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Energy deficiency, menstrual disorders, and low bone mineral density in female athletes: a systematic review

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Abstract

Purpose

Low energy availability (LEA) may lead to menstrual disorders and low bone mineral density, predisposing to the female athlete triad. The primary aim of the present review was to systematically investigate the impact of chronic strenuous exercise on the energy status of professional female athletes compared to sedentary, recreationally active controls as concerns their menstrual status and bone mineral density (BMD). A secondary aim was evaluation of the combined prevalence of the components of the female athlete triad in athletes as compared to non-athletes.

Methods

A systematic review was conducted from 2007 to February 2018. The inclusion and exclusion criteria of the studies were established in advance of the literature search according to the clinical inquiry and the study design.

Results

Four studies were included in this systematic review. The female athlete triad was more prevalent in professional athletes compared to non-athletes. The same results were obtained for both LEA and menstrual disorders. However, BMD and Z-scores showed high heterogeneity among the studies.

Conclusion

Both female athletes and non-athletes are prone to LEA and subsequent menstrual disorders and low BMD or osteoporosis. Future studies are needed to examine energy availability in elite female athletes as well as in non-athletes.

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References

  1. Otis CL, Drinkwater B, Johnson M, Loucks A, Wilmore J (1997) American College of Sports Medicine position stand. The female athlete triad. Med Sci Sports Exerc 29(5):i–ix

    Article  CAS  Google Scholar 

  2. Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP, College American, of Sports M, (2007) American College of Sports Medicine position stand. The female athlete triad. Med Sci Sports Exerc 39(10):1867–1882. https://doi.org/10.1249/mss.0b013e318149f111

    Article  PubMed  Google Scholar 

  3. De Souza MJ, Nattiv A, Joy E, Misra M, Williams NI, Mallinson RJ, Gibbs JC, Olmsted M, Goolsby M, Matheson G, Female Athlete Triad C, American College of Sports M, American Medical Society for Sports M, American Bone Health A (2014) 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 24(2):96–119. https://doi.org/10.1097/JSM.0000000000000085

    Article  Google Scholar 

  4. Mountjoy M, Sundgot-Borgen J, Burke L, Carter S, Constantini N, Lebrun C, Meyer N, Sherman R, Steffen K, Budgett R, Ljungqvist A (2014) The IOC consensus statement: Beyond the Female Athlete Triad-Relative Energy Deficiency in Sport (RED-S). Br J Sports Med 48(7):491–497. https://doi.org/10.1136/bjsports-2014-093502

    Article  PubMed  Google Scholar 

  5. Loucks AB, Thuma JR (2003) Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. J Clin Endocrinol Metab 88(1):297–311. https://doi.org/10.1210/jc.2002-020369

    Article  CAS  PubMed  Google Scholar 

  6. Loucks AB, Verdun M, Heath EM (1998) Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. J ApplPhysiol (1985) 84(1):37–46. https://doi.org/10.1152/jappl.1998.84.1.37

    Article  CAS  Google Scholar 

  7. Mulligan K, Butterfield GE (1990) Discrepancies between energy intake and expenditure in physically active women. Br J Nutr 64(1):23–36

    Article  CAS  Google Scholar 

  8. Ihle R, Loucks AB (2004) Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res 19(8):1231–1240. https://doi.org/10.1359/JBMR.040410

    Article  PubMed  Google Scholar 

  9. Loucks AB (2007) Energy availability and infertility. Curr Opin Endocrinol Diabetes Obes 14(6):470–474. https://doi.org/10.1097/MED.0b013e3282f1cb6a

    Article  PubMed  Google Scholar 

  10. Hoek HW (2013) Classification, epidemiology and treatment of DSM-5 feeding and eating disorders. Curr Opin Psychiatry 26(6):529–531. https://doi.org/10.1097/YCO.0b013e328365b656

    Article  PubMed  Google Scholar 

  11. Kroshus E, Austin SB (2015) Definition and epidemiology of the female athlete triad. In: The female athlete triad. Springer, pp 1–12

  12. Loucks AB (2004) Energy balance and body composition in sports and exercise. J Sports Sci 22(1):1–14. https://doi.org/10.1080/0264041031000140518

    Article  PubMed  Google Scholar 

  13. Loucks AB, Kiens B, Wright HH (2011) Energy availability in athletes. J Sports Sci 29(Suppl 1):S7-15. https://doi.org/10.1080/02640414.2011.588958

    Article  PubMed  Google Scholar 

  14. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB (2000) Meta-analysis of observational studies in epidemiology: A proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283(15):2008–2012

    Article  CAS  Google Scholar 

  15. Wells GJhw, ohri. ca/programs/clinical_epidemiology. oxford. htm (2004) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analysis

  16. Coelho GM, de Farias ML, de Mendonca LM, de Mello DB, Lanzillotti HS, Ribeiro BG, Soares Ede A (2013) The prevalence of disordered eating and possible health consequences in adolescent female tennis players from Rio de Janeiro, Brazil. Appetite 64:39–47. https://doi.org/10.1016/j.appet.2013.01.001

