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Published in: Sports Medicine 2/2016

01-02-2016 | Review Article

Parallels with the Female Athlete Triad in Male Athletes

Authors: Adam S. Tenforde, Michelle T. Barrack, Aurelia Nattiv, Michael Fredericson

Published in: Sports Medicine | Issue 2/2016

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Abstract

Participation in sports offers many health benefits to athletes of both sexes. However, subsets of both female and male athletes are at increased risk of impaired bone health and bone stress injuries. The Female Athlete Triad (Triad) is defined as the interrelationship of low energy availability (with or without disordered eating), menstrual dysfunction, and low bone mineral density. The Triad may result in health consequences, including bone stress injuries. Our review presents evidence that an analogous process may occur in male athletes. Our review of the available literature indicates that a subset of male athletes may experience adverse health issues that parallel those associated with the Triad, including low energy availability (with or without disordered eating), hypogonadotropic hypogonadism, and low bone mineral density. Consequently, male athletes may be predisposed to developing bone stress injuries, and these injuries can be the first presenting feature of associated Triad conditions. We discuss the evidence for impaired nutrition, hormonal dysfunction, and low bone mineral density in a subset of male athletes, and how these health issues may parallel those of the Triad. With further research into the mechanisms and outcomes of these health concerns in active and athletic men, evidence-based guidelines can be developed that result in best practice.
Literature
1.
go back to reference Yeager KK, Agostini R, Nattiv A, Drinkwater B. The female athlete triad: disordered eating, amenorrhea, osteoporosis. Med Sci Sports Exerc. 1993;25(7):775–7.PubMedCrossRef Yeager KK, Agostini R, Nattiv A, Drinkwater B. The female athlete triad: disordered eating, amenorrhea, osteoporosis. Med Sci Sports Exerc. 1993;25(7):775–7.PubMedCrossRef
2.
go back to reference Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP, et al. American College of Sports Medicine position stand. The female athlete triad. Med Sci Sports Exerc. 2007;39(10):1867–82.PubMedCrossRef Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP, et al. American College of Sports Medicine position stand. The female athlete triad. Med Sci Sports Exerc. 2007;39(10):1867–82.PubMedCrossRef
3.
go back to reference De Souza MJ, Nattiv A, Joy E, Misra M, Williams NI, Mallinson RJ, 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, California, May 2012 and 2nd International Conference held in Indianapolis, Indiana, May 2013. Br J Sports Med. 2014;48(4):289.PubMedCrossRef De Souza MJ, Nattiv A, Joy E, Misra M, Williams NI, Mallinson RJ, 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, California, May 2012 and 2nd International Conference held in Indianapolis, Indiana, May 2013. Br J Sports Med. 2014;48(4):289.PubMedCrossRef
4.
go back to reference Barrack MT, Van Loan MD, Rauh MJ, Nichols JF. Body mass, training, menses, and bone in adolescent runners: a 3-yr follow-up. Med Sci Sports Exerc. 2011;43(6):959–66.PubMedCrossRef Barrack MT, Van Loan MD, Rauh MJ, Nichols JF. Body mass, training, menses, and bone in adolescent runners: a 3-yr follow-up. Med Sci Sports Exerc. 2011;43(6):959–66.PubMedCrossRef
5.
go back to reference Burge MR, Lanzi RA, Skarda ST, Eaton RP. Idiopathic hypogonadotropic hypogonadism in a male runner is reversed by clomiphene citrate. Fert Steril. 1997;67(4):783–5.CrossRef Burge MR, Lanzi RA, Skarda ST, Eaton RP. Idiopathic hypogonadotropic hypogonadism in a male runner is reversed by clomiphene citrate. Fert Steril. 1997;67(4):783–5.CrossRef
6.
go back to reference Thienpont E, Bellemans J, Samson I, Fabry G. Stress fracture of the inferior and superior pubic ramus in a man with anorexia nervosa and hypogonadism. Acta Orthop Belg. 2000;66(3):297–301.PubMed Thienpont E, Bellemans J, Samson I, Fabry G. Stress fracture of the inferior and superior pubic ramus in a man with anorexia nervosa and hypogonadism. Acta Orthop Belg. 2000;66(3):297–301.PubMed
7.
go back to reference Touhy J, Nattiv A, Streja L. A prospective analysis of tibial stress fracture incidence, distribution and risk factors in collegiate track athletes. Clin J Sport Med. 2008;18(2):186. Touhy J, Nattiv A, Streja L. A prospective analysis of tibial stress fracture incidence, distribution and risk factors in collegiate track athletes. Clin J Sport Med. 2008;18(2):186.
8.
go back to reference Hackney AC. Effects of endurance exercise on the reproductive system of men: the “exercise-hypogonadal male condition”. J Endocrinol Invest. 2008;31(10):932–8.PubMedCrossRef Hackney AC. Effects of endurance exercise on the reproductive system of men: the “exercise-hypogonadal male condition”. J Endocrinol Invest. 2008;31(10):932–8.PubMedCrossRef
9.
go back to reference Loucks AB. Low energy availability in the marathon and other endurance sports. Sports Med. 2007;37(4–5):348–52.PubMedCrossRef Loucks AB. Low energy availability in the marathon and other endurance sports. Sports Med. 2007;37(4–5):348–52.PubMedCrossRef
10.
go back to reference Ihle R, Loucks AB. Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res. 2004;19(8):1231–40.PubMedCrossRef Ihle R, Loucks AB. Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res. 2004;19(8):1231–40.PubMedCrossRef
11.
go back to reference Dolan E, O’Connor H, McGoldrick A, O’Loughlin G, Lyons D, Warrington G. Nutritional, lifestyle, and weight control practices of professional jockeys. J Sports Sci. 2011;29(8):791–9.PubMedCrossRef Dolan E, O’Connor H, McGoldrick A, O’Loughlin G, Lyons D, Warrington G. Nutritional, lifestyle, and weight control practices of professional jockeys. J Sports Sci. 2011;29(8):791–9.PubMedCrossRef
12.
go back to reference Beals KA, Manore MM. Nutritional status of female athletes with subclinical eating disorders. J Am Diet Assoc. 1998;98(4):419–25.PubMedCrossRef Beals KA, Manore MM. Nutritional status of female athletes with subclinical eating disorders. J Am Diet Assoc. 1998;98(4):419–25.PubMedCrossRef
13.
