Female athletes and health

Open access

Summary

It is well documented that regular physical activity has a beneficial effect on human health by affecting the metabolic processes that are of fundamental importance in the body’s functions, such as insulin sensitivity and glucose disposal, as well as lipid and lipoprotein turnover. On the other hand, there is a wealth of studies which indicate that strenuous, regular physical activity, such as that performed by high performance athletes, may be detrimental for the athletes’ health especially in women. This review focuses on the factors that contribute to health problems in female athletes, named the female athlete triad, which includes excessive dieting, menstrual dysfunctions (anovulatory menstrual cycles, oligomenorrhea, amenorrhea) and a low bone mineral density (BMD). As a result of these factors, women who participate in sports, especially those focused on leanness, need special attention and education from health professionals, coaches and the athletes themselves to prevent the detrimental effects of an inadequate energy supply against high energy demands.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • 1. Alaunyte I. V. Stojceska A.S. Plunkett (2015) Iron and female athlete: a review of dietary treatment methods for improving iron status and exercise performance. J. Int. Soc. Sports Nutr. 12: 38. DOI: 10.1186/s1270-015-0099-2.

  • 2. Arends J.C. M.Y. Cheung M.T. Barrack A. Nattiv (2012) Restoration of menses with non-pharmacologic therapy in college athletes with menstrual disturbances: a 5-year retrospective study. Int. J. Sport Nutr. Exerc. Metab. 22: 98-108.

  • 3. Beitins I.Z. J.W McArthur. B.A. Turnbull G.S. Skrinar B.A. Bullen (1991) Exercise induces two types of human luteal dysfunction: confirmation by urinary free progesterone. J. Clin. Endocrinol. Metab. 72: 1350-1358.

  • 4. Broocks A. K.M. Pirke U. Schweiger R.J. Tuschl R.G. Laesser T. Strowitzki (1990) Cyclic ovarian function in recreational athletes. J. Appl. Physiol. 68: 2083-2086.

  • 5. Brunet M. (2005) Female athlete triad. Clin. Sports 24: 623-636. DOI: 10.1016/j.csm.2005.03.009.

  • 6. Bullen B.A. G.S. Skrinar I.Z. Beitins B. Van Mehring A. Turnbull J.W. McArthur (1985) Induction of menstrual disorders by strenuous exercise in untrained women. N. Eng. J Med. 312: 1349-1353.

  • 7. Ciadell-Kam L. C.P. Guebels G.F. Maddalozzo M.M. Manore (2014) Dietary intervention restored menses in female athletes with exercise – associated menstrual dysfunction with limited impact on bone and muscle health. Nutrients 6: 3018-3039. DOI: 10.3390/nu6083018.

  • 8. Cioni G. A. Berni G.F. Gensini R. Abbate M. Boddi (2015) Impaired femoral vascular compliance and endothelial dysfunction in 30 healthy male soccer players: competitive sports and local detrimental effects. Sport Health 7: 335-340. DOI: 10.1177/19417381115577931.

  • 9. Cobb K.L. L.K. Bachrach G. Greendale R. Marcus R.M. Neer J. Nieves (2003) Disordered eating menstrual irregularity and bone mineral density in female runners. Med. Sci. Sports Exerc. 35: 711-719.

  • 10. De Souza M.J. R. Hontscharuk M. Olmsted G. Kerr N.I. Williams (2007) Drive for thinness score is a proxy indicator of energy deficiency in exercising women. Appetite 48: 359-367.

  • 11. De Souza M.J. D.K. Lee J.L. Van Heest J.L. Scheid S.L. West N.I. Williams (2007) Severity of energy related menstrual disturbances increases in proportion to indices of energy conservation in exercising women. Fertil. Steril. 88: 971-975.

  • 12. De Souza M.J. B.E. Miller A.B. Loucks A.A. Luciano L.S. Pescatello C.G. Campbell (1998) High frequency of luteal phase deficiency and anovulation in recreational women runners: blunted elevation in follicle-stimulating hormone observed during luteal-follicular transition. J. Clin. Endocrinol. Metab. 83: 4220-4232.

  • 13. De Souza M.J. J. Van Heest L.M. Demers B.L. Lasley (2003) Luteal phase deficiency in recreational runners: evidence for hypometabolic state. J. Clin. Endocrinol. Metab. 88: 337-346.

