC, Sinning WE, Bruot BC. Reproductive hormonal profiles of endurance-trained and untrained males. Med Sci Sports Exerc. 1988 Feb;20(1):60–65. PubMed PMID: 3343919; eng.
   PubMed Web of Science ®Google Scholar
• MacConnie SE, Barkan A, Lampman RM, et al. Decreased hypothalamic gonadotropin-releasing hormone secretion in male marathon runners. N Engl J Med. 1986 Aug 14;315(7):411–417. PubMed PMID: 3090437; eng.
   PubMed Web of Science ®Google Scholar
• Hooper DR, Kraemer WJ, Saenz C, et al. The presence of symptoms of testosterone deficiency in the exercise-hypogonadal male condition and the role of nutrition. Eur J Appl Physiol. 2017; Jul117(7):1349–1357. PubMed PMID: 28470410.
   PubMed Web of Science ®Google Scholar
• Hackney AC, Dolny DG, Ness RJ. Comparison of reproductive hormonal profiles in select athletic groups. Biology of Sport. 1988;5(4):297–304.
   Google Scholar
• Hackney AC, Moore AW, Brownlee KK. Testosterone and endurance exercise: development of the “exercise-hypogonadal male condition”. PubMed PMID: 16268050; eng Acta Physiol Hung. 2005;922:121–137.
   PubMedGoogle Scholar
• Hooper DR, Kraemer WJ, Stearns RL, et al. Evidence of the exercise hypogonadal male condition at the 2011 kona ironman world championships. Int J Sports Physiol Perform. 2018 Jun 28:1–22. PubMed PMID: 29952670.
   PubMed Web of Science ®Google Scholar
• Hackney AC. Effects of endurance exercise on the reproductive system of men: the “exercise-hypogonadal male condition”. J Endocrinol Invest. 2008 Oct;31(10):932–938. 5022 [pii]. PubMed PMID: 19092301; eng.
   PubMed Web of Science ®Google Scholar
• Hackney AC, Lane AR, Register-Mihalik J, et al. Endurance exercise training and male sexual libido. Med Sci Sports Exerc. 2017 Jul;49(7):1383–1388. PubMed PMID: 28195945.
   PubMed Web of Science ®Google Scholar
• Meeusen R, Duclos M, Foster C, et al. Prevention, diagnosis, and treatment of the overtraining syndrome: joint consensus statement of the european college of sport science and the american college of sports medicine. Med Sci Sports Exerc. 2013 Jan;45(1):186–205. 00005768-201301000-00027 [pii]. PubMed PMID: 23247672; eng.
   PubMed Web of Science ®Google Scholar
• Tenforde AS, Barrack MT, Nattiv A, et al. Parallels with the female athlete triad in male athletes. Sports Med. 2016; Feb46(2):171–182. PubMed PMID: 26497148.
   PubMed Web of Science ®Google Scholar
• Lane AR, Hackney AC. Reproductive dysfunction from the stress of exercise training is not gender specific: the “exercise-hypogonadal male condition”. J Endocrinol Diabetes. 2014;1(2):4.
   PubMedGoogle Scholar
• Mountjoy M, Sundgot-Borgen J, Burke L, et al. The IOC consensus statement: beyond the female athlete triad–relative energy deficiency in sport (red-S). Br J Sports Med. 2014 Apr;48(7):491–497. PubMed PMID: 24620037.
   PubMed Web of Science ®Google Scholar
• Ayers JW, Komesu Y, Romani T, et al. Anthropomorphic, hormonal, and psychologic correlates of semen quality in endurance-trained male athletes [Research support, non-U.S. gov’t]. Fertility and Sterility. 1985; Jun43(6):917–921. PubMed PMID: 3158553; eng.
   PubMed Web of Science ®Google Scholar
• Bhasin S, Cunningham GR, Hayes FJ, et al. Testosterone therapy in men with androgen deficiency syndromes: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab. 2010 Jun;95(6):2536–2559. PubMed PMID: 20525905.