go back to reference Sundgot-Borgen J, Torstveit MK. Prevalence of eating disorders in elite athletes is higher than in the general population. Clin J Sport Med. 2004;14(1):25–32.PubMedCrossRef Sundgot-Borgen J, Torstveit MK. Prevalence of eating disorders in elite athletes is higher than in the general population. Clin J Sport Med. 2004;14(1):25–32.PubMedCrossRef
14.
go back to reference Chatterton JM, Petrie TA. Prevalence of disordered eating and pathogenic weight control behaviors among male collegiate athletes. Eat Disord. 2013;21(4):328–41.PubMedCrossRef Chatterton JM, Petrie TA. Prevalence of disordered eating and pathogenic weight control behaviors among male collegiate athletes. Eat Disord. 2013;21(4):328–41.PubMedCrossRef
15.
go back to reference van Erp-Baart AM, Saris WH, Binkhorst RA, Vos JA, Elvers JW. Nationwide survey on nutritional habits in elite athletes. Part I. Energy, carbohydrate, protein, and fat intake. Int J Sports Med. 1989;10(Suppl 1):S3–10.PubMedCrossRef van Erp-Baart AM, Saris WH, Binkhorst RA, Vos JA, Elvers JW. Nationwide survey on nutritional habits in elite athletes. Part I. Energy, carbohydrate, protein, and fat intake. Int J Sports Med. 1989;10(Suppl 1):S3–10.PubMedCrossRef
16.
go back to reference Rankinen T, Fogelholm M, Kujala U, Rauramaa R, Uusitupa M. Dietary intake and nutritional status of athletic and nonathletic children in early puberty. Int J Sport Nutr. 1995;5(2):136–50.PubMed Rankinen T, Fogelholm M, Kujala U, Rauramaa R, Uusitupa M. Dietary intake and nutritional status of athletic and nonathletic children in early puberty. Int J Sport Nutr. 1995;5(2):136–50.PubMed
17.
go back to reference Hickson JF Jr, Duke MA, Risser WL, Johnson CW, Palmer R, Stockton JE. Nutritional intake from food sources of high school football athletes. J Am Diet Assoc. 1987;87(12):1656–9.PubMed Hickson JF Jr, Duke MA, Risser WL, Johnson CW, Palmer R, Stockton JE. Nutritional intake from food sources of high school football athletes. J Am Diet Assoc. 1987;87(12):1656–9.PubMed
18.
go back to reference Rico-Sanz J, Frontera WR, Mole PA, Rivera MA, Rivera-Brown A, Meredith CN. Dietary and performance assessment of elite soccer players during a period of intense training. Int J Sport Nutr. 1998;8(3):230–40.PubMed Rico-Sanz J, Frontera WR, Mole PA, Rivera MA, Rivera-Brown A, Meredith CN. Dietary and performance assessment of elite soccer players during a period of intense training. Int J Sport Nutr. 1998;8(3):230–40.PubMed
19.
go back to reference Petrie HJ, Stover EA, Horswill CA. Nutritional concerns for the child and adolescent competitor. Nutrition. 2004;20(7–8):620–31.PubMedCrossRef Petrie HJ, Stover EA, Horswill CA. Nutritional concerns for the child and adolescent competitor. Nutrition. 2004;20(7–8):620–31.PubMedCrossRef
20.
go back to reference Horswill CA, Park SH, Roemmich JN. Changes in the protein nutritional status of adolescent wrestlers. Med Sci Sports Exerc. 1990;22(5):599–604.PubMedCrossRef Horswill CA, Park SH, Roemmich JN. Changes in the protein nutritional status of adolescent wrestlers. Med Sci Sports Exerc. 1990;22(5):599–604.PubMedCrossRef
21.
go back to reference Fogelholm GM, Koskinen R, Laakso J, Rankinen T, Ruokonen I. Gradual and rapid weight loss: effects on nutrition and performance in male athletes. Med Sci Sports Exerc. 1993;25(3):371–7.PubMedCrossRef Fogelholm GM, Koskinen R, Laakso J, Rankinen T, Ruokonen I. Gradual and rapid weight loss: effects on nutrition and performance in male athletes. Med Sci Sports Exerc. 1993;25(3):371–7.PubMedCrossRef
22.
go back to reference Julian-Almarcegui C, Gomez-Cabello A, Gonzalez-Aguero A, Olmedillas H, Gomez-Bruton A, Matute-Llorente A, et al. The nutritional status in adolescent Spanish cyclists. Nutr Hosp. 2013;28(4):1184–9.PubMed Julian-Almarcegui C, Gomez-Cabello A, Gonzalez-Aguero A, Olmedillas H, Gomez-Bruton A, Matute-Llorente A, et al. The nutritional status in adolescent Spanish cyclists. Nutr Hosp. 2013;28(4):1184–9.PubMed
23.
go back to reference Riebl SK, Subudhi AW, Broker JP, Schenck K, Berning JR. The prevalence of subclinical eating disorders among male cyclists. J Am Diet Assoc. 2007;107(7):1214–7.PubMedCrossRef Riebl SK, Subudhi AW, Broker JP, Schenck K, Berning JR. The prevalence of subclinical eating disorders among male cyclists. J Am Diet Assoc. 2007;107(7):1214–7.PubMedCrossRef
24.
go back to reference Barrack MT, Giacomazzi C, Barrack FA, Nattiv A. Diet patterns, anthropometric measures, bone density and injury among male adolescent runners and non-runner athletes. Med Sci Sports Exerc. 2012;44(5S Supplement 2):109. Barrack MT, Giacomazzi C, Barrack FA, Nattiv A. Diet patterns, anthropometric measures, bone density and injury among male adolescent runners and non-runner athletes. Med Sci Sports Exerc. 2012;44(5S Supplement 2):109.