  • 14. Ellison P.T. C. Lager (1986) Moderate recreational running is associated with lowered progesterone profiles in women. Am. J. Obstet. Gynecol. 154: 1000-1003.

  • 15. Felder J.M. L.M. Burke B.J. Lowdon D. Cameron-Smith G.R. Collier (1998) Nutritional practices of elite female surfers during training and competition. Int. J. Sport. Nutr. Metab. 8: 36-48.

  • 16. Fiuza-Luces C. N. Garatechea N.A. Bergier A. Lucia (2013) Exercie is the real polypill. Physiology 28 330-358. DOI: 10.1152/physiol.00019.2013.

  • 17. Friday K.E. B.L. Drinkwater B. Bruemmer C. Chestnut A. Chait (1993) Elevated plasma low-density and high-density lipoprotein cholesterol levels in amehorrheic athletes: effects of endogenous hormone status and nutrient intake. J. Clin. Endocrinol. Metab. 7: 1605-1609.

  • 18. Frisch R.E. J.W. McArthur (1974) Menstrual cycles: fatness as a determinant of minimum weight for height necessary for their maintenance or onset. Science 185: 949-951.

  • 19. Frisch R.E. G. Wyshak L. Vincent (1989) Delayed menarche and amenorrhea in ballet dancers. N. Eng. J. Med. 303: 17-19.

  • 20. Gleeson M. D.B. Pyne (2016) Respiratory inflammation and infections in high-performance athletes. Immunol. Cell Biol. 94: 124-131. DOI: 10.1038/icb.2015.100.

  • 21. Guebels C.P. L.C. Kam G.F. Maddalozzo M.M. Manore (2014) Active women before/after an intervention designed to restore menstrual function: resting metabolic rat and comparison of four methods to quantify energy expenditure and energy availability. Int. J. Sport. Nutr. Exerc. Metab. 24 37-46. DOI: og/10.1123/ijsnem.2012-0165.

  • 22. Hawley J.A. M. Hargreaves M.J. Joyner J.R. Zierath (2014) Integrative biology of exercise. Cell 159: 738-749. DOI: .org/10.1016/j.cell.2014.10.10.029.

  • 23. Heinonen I. K.K. Kalliokoski J.C. Hanukainen D.J. Duncker P. Nuutila J. Knuuti (2014) Organ-specific physiological responses to acute physical exercise and long-term training in humans. Physiology 29: 421-436. DOI:10.1152/physiol.00067.2013.

  • 24. Joy E. A. Kussman A. Nattiv (2016) update on eating disorders in athletes: a comprehensive narrative review with a focus on clinical assessment and management. Br. J. Sports Med. 50: 154-162. DOI: 10.1136/bjsports-2015-095735.

  • 25. Kaiserauer S. A.C. Snyder M. Sleeper J. Zierath (1989) Nutritional physiological and menstrual status of distance runners. Med. Sci Sports Exec. 21: 120-125.

  • 26. Klungland-Torstveit M. J. Sundgot-Borgen (2005) The female athlete triad exists in both elite athletes and controls. Med. Sci. Sports Exerc. 37: 1449-1459.

  • 27. Koehler K. H. Braun S. Achtzen U. Hilderbrandt H.G. Predel J. Mesyer W. Schänzer (2012) Iron status in elite young athletes: gender-dependent influences of diet and exercise. Eur. J. Appl. Physiol. 112: 513-523.

  • 28. Lamon-Fava S. E.C. Fisher M.E. Nelson W.J. Evans J.S. Millar J.M. Ordovas E.J. Schaefer (1989) Effect of exercise and menstrual cycle status on plasma lipids low density lipoprotein particle size and apolipoproteins. J. Clin. Endocrinol. Metab. 68: 17-21.

  • 29. Laughlin G.A. C.E. Dominguez S.S. Yen (1998) Nutritional and endocrine-metabolic aberrations in women with functional hypothalamic amenorrhea. J. Clin. Endocrinol. Metab. 83: 25-32.