   PubMed Web of Science ®Google Scholar
• Kraemer WJ, Fragala MS, Watson G, et al. Hormonal responses to a 160-km race across frozen Alaska. Br J Sports Med. 2008; Feb42(2):116–120. DOI: bjsm.2007.035535 [pii] 10.1136/bjsm.2007.035535 PubMed PMID: 17638844; eng.
   PubMed Web of Science ®Google Scholar
• Hooper DR, Kraemer WJ, Kupchak BR, et al. Evidence of exercise-induced hypogonadism at the 2011 ironman world championships. J Strength Cond Res. 2014;28(Supplement 2):51.
   Google Scholar
• Kupchak BR, Kraemer WJ, Hoffman MD, et al. The impact of an ultramarathon on hormonal and biochemical parameters in men. Wilderness Environ Med. 2014 Sep;25(3):278–288. PubMed PMID: 24931590.
   PubMed Web of Science ®Google Scholar
• Arver S, Lehtihet M. Current guidelines for the diagnosis of testosterone deficiency. Front Horm Res. 2009;37:5–20. 175839 [pii]. PubMed PMID: 19011285; eng.
   PubMed Web of Science ®Google Scholar
• Burge MR, Lanzi RA, Skarda ST, et al. Idiopathic hypogonadotropic hypogonadism in a male runner is reversed by clomiphene citrate [Case reports research support, U.S. gov’t, P.H.S.]. Fertility and Sterility. 1997; Apr67(4):783–785. PubMed PMID: 9093212; eng.
   PubMed Web of Science ®Google Scholar
• De Souza MJ, Nattiv A, Joy E, et al. 2014 female athlete triad coalition consensus statement on treatment and return to play of the female athlete triad: 1st international conference held in San Francisco, ca, May 2012, and 2nd international conference held in Indianapolis, in, May 2013. Clin J Sport Med. 2014 Mar;24(2):96–119. PubMed PMID: 24569429.
   PubMed Web of Science ®Google Scholar
• Feicht CB, Johnson TS, Martin BJ, et al. Secondary amenorrhoea in athletes [Letter research support, U.S. gov’t, P.H.S.]. Lancet. 1978 Nov 25;2(8100):1145–1146. PubMed PMID: 82698; eng.
   PubMed Web of Science ®Google Scholar
• De Souza MJ, Miller BE. The effect of endurance training on reproductive function in male runners. A ‘volume threshold’ hypothesis. Sports Med. 1997 Jun;23(6):357–374. PubMed PMID: 9219320.
   PubMed Web of Science ®Google Scholar
• Loucks AB, Verdun M, Heath EM. Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. J Appl Physiol (1985). 1998 Jan;84(1):37–46. PubMed PMID: 9451615.
   PubMed Web of Science ®Google Scholar
• Elliott-Sale KJ, Tenforde AS, Parziale AL, et al. Endocrine effects of relative energy deficiency in sport. Int J Sport Nutr Exerc Metab. 2018;28:4.
   Web of Science ®Google Scholar
• Cumming DC, Quigley ME, Yen SS. Acute suppression of circulating testosterone levels by cortisol in men [research support, non-U.S. gov’tresearch support, U.S. gov’t, P.H.S.]. J Clin Endocrinol Metab. 1983 Sep;57(3):671–673. PubMed PMID: 6348068; eng.
   PubMed Web of Science ®Google Scholar
• Alemany JA, Nindl BC, Kellogg MD, et al. Effects of dietary protein content on IGF-I, testosterone, and body composition during 8 days of severe energy deficit and arduous physical activity[Randomized controlled trial]. J Appl Physiol (1985). 2008 Jul;105(1):58–64. PubMed PMID: 18450989; eng.
   PubMed Web of Science ®Google Scholar
• Opstad PK. Androgenic hormones during prolonged physical stress, sleep, and energy deficiency. J Clin Endocrinol Metab. 1992 May;74(5):1176–1183. PubMed PMID: 1314847.