25.
go back to reference Glace BW, Murphy CA, McHugh MP. Food intake and electrolyte status of ultramarathoners competing in extreme heat. J Am Coll Nutr. 2002;21(6):553–9.PubMedCrossRef Glace BW, Murphy CA, McHugh MP. Food intake and electrolyte status of ultramarathoners competing in extreme heat. J Am Coll Nutr. 2002;21(6):553–9.PubMedCrossRef
26.
go back to reference Eden BD, Abernethy PJ. Nutritional intake during an ultraendurance running race. Int J Sport Nutr. 1994;4(2):166–74.PubMed Eden BD, Abernethy PJ. Nutritional intake during an ultraendurance running race. Int J Sport Nutr. 1994;4(2):166–74.PubMed
27.
go back to reference Pfeiffer B, Stellingwerff T, Hodgson AB, Randell R, Pottgen K, Res P, et al. Nutritional intake and gastrointestinal problems during competitive endurance events. Med Sci Sports Exerc. 2012;44(2):344–51.PubMedCrossRef Pfeiffer B, Stellingwerff T, Hodgson AB, Randell R, Pottgen K, Res P, et al. Nutritional intake and gastrointestinal problems during competitive endurance events. Med Sci Sports Exerc. 2012;44(2):344–51.PubMedCrossRef
28.
go back to reference Petrie TA, Greenleaf C, Reel J, Carter J. Prevalence of eating disorders and disordered eating behaviors among male collegiate athletes. Psychol Men Masc. 2008;9(4):267–77.CrossRef Petrie TA, Greenleaf C, Reel J, Carter J. Prevalence of eating disorders and disordered eating behaviors among male collegiate athletes. Psychol Men Masc. 2008;9(4):267–77.CrossRef
29.
go back to reference Johnson C, Powers PS, Dick R. Athletes and eating disorders: the National Collegiate Athletic Association study. Int J Eat Disord. 1999;26(2):179–88.PubMedCrossRef Johnson C, Powers PS, Dick R. Athletes and eating disorders: the National Collegiate Athletic Association study. Int J Eat Disord. 1999;26(2):179–88.PubMedCrossRef
30.
go back to reference Oppliger RA, Landry GL, Foster SW, Lambrecht AC. Wisconsin minimum weight program reduces weight-cutting practices of high school wrestlers. Clin J Sport Med. 1998;8(1):26–31.PubMedCrossRef Oppliger RA, Landry GL, Foster SW, Lambrecht AC. Wisconsin minimum weight program reduces weight-cutting practices of high school wrestlers. Clin J Sport Med. 1998;8(1):26–31.PubMedCrossRef
31.
go back to reference Oppliger RA, Steen SA, Scott JR. Weight loss practices of college wrestlers. Int J Sport Nutr Exerc Metab. 2003;13(1):29–46.PubMed Oppliger RA, Steen SA, Scott JR. Weight loss practices of college wrestlers. Int J Sport Nutr Exerc Metab. 2003;13(1):29–46.PubMed
33.
go back to reference Moore JM, Timperio AF, Crawford DA, Burns CM, Cameron-Smith D. Weight management and weight loss strategies of professional jockeys. Int J Sport Nutr Exerc Metab. 2002;12(1):1–13.PubMed Moore JM, Timperio AF, Crawford DA, Burns CM, Cameron-Smith D. Weight management and weight loss strategies of professional jockeys. Int J Sport Nutr Exerc Metab. 2002;12(1):1–13.PubMed
34.
go back to reference Pietrowsky R, Straub K. Body dissatisfaction and restrained eating in male juvenile and adult athletes. Eat Weight Disord. 2008;13(1):14–21.PubMedCrossRef Pietrowsky R, Straub K. Body dissatisfaction and restrained eating in male juvenile and adult athletes. Eat Weight Disord. 2008;13(1):14–21.PubMedCrossRef
35.
go back to reference Thiel A, Gottfried H, Hesse FW. Subclinical eating disorders in male athletes. A study of the low weight category in rowers and wrestlers. Acta Psychiatr Scand. 1993;88(4):259–65.PubMedCrossRef Thiel A, Gottfried H, Hesse FW. Subclinical eating disorders in male athletes. A study of the low weight category in rowers and wrestlers. Acta Psychiatr Scand. 1993;88(4):259–65.PubMedCrossRef
36.
go back to reference Rouveix M, Bouget M, Pannafieux C, Champely S, Filaire E. Eating attitudes, body esteem, perfectionism and anxiety of judo athletes and nonathletes. Int J Sports Med. 2007;28(4):340–5.PubMedCrossRef Rouveix M, Bouget M, Pannafieux C, Champely S, Filaire E. Eating attitudes, body esteem, perfectionism and anxiety of judo athletes and nonathletes. Int J Sports Med. 2007;28(4):340–5.PubMedCrossRef
37.
go back to reference Ferrand C, Brunet E. Perfectionism and risk for disordered eating among young French male cyclists of high performance. Percept Mot Skills. 2004;99(3 Pt 1):959–67.PubMed Ferrand C, Brunet E. Perfectionism and risk for disordered eating among young French male cyclists of high performance. Percept Mot Skills. 2004;99(3 Pt 1):959–67.PubMed
38.
go back to reference Filaire E, Rouveix M, Pannafieux C, Ferrand C. Eating attitudes, perfectionism and body-esteem of elite male judoists and cyclists. J Sports Sci Med. 2007;6(1):50–7.PubMedCentralPubMed Filaire E, Rouveix M, Pannafieux C, Ferrand C. Eating attitudes, perfectionism and body-esteem of elite male judoists and cyclists. J Sports Sci Med. 2007;6(1):50–7.PubMedCentralPubMed
39.
go back to reference Tenforde AS, Sayres LC, McCurdy ML, Collado H, Sainani KL, Fredericson M. Overuse injuries in high school runners: lifetime prevalence and prevention strategies. PM R. 2011;3(2):125–31 (quiz 31). Tenforde AS, Sayres LC, McCurdy ML, Collado H, Sainani KL, Fredericson M. Overuse injuries in high school runners: lifetime prevalence and prevention strategies. PM R. 2011;3(2):125–31 (quiz 31).