  • 30. Lloyd T. J.R. Buchanan S. Bitzer C.J. Waldman C. Myers B.G. Ford (1987) Interrelationships of diet athletic activity menstrual status and bone density in collegiate women. Am. J. Clin. Nutr. 46: 681-684. 31. Loucks A.B. E.M. Heath (1994) Dietary restrictions reduces luteinizing hormone (LH) pulse frequency during waking hours and increases LH pulse amplitude during sleep in young menstruating women. J. Clin. Endocrinol. Metab. 78: 910-915.

  • 32. Loucks A.B. S.M. Horvath (1984) Exercise-induced stress responses of amenorrheic and eumenorrheic runners. J. Clin. Endocrinol. Metab. 59: 1109-1120.

  • 33. Loucks A.B. J.R. Thuma (2003) Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. J. Clin. Endocrinol. Metab. 88: 297-311.

  • 34. Loucks A.B. M. Verdun E.M. Heath (1998) Low energy availability not stress of exercise alters LH pulsatility in exercising women. J. Appl. Physiol. 84: 37-46.

  • 35. Loucks A.B. (1990) Effects of exercise training on the menstrual cycle: existence and mechanisms. Med. Sci. Sports Exerc. 22: 275-280.

  • 36. Łagowska K. K. Kapzuk Z. Friebe J. Bajerska (2014) Effects of dietary intervention in young female athletes with menstrual disorders. J. Int. So. Sport Nutr. 11: 21. http://www.jissn.com.content/11/1/21. 37. Manore M.M. (2002) Dietary recommendations and athletic menstrual dysfunction. Sports Med. 32: 887-901.

  • 38. Marin D.P. A.P. Bolin T.R. Campoio B.A. Guerra R. Otton (2013) Oxidative stress and antioxidant status response of handball athletes: implications for sport training monitoring. Int. Immunopharm. 17: 462-470. DOI: org/j.intimp.2013.07009.

  • 39. Melin A. A.B. Tornberg S. Skouby J. Faber C. Ritz A. Sjödin J. Sundgot-Borgen (2014) The LEAF questionnaire: a screening tool for the identification of female athletes at risk for the female athlete triad. Br. J. Sports Med. 48: 540-545. DOI: 10.1136/bjsports-2013-093240.

  • 40. Melin A. A.B. Tornberg S. Skouby S.S. Möller J. Faber J.J. Sidelmann M. Aziz A. Sjödin (2015) Energy availability and female athlete triad in elite endurance athletes. Scand. J. Med. Sci. Sports 25: 610-622. DOI: 10.1111/sms.12261.

  • 41. Mullinix M.C. S.S. Jonnalagadda C.A. Rosenbloom W.R. Thompson J.R. Kicklighter (2003) Dietary intake of female U.S. soccer players. Nutr. Res. 23: 585-593.

  • 42. Nichols J.F M.J. Rauh M.T. Barrack H.S. Barkai (2007) Bone mineral density in female high school athletes: interactions of menstrual function and type of mechanical loading. Bone 41: 371-377.

  • 43. Nichols J.F. M.J. Rauh M.J. Lawson J. Ming H.S. Barkai (2006) Prevalence of the female athlete triad syndrome among high school athletes. Arch. Pediatr. Adolesc. Med. 160: 137-142.

  • 44. Nova E. A. Montero S. López-Varela A. Marcos (2001) Are elite gymnasts really malnourished? Evaluation of diet anthropometry and immunocompetence. Nutr. Res. 21: 15-29.

  • 45. Peach G. G. Schep R. Palfreemen J.D. Beard M.M. Thompson R.J. Hinchliff (2012) Endofibrosis and kinking of the ilac arterie in athletes: A systemic review. Eur. J. Vasc. Endovasc. Surg. 43: 208-217. DOI: 10.1016/j.ejvs.2011.11.019.

  • 46. Prior J.C. K. Cameron B.H. Yuen J. Thomas (1982) Menstrual cycle changes with marathon training: anovulation and short luteal phase. Can. J. Appl. Sport Sci. 7: 173-177.

  • 47. Reed J.L. J.L. Bowell B.R. Hill B.A. Williams M.J. De Souza N.L. Williams (2011) Exercising women with menstrual disturbances consume low energy dense foods and beverages. Appl. Physiol. Nutr. Metab. 36: 382-394. DOI: 10.11349/H11-030.