   PubMed Web of Science ®Google Scholar
• Kelly DM, Jones TH. Testosterone and obesity. Obes Rev. 2015 Jul;16(7):581–606. PubMed PMID: 25982085.
   PubMed Web of Science ®Google Scholar
• Mountjoy M, Sundgot-Borgen JK, Burke LM, et al. IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update. Br J Sports Med. 2018 Jun;52(11):687–697. PubMed PMID: 29773536.
   PubMed Web of Science ®Google Scholar
• Stone JD, Kreutzer A, Mata JD, et al. Changes in creatine kinase and hormones over the course of an American football season. J Strength Conditioning Res. 2017 Apr 04:1. PubMed PMID: 28394834.
   Web of Science ®Google Scholar
• Moore CA, Fry AC. Nonfunctional overreaching during off-season training for skill position players in collegiate American football. J Strength Cond Res. 2007 Aug;21(3):793–800. PubMed PMID: 17685717.
   PubMed Web of Science ®Google Scholar
• Opstad PK. The hypothalamo-pituitary regulation of androgen secretion in young men after prolonged physical stress combined with energy and sleep deprivation. Acta Endocrinol (Copenh). 1992 Sep;127(3):231–236. PubMed PMID: 1414148.
   PubMedGoogle Scholar
• Ratamess NA, Hoffman JR, Kraemer WJ, et al. Effects of a competitive wrestling season on body composition, endocrine markers, and anaerobic exercise performance in NCAA collegiate wrestlers. Eur J Appl Physiol. 2013 May;113(5):1157–1168. PubMed PMID: 23114663; eng.
   PubMed Web of Science ®Google Scholar
• Morley JE, Charlton E, Patrick P, et al. Validation of a screening questionnaire for androgen deficiency in aging males. Metabolism. 2000 Sep;49(9):1239–1242. PubMed PMID: 11016912.
   PubMed Web of Science ®Google Scholar
• Heinemann LA, Saad F, Heinemann K, et al. Can results of the Aging Males’ Symptoms (AMS) scale predict those of screening scales for androgen deficiency? Aging Male. 2004; Sep7(3):211–218. PubMed PMID: 15669540; eng.
   PubMedGoogle Scholar
• Spector IP, Carey MP, Steinberg L. The sexual desire inventory: development, factor structure, and evidence of reliability. J Sex Marital Ther. 1996 Fall;22(3): 175–190. PubMed PMID: 8880651.
   PubMed Web of Science ®Google Scholar
• Bhasin S, Cunningham GR, Hayes FJ, et al. Testosterone therapy in adult men with androgen deficiency syndromes: an endocrine society clinical practice guideline. J Clin Endocrinol Metab. 2006 Jun;91(6):1995–2010. PubMed PMID: 16720669.
   PubMed Web of Science ®Google Scholar
• Vermeulen A, Verdonck L, Kaufman JM. A critical evaluation of simple methods for the estimation of free testosterone in serum. J Clin Endocrinol Metab. 1999 Oct;84(10):3666–3672. PubMed PMID: 10523012.
   PubMed Web of Science ®Google Scholar
• Bhasin S, Pencina M, Jasuja GK, et al. Reference ranges for testosterone in men generated using liquid chromatography tandem mass spectrometry in a community-based sample of healthy nonobese young men in the framingham heart study and applied to three geographically distinct cohorts. J Clin Endocrinol Metab. 2011 Aug;96(8):2430–2439. PubMed PMID: 21697255; PubMed Central PMCID: PMCPMC3146796.
   PubMed Web of Science ®Google Scholar
• Kohrt WM, Bloomfield SA, Little KD, et al. American college of sports medicine position stand: physical activity and bone health. Med Sci Sports Exerc. 2004; Nov36(11):1985–1996. PubMed PMID: 15514517.