40.
go back to reference Wheeler GD, Wall SR, Belcastro AN, Conger P, Cumming DC. Are anorexic tendencies prevalent in the habitual runner? Br J Sports Med. 1986;20(2):77–81.PubMedCentralPubMedCrossRef Wheeler GD, Wall SR, Belcastro AN, Conger P, Cumming DC. Are anorexic tendencies prevalent in the habitual runner? Br J Sports Med. 1986;20(2):77–81.PubMedCentralPubMedCrossRef
41.
go back to reference DiGioacchino DeBate R, Wethington H, Sargent R. Sub-clinical eating disorder characteristics among male and female triathletes. Eat Weight Disord. 2002;7(3):210–20. DiGioacchino DeBate R, Wethington H, Sargent R. Sub-clinical eating disorder characteristics among male and female triathletes. Eat Weight Disord. 2002;7(3):210–20.
42.
go back to reference Goltz FR, Stenzel LM, Schneider CD. Disordered eating behaviors and body image in male athletes. Rev Bras Psiquiatr. 2013;35(3):237–42.PubMedCrossRef Goltz FR, Stenzel LM, Schneider CD. Disordered eating behaviors and body image in male athletes. Rev Bras Psiquiatr. 2013;35(3):237–42.PubMedCrossRef
43.
go back to reference Williams NI, Leidy HJ, Hill BR, Lieberman JL, Legro RS, De Souza MJ. Magnitude of daily energy deficit predicts frequency but not severity of menstrual disturbances associated with exercise and caloric restriction. Am J Physiol Endocrinol Metab. 2015;308(1):E29–39.PubMedCentralPubMedCrossRef Williams NI, Leidy HJ, Hill BR, Lieberman JL, Legro RS, De Souza MJ. Magnitude of daily energy deficit predicts frequency but not severity of menstrual disturbances associated with exercise and caloric restriction. Am J Physiol Endocrinol Metab. 2015;308(1):E29–39.PubMedCentralPubMedCrossRef
44.
go back to reference De Souza MJ, Miller BE. The effect of endurance training on reproductive function in male runners. A ‘volume threshold’ hypothesis. Sports Med. 1997;23(6):357–74.PubMedCrossRef De Souza MJ, Miller BE. The effect of endurance training on reproductive function in male runners. A ‘volume threshold’ hypothesis. Sports Med. 1997;23(6):357–74.PubMedCrossRef
45.
go back to reference McColl EM, Wheeler GD, Gomes P, Bhambhani Y, Cumming DC. The effects of acute exercise on pulsatile LH release in high-mileage male runners. Clin Endocrinol. 1989;31(5):617–21.CrossRef McColl EM, Wheeler GD, Gomes P, Bhambhani Y, Cumming DC. The effects of acute exercise on pulsatile LH release in high-mileage male runners. Clin Endocrinol. 1989;31(5):617–21.CrossRef
46.
go back to reference Hackney AC, Sinning WE, Bruot BC. Reproductive hormonal profiles of endurance-trained and untrained males. Med Sci Sports Exerc. 1988;20(1):60–5.PubMedCrossRef Hackney AC, Sinning WE, Bruot BC. Reproductive hormonal profiles of endurance-trained and untrained males. Med Sci Sports Exerc. 1988;20(1):60–5.PubMedCrossRef
47.
go back to reference Roberts AC, McClure RD, Weiner RI, Brooks GA. Overtraining affects male reproductive status. Fert Steril. 1993;60(4):686–92. Roberts AC, McClure RD, Weiner RI, Brooks GA. Overtraining affects male reproductive status. Fert Steril. 1993;60(4):686–92.
48.
go back to reference Gomez-Merino D, Chennaoui M, Drogou C, Bonneau D, Guezennec CY. Decrease in serum leptin after prolonged physical activity in men. Med Sci Sports Exerc. 2002;34(10):1594–9.PubMedCrossRef Gomez-Merino D, Chennaoui M, Drogou C, Bonneau D, Guezennec CY. Decrease in serum leptin after prolonged physical activity in men. Med Sci Sports Exerc. 2002;34(10):1594–9.PubMedCrossRef
49.
go back to reference Arce JC, De Souza MJ, Pescatello LS, Luciano AA. Subclinical alterations in hormone and semen profile in athletes. Fert Steril. 1993;59(2):398–404. Arce JC, De Souza MJ, Pescatello LS, Luciano AA. Subclinical alterations in hormone and semen profile in athletes. Fert Steril. 1993;59(2):398–404.
50.
go back to reference Wheeler GD, Singh M, Pierce WD, Epling WF, Cumming DC. Endurance training decreases serum testosterone levels in men without change in luteinizing hormone pulsatile release. J Clin Endocrinol Metabol. 1991;72(2):422–5.CrossRef Wheeler GD, Singh M, Pierce WD, Epling WF, Cumming DC. Endurance training decreases serum testosterone levels in men without change in luteinizing hormone pulsatile release. J Clin Endocrinol Metabol. 1991;72(2):422–5.CrossRef
51.
go back to reference Bennell KL, Brukner PD, Malcolm SA. Effect of altered reproductive function and lowered testosterone levels on bone density in male endurance athletes. Br J Sports Med. 1996;30(3):205–8.PubMedCentralPubMedCrossRef Bennell KL, Brukner PD, Malcolm SA. Effect of altered reproductive function and lowered testosterone levels on bone density in male endurance athletes. Br J Sports Med. 1996;30(3):205–8.PubMedCentralPubMedCrossRef
52.
go back to reference Hackney AC, Fahrner CL, Gulledge TP. Basal reproductive hormonal profiles are altered in endurance trained men. J Sports Med Phys Fit. 1998;38(2):138–41. Hackney AC, Fahrner CL, Gulledge TP. Basal reproductive hormonal profiles are altered in endurance trained men. J Sports Med Phys Fit. 1998;38(2):138–41.