  • 48. Reed J.L. M.J. De Souza J.M. Kindler N.I. Williams (2014) Nutritional practices associated with low energy availability in Division I female soccer players. J. Sports Sci. 32: 1499-1509.

  • 49. Resch M. G. Sznedel P. Haasz (2004) Eating disorders from gynecologic and endocrinologic view: hormonal changes Fertil. Steril. 81: 1151-1153.

  • 50. Rickenlund A. M.J. Eriksson K. Schenk-Gustafsson A.L. Hirschberg (2005) Amenorrhea in female athlete is associated with endothelial dysfunction and unfavorable lipid profile. J. Clin. Endocrinol. Metab. 90: 1354-1359.

  • 51. Sanborn C.F. B.H. Albrecht W.W. Wagner (1987) Amenorrhea: lack of associations with body fat. Med. Sci. Sports Exerc. 19: 207-222.

  • 52. Scharhag J. H. Löllgen W. Kinderman (2013) Competitive sports and the heart: benefit or risk? Dtsch. Arztebl. Int. 110: 14-24.

  • 53. Silva M.R. T. Paiva (2015) Low energy availability and low body fat of female gymnasts before an international competition. Eur. J. Sports. Sci. 15: 591 – 599.

  • 54. Solomon C.G. F.B. Hu A. Dunaif J.E. Rich-Edwards M.J. Stampfer W.C. Willet (2002) Menstrual cycle irregularities and risk of future cardiovascular disease. J. Clin. Endocrinol. Metab. 87: 2013-2017.

  • 55. Sudi K. K. Őttl D. Payerl P. Baumgartl K. Tauschmann W. Műller (2004) Anorexia athletica. Nutrition 20: 657-661.

  • 56. Sundgot-Borgen J. M. Klungland-Torsveit (2007) The female football players disordered eating menstrual function and bone health. Br. J. Sports Med. 41: 168-172.

  • 57. Tenforde A.S. M.T. Barrack A. Nattiv M. Fredericson (2016) Parallels with the female athlete triad in male athletes. Sports Med. 46: 171-182. DOI: 10.1007/s40279-015-0411-y.

  • 58. Thein-Nissenbaum J. (2013) Long-term consequences of the female athlete triad. Maturitas 75: 107-112. DOI: org/10.1018/j.maturitas.2013.02.010.

  • 59. To W.W. M.W. Wong I.Y. Lam (2005) Bone mineral density differences between adolescent dancers and non-exercising adolescent females. J. Pediatr. Adolesc. Gynecol. 18: 337-342.

  • 60. Torstveit M.K. J. Sundgot-Borgen (2005) Participation in leanness sports but not training volume is associated with menstrual dysfunction: a national survey of 1276 elite athletes and controls. Br. J. Sports. Med. 39: 141-147.

  • 61. Vanheest J.L. Rodgers C.D. Mahoney C.E. M.J. De Souza (2014) Ovarian suppression impairs sport performance in junior elite female swimmers. Med. Sci. Sports Exerc. 46: 156-166. DOI: 10.129/MSS.0b0143e3182a32672.

  • 62. Williams N.I. H.J. Leidy B.R. Hill J.L. Lieberman R.S. Legro M.J. De Souza (2015) Magnitude of daily energy deficit predicts frequency but not severity of menstrual disturbances associated with exercise and caloric restriction. Am. J. Physiol. Endocrinol. Metab. 308: E29-E39.

  • 63. Williams N.I. D.L. Helmreich D.B. Parfitt A. Casto-Balderrama J.L. Cameron (2001) Evidence of a causal role of low energy availability in the induction of menstrual cycle disturbances during strenuous exercise training. J. Clin. Endocrinol. Metab. 86: 5184-5193.

  • 64. Ziegler P. J.A. Nelson A Fornell-Barratt. L. Fiveash A. Drewnowski (2001) Energy and macronutrient intakes of elite figure skaters. J. Am. Diet. Assoc. 101: 319-325.

Search
Journal information
Impact Factor


CiteScore 2018: 0.38

SCImago Journal Rank (SJR) 2018: 0.144
Source Normalized Impact per Paper (SNIP) 2018: 0.432

Metrics
All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 245 116 3
PDF Downloads 133 76 6