   PubMed Web of Science ®Google Scholar
• Schousboe JT, Shepherd JA, Bilezikian JP, et al. Executive summary of the 2013 international society for clinical densitometry position development conference on bone densitometry. J Clin Densitom. 2013 Oct-Dec;16(4):455–466. PubMed PMID: 24183638.
   PubMed Web of Science ®Google Scholar
• Crabtree NJ, Arabi A, Bachrach LK, et al. Dual-energy X-ray absorptiometry interpretation and reporting in children and adolescents: the revised 2013 ISCD pediatric official positions. J Clin Densitom. 2014 Apr-Jun;17(2):225–242. PubMed PMID: 24690232.
   PubMed Web of Science ®Google Scholar
• Nattiv A, Loucks AB, Manore MM, et al. American college of sports medicine position stand. The female athlete triad. Med Sci Sports Exerc. 2007 Oct;39(10):1867–1882. PubMed PMID: 17909417.
   PubMed Web of Science ®Google Scholar
• Barrack MT, Fredericson M, Tenforde AS, et al. Evidence of a cumulative effect for risk factors predicting lower bone mass among male adolescent athletes. Br J Sports Med. 2017.
   Web of Science ®Google Scholar
• Loucks AB. Low energy availability in the marathon and other endurance sports. Sports Med. 2007;37(4–5): 348–352. PubMed PMID: 17465605; eng.
   PubMed Web of Science ®Google Scholar
• Tenforde AS, Fredericson M. Influence of sports participation on bone health in the young athlete: a review of the literature [Review]. PM & R: J Inj Funct and Rehabil. 2011 Sep;3(9):861–867. PubMed PMID: 21944303; eng.
   Google Scholar
• Fredericson M, Chew K, Ngo J, et al. Regional bone mineral density in male athletes: a comparison of soccer players, runners and controls[Comparative study]. Br J Sports Med. 2007; Oct41(10):664–668. discussion 668. PubMed PMID: 17473003; PubMed Central PMCID: PMC2465163. eng.
   PubMed Web of Science ®Google Scholar
• Hind K, Truscott JG, Evans JA. Low lumbar spine bone mineral density in both male and female endurance runners. Bone. 2006 Oct;39(4):880–885. PubMed PMID: 16682267.
   PubMed Web of Science ®Google Scholar
• Tenforde AS, Sainani KL, Sayres LC, et al. Identifying sex-specific risk factors for low bone mineral density in adolescent runners. Am J Sports Med. 2015;43(6):1494–1504.
   PubMed Web of Science ®Google Scholar
• Smathers AM, Bemben MG, Bemben DA. Bone density comparisons in male competitive road cyclists and untrained controls. Med Sci Sports Exerc. 2009 Feb;41(2):290–296. PubMed PMID: 19127198.
   PubMed Web of Science ®Google Scholar
• Nichols JF, Rauh MJ. Longitudinal changes in bone mineral density in male master cyclists and nonathletes. J Strength Cond res/NSCA. 2011 Mar;25(3):727–734. PubMed PMID: 20581701.
   PubMed Web of Science ®Google Scholar
• Freitas L, Amorim T, Humbert L, et al. Cortical and trabecular bone analysis of professional dancers using 3D-DXA: a case-control study. J Sports Sci. 2018 Jun 18:1–8. PubMed PMID: 29912627.
   Web of Science ®Google Scholar
• Ihle R, Loucks AB. Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Mineral Res: Off J Am Soc Bone Mineral Res. 2004 Aug;19(8):1231–1240. PubMed PMID: 15231009.
   PubMed Web of Science ®Google Scholar
• Medicine I. Dietary reference intakes for calcium and vitamin D. National academy of sciences; Nov 2010, Report Brief 2010 [ cited 2018 Jul 08]. http://www.nationalacademies.org/hmd/Reports/2010/Dietary-Reference-Intakes-for-Calcium-and-Vitamin-D/DRI-Values.aspx?