53.
go back to reference MacConnie SE, Barkan A, Lampman RM, Schork MA, Beitins IZ. Decreased hypothalamic gonadotropin-releasing hormone secretion in male marathon runners. N Engl J Med. 1986;315(7):411–7.PubMedCrossRef MacConnie SE, Barkan A, Lampman RM, Schork MA, Beitins IZ. Decreased hypothalamic gonadotropin-releasing hormone secretion in male marathon runners. N Engl J Med. 1986;315(7):411–7.PubMedCrossRef
54.
go back to reference De Souza MJ, Arce JC, Pescatello LS, Scherzer HS, Luciano AA. Gonadal hormones and semen quality in male runners. A volume threshold effect of endurance training. Int J Sports Med. 1994;15(7):383–91.PubMedCrossRef De Souza MJ, Arce JC, Pescatello LS, Scherzer HS, Luciano AA. Gonadal hormones and semen quality in male runners. A volume threshold effect of endurance training. Int J Sports Med. 1994;15(7):383–91.PubMedCrossRef
55.
go back to reference Hackney AC, Sinning WE, Bruot BC. Hypothalamic-pituitary-testicular axis function in endurance-trained males. Int J Sports Med. 1990;11(4):298–303.PubMedCrossRef Hackney AC, Sinning WE, Bruot BC. Hypothalamic-pituitary-testicular axis function in endurance-trained males. Int J Sports Med. 1990;11(4):298–303.PubMedCrossRef
56.
go back to reference Ayers JW, Komesu Y, Romani T, Ansbacher R. Anthropomorphic, hormonal, and psychologic correlates of semen quality in endurance-trained male athletes. Fert Steril. 1985;43(6):917–21. Ayers JW, Komesu Y, Romani T, Ansbacher R. Anthropomorphic, hormonal, and psychologic correlates of semen quality in endurance-trained male athletes. Fert Steril. 1985;43(6):917–21.
57.
go back to reference Bagatell CJ, Bremner WJ. Sperm counts and reproductive hormones in male marathoners and lean controls. Fert Steril. 1990;53(4):688–92. Bagatell CJ, Bremner WJ. Sperm counts and reproductive hormones in male marathoners and lean controls. Fert Steril. 1990;53(4):688–92.
58.
go back to reference Gutin B, Alejandro D, Duni T, Segal K, Phillips GB. Levels of serum sex hormones and risk factors for coronary heart disease in exercise-trained men. Am J Med. 1985;79(1):79–84.PubMedCrossRef Gutin B, Alejandro D, Duni T, Segal K, Phillips GB. Levels of serum sex hormones and risk factors for coronary heart disease in exercise-trained men. Am J Med. 1985;79(1):79–84.PubMedCrossRef
59.
go back to reference Mathur DN, Toriola AL, Dada OA. Serum cortisol and testosterone levels in conditioned male distance runners and nonathletes after maximal exercise. J Sports Med Phys Fit. 1986;26(3):245–50. Mathur DN, Toriola AL, Dada OA. Serum cortisol and testosterone levels in conditioned male distance runners and nonathletes after maximal exercise. J Sports Med Phys Fit. 1986;26(3):245–50.
60.
go back to reference Griffith RO, Dressendorfer RH, Fullbright CD, Wade CE. Testicular function during exhaustive training. Phys Sports Med. 1990;18:54–64. Griffith RO, Dressendorfer RH, Fullbright CD, Wade CE. Testicular function during exhaustive training. Phys Sports Med. 1990;18:54–64.
61.
go back to reference Vinther A, Kanstrup IL, Christiansen E, Ekdahl C, Aagaard P. Testosterone and BMD in elite male lightweight rowers. Int J Sports Med. 2008;29(10):803–7.PubMedCrossRef Vinther A, Kanstrup IL, Christiansen E, Ekdahl C, Aagaard P. Testosterone and BMD in elite male lightweight rowers. Int J Sports Med. 2008;29(10):803–7.PubMedCrossRef
62.
go back to reference Smith R, Rutherford OM. Spine and total body bone mineral density and serum testosterone levels in male athletes. Eur J Appl Physiol Occup Physiol. 1993;67(4):330–4.PubMedCrossRef Smith R, Rutherford OM. Spine and total body bone mineral density and serum testosterone levels in male athletes. Eur J Appl Physiol Occup Physiol. 1993;67(4):330–4.PubMedCrossRef
63.
go back to reference Maimoun L, Lumbroso S, Manetta J, Paris F, Leroux JL, Sultan C. Testosterone is significantly reduced in endurance athletes without impact on bone mineral density. Horm Res. 2003;59(6):285–92.PubMedCrossRef Maimoun L, Lumbroso S, Manetta J, Paris F, Leroux JL, Sultan C. Testosterone is significantly reduced in endurance athletes without impact on bone mineral density. Horm Res. 2003;59(6):285–92.PubMedCrossRef
64.
go back to reference Hackney AC. Endurance exercise training and reproductive endocrine dysfunction in men: alterations in the hypothalamic-pituitary-testicular axis. Curr Pharm Des. 2001;7(4):261–73.PubMedCrossRef Hackney AC. Endurance exercise training and reproductive endocrine dysfunction in men: alterations in the hypothalamic-pituitary-testicular axis. Curr Pharm Des. 2001;7(4):261–73.PubMedCrossRef
65.
go back to reference Hackney AC, Szczepanowska E, Viru AM. Basal testicular testosterone production in endurance-trained men is suppressed. Eur J Appl Physiol. 2003;89(2):198–201.PubMedCrossRef Hackney AC, Szczepanowska E, Viru AM. Basal testicular testosterone production in endurance-trained men is suppressed. Eur J Appl Physiol. 2003;89(2):198–201.PubMedCrossRef
66.
go back to reference Vaamonde D, Da Silva ME, Poblador MS, Lancho JL. Reproductive profile of physically active men after exhaustive endurance exercise. Int J Sports Med. 2006;27(9):680–9.PubMedCrossRef Vaamonde D, Da Silva ME, Poblador MS, Lancho JL. Reproductive profile of physically active men after exhaustive endurance exercise. Int J Sports Med. 2006;27(9):680–9.PubMedCrossRef
67.
go back to reference Loucks AB, Thuma JR. Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. J Clin Endocrinol Metab. 2003;88(1):297–311.PubMedCrossRef Loucks AB, Thuma JR. Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. J Clin Endocrinol Metab. 2003;88(1):297–311.PubMedCrossRef
68.
go back to reference Hilton LK, Loucks AB. Low energy availability, not exercise stress, suppresses the diurnal rhythm of leptin in healthy young women. Am J Physiol Endocrinol Metab. 2000;278(1):E43–9.PubMed Hilton LK, Loucks AB. Low energy availability, not exercise stress, suppresses the diurnal rhythm of leptin in healthy young women. Am J Physiol Endocrinol Metab. 2000;278(1):E43–9.PubMed
69.
go back to reference Chan JL, Heist K, DePaoli AM, Veldhuis JD, Mantzoros CS. The role of falling leptin levels in the neuroendocrine and metabolic adaptation to short-term starvation in healthy men. J Clin Invest. 2003;111(9):1409–21.PubMedCentralPubMedCrossRef Chan JL, Heist K, DePaoli AM, Veldhuis JD, Mantzoros CS. The role of falling leptin levels in the neuroendocrine and metabolic adaptation to short-term starvation in healthy men. J Clin Invest. 2003;111(9):1409–21.PubMedCentralPubMedCrossRef
70.
go back to reference Chan JL, Mantzoros CS. Role of leptin in energy-deprivation states: normal human physiology and clinical implications for hypothalamic amenorrhoea and anorexia nervosa. Lancet. 2005;366(9479):74–85.PubMedCrossRef Chan JL, Mantzoros CS. Role of leptin in energy-deprivation states: normal human physiology and clinical implications for hypothalamic amenorrhoea and anorexia nervosa. Lancet. 2005;366(9479):74–85.PubMedCrossRef
71.
go back to reference Papageorgiou M, Elliott-Sale KJ, Greeves JP, Fraser WD, Sale C. The effects of short-term low energy availability on bone turnover in men. Med Sci Sports Exerc. 2015;46(5 Supplement):S329. Papageorgiou M, Elliott-Sale KJ, Greeves JP, Fraser WD, Sale C. The effects of short-term low energy availability on bone turnover in men. Med Sci Sports Exerc. 2015;46(5 Supplement):S329.
72.
go back to reference Dias Quiterio AL, Carnero EA, Baptista FM, Sardinha LB. Skeletal mass in adolescent male athletes and nonathletes: relationships with high-impact sports. J Strength Cond Res. 2011;25(12):3439–47.PubMedCrossRef Dias Quiterio AL, Carnero EA, Baptista FM, Sardinha LB. Skeletal mass in adolescent male athletes and nonathletes: relationships with high-impact sports. J Strength Cond Res. 2011;25(12):3439–47.PubMedCrossRef
73.
go back to reference Tenforde AS, Fredericson M. Influence of sports participation on bone health in the young athlete: a review of the literature. PM R. 2011;3(9):861–7.PubMedCrossRef Tenforde AS, Fredericson M. Influence of sports participation on bone health in the young athlete: a review of the literature. PM R. 2011;3(9):861–7.PubMedCrossRef
74.
go back to reference Fredericson M, Chew K, Ngo J, Cleek T, Kiratli J, Cobb K. Regional bone mineral density in male athletes: a comparison of soccer players, runners and controls. Br J Sports Med. 2007;41(10):664–8 (discussion 8). Fredericson M, Chew K, Ngo J, Cleek T, Kiratli J, Cobb K. Regional bone mineral density in male athletes: a comparison of soccer players, runners and controls. Br J Sports Med. 2007;41(10):664–8 (discussion 8).
75.
go back to reference Bilanin JE, Blanchard MS, Russek-Cohen E. Lower vertebral bone density in male long distance runners. Med Sci Sports Exerc. 1989;21(1):66–70.PubMedCrossRef Bilanin JE, Blanchard MS, Russek-Cohen E. Lower vertebral bone density in male long distance runners. Med Sci Sports Exerc. 1989;21(1):66–70.PubMedCrossRef
76.
go back to reference Hind K, Truscott JG, Evans JA. Low lumbar spine bone mineral density in both male and female endurance runners. Bone. 2006;39(4):880–5.PubMedCrossRef Hind K, Truscott JG, Evans JA. Low lumbar spine bone mineral density in both male and female endurance runners. Bone. 2006;39(4):880–5.PubMedCrossRef
77.
go back to reference Lewiecki EM, Gordon CM, Baim S, Leonard MB, Bishop NJ, Bianchi ML, et al. International society for clinical densitometry 2007 adult and pediatric official positions. Bone. 2008;43(6):1115–21.PubMedCrossRef Lewiecki EM, Gordon CM, Baim S, Leonard MB, Bishop NJ, Bianchi ML, et al. International society for clinical densitometry 2007 adult and pediatric official positions. Bone. 2008;43(6):1115–21.PubMedCrossRef
78.
go back to reference Wolf JH. Julis Wolff and his “law of bone remodeling”. Orthopade. 1995;24(5):378–86.PubMed Wolf JH. Julis Wolff and his “law of bone remodeling”. Orthopade. 1995;24(5):378–86.PubMed
79.
go back to reference Andreoli A, Monteleone M, Van Loan M, Promenzio L, Tarantino U, De Lorenzo A. Effects of different sports on bone density and muscle mass in highly trained athletes. Med Sci Sports Exerc. 2001;33(4):507–11.PubMedCrossRef Andreoli A, Monteleone M, Van Loan M, Promenzio L, Tarantino U, De Lorenzo A. Effects of different sports on bone density and muscle mass in highly trained athletes. Med Sci Sports Exerc. 2001;33(4):507–11.PubMedCrossRef
80.
go back to reference Morel J, Combe B, Francisco J, Bernard J. Bone mineral density of 704 amateur sportsmen involved in different physical activities. Osteoporos Int. 2001;12(2):152–7.PubMedCrossRef Morel J, Combe B, Francisco J, Bernard J. Bone mineral density of 704 amateur sportsmen involved in different physical activities. Osteoporos Int. 2001;12(2):152–7.PubMedCrossRef
81.
go back to reference Heaney RP, Abrams S, Dawson-Hughes B, Looker A, Marcus R, Matkovic V, et al. Peak bone mass. Osteoporos Int. 2000;11(12):985–1009.PubMedCrossRef Heaney RP, Abrams S, Dawson-Hughes B, Looker A, Marcus R, Matkovic V, et al. Peak bone mass. Osteoporos Int. 2000;11(12):985–1009.PubMedCrossRef
82.