   Google Scholar
• Matias CN, Santos DA, Monteiro CP, et al. Magnesium intake mediates the association between bone mineral density and lean soft tissue in elite swimmers. Magnes Res. 2012 Jul-Sep;25(3):120–125. PubMed PMID: 23015157.
   PubMed Web of Science ®Google Scholar
• Allison RJ, Farooq A, Hamilton B, et al. No association between vitamin D deficiency and markers of bone health in athletes. Med Sci Sports Exerc. 2015 Apr;47(4):782–788. PubMed PMID: 25058327.
   PubMed Web of Science ®Google Scholar
• Ben-Sasson SA, Finestone A, Moskowitz M, et al. Extended duration of vertical position might impair bone metabolism. Eur J Clin Invest. 1994; Jun24(6):421–425. PubMed PMID: 7957496.
   PubMed Web of Science ®Google Scholar
• Finestone A, Milgrom C. How stress fracture incidence was lowered in the Israeli army: a 25-yr struggle. Med Sci Sports Exerc. 2008 Nov;40(11 Suppl):S623–9. PubMed PMID: 18849873.
   PubMed Web of Science ®Google Scholar
• Fredericson M, Ngo J, Cobb K. Effects of ball sports on future risk of stress fracture in runners[comparative study]. Clin J Sport Med: Off J Can Acad Sport Med. 2005 May;15(3):136–141. PubMed PMID: 15867555; eng.
   PubMed Web of Science ®Google Scholar
• Tenforde AS, Sayres LC, McCurdy ML, et al. Identifying sex-specific risk factors for stress fractures in adolescent runners. Med Sci Sports Exerc. 2013 Oct;45(10):1843–1851. PubMed PMID: 23584402; eng.
   PubMed Web of Science ®Google Scholar
• Milgrom C, Simkin A, Eldad A, et al. Using bone’s adaptation ability to lower the incidence of stress fractures [Research support, non-U.S. Gov’t]. Am J Sports Med. 2000; Mar-Apr28(2):245–251. PubMed PMID: 10751003; eng.
   PubMed Web of Science ®Google Scholar
• Hammami MA, Ben Abderrahman A, Hackney AC, et al. Hormonal (Cortical-gonadotropic axis) and physical changes with two years intense exercise training in elite young soccer players. J Strength Cond Res. 2017 Sep;31(9):2388–2397. PubMed PMID: 27676275.
   PubMed Web of Science ®Google Scholar
• World Anti Doping Agency Prohibited List [10/23/2017]. [ cited 2018 Jul 08]. https://www.wada-ama.org/en/prohibited-list
   Google Scholar
• Milgrom C, Finestone A, Novack V, et al. The effect of prophylactic treatment with risedronate on stress fracture incidence among infantry recruits. Bone. 2004 Aug;35(2):418–424. PubMed PMID: 15268892.
   PubMed Web of Science ®Google Scholar
• Topo E, Soricelli A, D’Aniello A, et al. The role and molecular mechanism of D-aspartic acid in the release and synthesis of LH and testosterone in humans and rats. Reprod Biol Endocrinol. 2009 Oct 27;7:120. PubMed PMID: 19860889; PubMed Central PMCID: PMCPMC2774316.
   PubMed Web of Science ®Google Scholar
• Rao A, Steels E, Inder WJ, et al. Testofen, a specialised Trigonella foenum-graecum seed extract reduces age-related symptoms of androgen decrease, increases testosterone levels and improves sexual function in healthy aging males in a double-blind randomised clinical study. Aging Male. 2016 Jun;19(2):134–142. PubMed PMID: 26791805.
   PubMed Web of Science ®Google Scholar
• Poole C, Bushey B, Foster C, et al. The effects of a commercially available botanical supplement on strength, body composition, power output, and hormonal profiles in resistance-trained males. J Int Soc Sports Nutr. 2010 Oct 27;7:34. PubMed PMID: 20979623; PubMed Central PMCID: PMCPMC2978122.
   PubMed Web of Science ®Google Scholar