go back to reference Tenforde AS, Sayres LC, McCurdy ML, Sainani KL, Fredericson M. Identifying sex-specific risk factors for stress fractures in adolescent runners. Med Sci Sports Exerc. 2013;45(10):1843–51.PubMedCrossRef Tenforde AS, Sayres LC, McCurdy ML, Sainani KL, Fredericson M. Identifying sex-specific risk factors for stress fractures in adolescent runners. Med Sci Sports Exerc. 2013;45(10):1843–51.PubMedCrossRef
83.
go back to reference Milgrom C, Simkin A, Eldad A, Nyska M, Finestone A. Using bone’s adaptation ability to lower the incidence of stress fractures. Am J Sports Med. 2000;28(2):245–51.PubMed Milgrom C, Simkin A, Eldad A, Nyska M, Finestone A. Using bone’s adaptation ability to lower the incidence of stress fractures. Am J Sports Med. 2000;28(2):245–51.PubMed
84.
go back to reference Chen YT, Tenforde AS, Fredericson M. Update on stress fractures in female athletes: epidemiology, treatment, and prevention. Curr Rev Musculoskel Med. 2013;6(2):173–81.CrossRef Chen YT, Tenforde AS, Fredericson M. Update on stress fractures in female athletes: epidemiology, treatment, and prevention. Curr Rev Musculoskel Med. 2013;6(2):173–81.CrossRef
85.
go back to reference Dolan E, Crabtree N, McGoldrick A, Ashley DT, McCaffrey N, Warrington GD. Weight regulation and bone mass: a comparison between professional jockeys, elite amateur boxers, and age, gender and BMI matched controls. J Bone Miner Metab. 2012;30(2):164–70.PubMedCrossRef Dolan E, Crabtree N, McGoldrick A, Ashley DT, McCaffrey N, Warrington GD. Weight regulation and bone mass: a comparison between professional jockeys, elite amateur boxers, and age, gender and BMI matched controls. J Bone Miner Metab. 2012;30(2):164–70.PubMedCrossRef
86.
go back to reference Tenforde AS, Sainani KL, Sayres LC, Cutti P, Fredericson M. Identifying sex-specific risk factors for low bone mineral density in adolescent runners. Am J Sports Med. 2015;43(6):1494–504.PubMedCrossRef Tenforde AS, Sainani KL, Sayres LC, Cutti P, Fredericson M. Identifying sex-specific risk factors for low bone mineral density in adolescent runners. Am J Sports Med. 2015;43(6):1494–504.PubMedCrossRef
87.
go back to reference Kussman A, Fredericson M, Kraus E, Kim B, Tenforde A, Nattiv A. Risk factors for bone stress injuries in NCAA division I collegiate distance runners: a 3 year retrospective study. Clin J Sport Med. 2015;25(2):195. Kussman A, Fredericson M, Kraus E, Kim B, Tenforde A, Nattiv A. Risk factors for bone stress injuries in NCAA division I collegiate distance runners: a 3 year retrospective study. Clin J Sport Med. 2015;25(2):195.
88.
go back to reference Hetland ML, Haarbo J, Christiansen C. Low bone mass and high bone turnover in male long distance runners. J Clin Endocrinol Metab. 1993;77(3):770–5.PubMed Hetland ML, Haarbo J, Christiansen C. Low bone mass and high bone turnover in male long distance runners. J Clin Endocrinol Metab. 1993;77(3):770–5.PubMed
89.
go back to reference Smathers AM, Bemben MG, Bemben DA. Bone density comparisons in male competitive road cyclists and untrained controls. Med Sci Sports Exerc. 2009;41(2):290–6.PubMedCrossRef Smathers AM, Bemben MG, Bemben DA. Bone density comparisons in male competitive road cyclists and untrained controls. Med Sci Sports Exerc. 2009;41(2):290–6.PubMedCrossRef
90.
go back to reference Nichols JF, Rauh MJ. Longitudinal changes in bone mineral density in male master cyclists and nonathletes. J Strength Cond Res. 2011;25(3):727–34.PubMedCrossRef Nichols JF, Rauh MJ. Longitudinal changes in bone mineral density in male master cyclists and nonathletes. J Strength Cond Res. 2011;25(3):727–34.PubMedCrossRef
91.
go back to reference Stewart AD, Hannan J. Total and regional bone density in male runners, cyclists, and controls. Med Sci Sports Exerc. 2000;32(8):1373–7.PubMedCrossRef Stewart AD, Hannan J. Total and regional bone density in male runners, cyclists, and controls. Med Sci Sports Exerc. 2000;32(8):1373–7.PubMedCrossRef
92.
go back to reference Nattiv A, Kennedy G, Barrack MT, Abdelkerim A, Goolsby MA, Arends JC, et al. Correlation of MRI grading of bone stress injuries with clinical risk factors and return to play: a 5-year prospective study in collegiate track and field athletes. Am J Sports Med. 2013;41(8):1930–41.PubMedCentralPubMedCrossRef Nattiv A, Kennedy G, Barrack MT, Abdelkerim A, Goolsby MA, Arends JC, et al. Correlation of MRI grading of bone stress injuries with clinical risk factors and return to play: a 5-year prospective study in collegiate track and field athletes. Am J Sports Med. 2013;41(8):1930–41.PubMedCentralPubMedCrossRef
93.
go back to reference Ackerman KE, Skrinar GS, Medvedova E, Misra M, Miller KK. Estradiol levels predict bone mineral density in male collegiate athletes: a pilot study. Clin Endocrinol. 2012;76(3):339–45.CrossRef Ackerman KE, Skrinar GS, Medvedova E, Misra M, Miller KK. Estradiol levels predict bone mineral density in male collegiate athletes: a pilot study. Clin Endocrinol. 2012;76(3):339–45.CrossRef
94.
go back to reference Brahm H, Strom H, Piehl-Aulin K, Mallmin H, Ljunghall S. Bone metabolism in endurance trained athletes: a comparison to population-based controls based on DXA, SXA, quantitative ultrasound, and biochemical markers. Calcif Tissue Int. 1997;61(6):448–54.PubMedCrossRef Brahm H, Strom H, Piehl-Aulin K, Mallmin H, Ljunghall S. Bone metabolism in endurance trained athletes: a comparison to population-based controls based on DXA, SXA, quantitative ultrasound, and biochemical markers. Calcif Tissue Int. 1997;61(6):448–54.PubMedCrossRef
95.
go back to reference Zanker CL, Swaine IL. Responses of bone turnover markers to repeated endurance running in humans under conditions of energy balance or energy restriction. Eur J Appl Physiol. 2000;83(4–5):434–40.PubMedCrossRef Zanker CL, Swaine IL. Responses of bone turnover markers to repeated endurance running in humans under conditions of energy balance or energy restriction. Eur J Appl Physiol. 2000;83(4–5):434–40.PubMedCrossRef
96.
go back to reference Misra M, Katzman DK, Cord J, Manning SJ, Mendes N, Herzog DB, et al. Bone metabolism in adolescent boys with anorexia nervosa. J Clin Endocrinol Metab. 2008;93(8):3029–36.PubMedCentralPubMedCrossRef Misra M, Katzman DK, Cord J, Manning SJ, Mendes N, Herzog DB, et al. Bone metabolism in adolescent boys with anorexia nervosa. J Clin Endocrinol Metab. 2008;93(8):3029–36.PubMedCentralPubMedCrossRef
97.
go back to reference MacDougall JD, Webber CE, Martin J, Ormerod S, Chesley A, Younglai EV, et al. Relationship among running mileage, bone density, and serum testosterone in male runners. J Appl Physiol. 1992;73(3):1165–70.PubMed MacDougall JD, Webber CE, Martin J, Ormerod S, Chesley A, Younglai EV, et al. Relationship among running mileage, bone density, and serum testosterone in male runners. J Appl Physiol. 1992;73(3):1165–70.PubMed
98.
go back to reference Tremblay MS, Copeland JL, Van Helder W. Effect of training status and exercise mode on endogenous steroid hormones in men. J Appl Physiol. 2004;96(2):531–9.PubMedCrossRef Tremblay MS, Copeland JL, Van Helder W. Effect of training status and exercise mode on endogenous steroid hormones in men. J Appl Physiol. 2004;96(2):531–9.PubMedCrossRef
99.
go back to reference Tsolakis C, Xekouki P, Kaloupsis S, Karas D, Messinis D, Vagenas G, et al. The influence of exercise on growth hormone and testosterone in prepubertal and early-pubertal boys. Hormones. 2003;2(2):103–12.PubMedCrossRef Tsolakis C, Xekouki P, Kaloupsis S, Karas D, Messinis D, Vagenas G, et al. The influence of exercise on growth hormone and testosterone in prepubertal and early-pubertal boys. Hormones. 2003;2(2):103–12.PubMedCrossRef
100.
go back to reference Mountjoy M, Sundgot-Borgen J, Burke L, Carter S, Constantini N, Lebrun C, et al. The IOC consensus statement: beyond the Female Athlete Triad-Relative Energy Deficiency in Sport (RED-S). Br J Sports Med. 2014;48(7):491–7.PubMedCrossRef Mountjoy M, Sundgot-Borgen J, Burke L, Carter S, Constantini N, Lebrun C, et al. The IOC consensus statement: beyond the Female Athlete Triad-Relative Energy Deficiency in Sport (RED-S). Br J Sports Med. 2014;48(7):491–7.PubMedCrossRef
101.
go back to reference De Souza MJ, Williams NI, Nattiv A, Joy E, Misra M, Loucks AB, et al. Misunderstanding the female athlete triad: refuting the IOC consensus statement on Relative Energy Deficiency in Sport (RED-S). Br J Sports Med. 2014;48(20):1461–5.PubMedCrossRef De Souza MJ, Williams NI, Nattiv A, Joy E, Misra M, Loucks AB, et al. Misunderstanding the female athlete triad: refuting the IOC consensus statement on Relative Energy Deficiency in Sport (RED-S). Br J Sports Med. 2014;48(20):1461–5.PubMedCrossRef
102.
go back to reference Di Luigi L, Romanelli F, Sgro P, Lenzi A. Andrological aspects of physical exercise and sport medicine. Endocrine. 2012;42(2):278–84.PubMedCrossRef Di Luigi L, Romanelli F, Sgro P, Lenzi A. Andrological aspects of physical exercise and sport medicine. Endocrine. 2012;42(2):278–84.PubMedCrossRef
104.
go back to reference Muller W, Groschl W, Muller R, Sudi K. Underweight in ski jumping: the solution of the problem. Int J Sports Med. 2006;27(11):926–34.PubMedCrossRef Muller W, Groschl W, Muller R, Sudi K. Underweight in ski jumping: the solution of the problem. Int J Sports Med. 2006;27(11):926–34.PubMedCrossRef
105.
go back to reference Vanheest JL, Rodgers CD, Mahoney CE, De Souza MJ. Ovarian suppression impairs sport performance in junior elite female swimmers. Med Sci Sports Exerc. 2014;46(1):156–66.PubMedCrossRef Vanheest JL, Rodgers CD, Mahoney CE, De Souza MJ. Ovarian suppression impairs sport performance in junior elite female swimmers. Med Sci Sports Exerc. 2014;46(1):156–66.PubMedCrossRef
106.
go back to reference Ratamess NA, Hoffman JR, Kraemer WJ, Ross RE, Tranchina CP, Rashti SL, 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;113(5):1157–68.PubMedCrossRef Ratamess NA, Hoffman JR, Kraemer WJ, Ross RE, Tranchina CP, Rashti SL, 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;113(5):1157–68.PubMedCrossRef
107.
go back to reference Roemmich JN, Sinning WE. Weight loss and wrestling training: effects on nutrition, growth, maturation, body composition, and strength. J Appl Physiol. 1997;82(6):1751–9.PubMed Roemmich JN, Sinning WE. Weight loss and wrestling training: effects on nutrition, growth, maturation, body composition, and strength. J Appl Physiol. 1997;82(6):1751–9.PubMed
Metadata
Title
Parallels with the Female Athlete Triad in Male Athletes
Authors
Adam S. Tenforde
Michelle T. Barrack
Aurelia Nattiv
Michael Fredericson
Publication date
01-02-2016
Publisher
Springer International Publishing
Published in
Sports Medicine / Issue 2/2016
Print ISSN: 0112-1642
Electronic ISSN: 1179-2035
DOI
https://doi.org/10.1007/s40279-015-0411-y

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