    Article  PubMed  Google Scholar 

  17. Doyle-Lucas AF, Akers JD, Davy BM (2010) Energetic efficiency, menstrual irregularity, and bone mineral density in elite professional female ballet dancers. J Dance Med Sci 14(4):146–154

    PubMed  Google Scholar 

  18. Hoch AZ, Pajewski NM, Moraski L, Carrera GF, Wilson CR, Hoffmann RG, Schimke JE, Gutterman DD (2009) Prevalence of the female athlete triad in high school athletes and sedentary students. Clin J Sport Med 19(5):421–428. https://doi.org/10.1097/JSM.0b013e3181b8c136

    Article  PubMed  PubMed Central  Google Scholar 

  19. Muia EN, Wright HH, Onywera VO, Kuria EN (2016) Adolescent elite Kenyan runners are at risk for energy deficiency, menstrual dysfunction and disordered eating. J Sports Sci 34(7):598–606. https://doi.org/10.1080/02640414.2015.1065340

    Article  PubMed  Google Scholar 

  20. Manore MM, Kam LC, Loucks AB, International Association of Athletics F (2007) The female athlete triad: Components, nutrition issues, and health consequences. J Sports Sci 25(Suppl 1):S61-71. https://doi.org/10.1080/02640410701607320

    Article  PubMed  Google Scholar 

  21. Lewiecki EM, Gordon CM, Baim S, Binkley N, Bilezikian JP, Kendler DL, Hans DB, Silverman S, Bishop NJ, Leonard MB, Bianchi ML, Kalkwarf HJ, Langman CB, Plotkin H, Rauch F, Zemel BS (2008) Special report on the 2007 adult and pediatric Position Development Conferences of the International Society for Clinical Densitometry. Osteoporos Int 19(10):1369–1378. https://doi.org/10.1007/s00198-008-0689-9

    Article  CAS  PubMed  Google Scholar 

  22. O’Donnell E, De Souza MJ (2004) The cardiovascular effects of chronic hypoestrogenism in amenorrhoeic athletes: A critical review. Sports Med 34(9):601–627

    Article  Google Scholar 

  23. Torstveit MK, Sundgot-Borgen J (2005) The female athlete triad exists in both elite athletes and controls. Med Sci Sports Exerc 37(9):1449–1459

    Article  Google Scholar 

  24. Nichols JF, Rauh MJ, Lawson MJ, Ji M, Barkai HS (2006) Prevalence of the female athlete triad syndrome among high school athletes. Arch Pediatr Adolesc Med 160(2):137–142. https://doi.org/10.1001/archpedi.160.2.137

    Article  PubMed  Google Scholar 

  25. Beals KA, Hill AK (2006) The prevalence of disordered eating, menstrual dysfunction, and low bone mineral density among US collegiate athletes. Int J Sport Nutr Exerc Metab 16(1):1–23

    Article  Google Scholar 

  26. Cobb KL, Bachrach LK, Greendale G, Marcus R, Neer RM, Nieves J, Sowers MF, Brown BW Jr, Gopalakrishnan G, Luetters C, Tanner HK, Ward B, Kelsey JL (2003) Disordered eating, menstrual irregularity, and bone mineral density in female runners. Med Sci Sports Exerc 35(5):711–719. https://doi.org/10.1249/01.MSS.0000064935.68277.E7

    Article  PubMed  Google Scholar 

  27. Drinkwater BL, Nilson K, Chesnut CH 3rd, Bremner WJ, Shainholtz S, Southworth MB (1984) Bone mineral content of amenorrheic and eumenorrheic athletes. N Engl J Med 311(5):277–281. https://doi.org/10.1056/NEJM198408023110501

    Article  CAS  PubMed  Google Scholar 

  28. Marcus R, Cann C, Madvig P, Minkoff J, Goddard M, Bayer M, Martin M, Gaudiani L, Haskell W, Genant H (1985) Menstrual function and bone mass in elite women distance runners. Endocrine and metabolic features. Ann Intern Med 102(2):158–163

    Article  CAS  Google Scholar 

  29. Biewener AA, Bertram JE (1993) Skeletal strain patterns in relation to exercise training during growth. J Exp Biol 185:51–69

    Article  CAS  Google Scholar 

  30. Drinkwater BL (1994) 1994 C. H. McCloy Research Lecture: Does physical activity play a role in preventing osteoporosis? Res Q Exerc Sport 65(3):197–206. https://doi.org/10.1080/02701367.1994.10607620

    Article  CAS  PubMed  Google Scholar 

  31. Heaney RP (1996) Pathophysiology of osteoporosis. Am J Med Sci 312(6):251–256

    Article  CAS  Google Scholar 

  32. Bennell KL, Malcolm SA, Wark JD, Brukner PD (1997) Skeletal effects of menstrual disturbances in athletes. Scand J Med Sci Sports 7(5):261–273

    Article  CAS  Google Scholar 

  33. Nichols DL, Bonnick SL, Sanborn CF (2000) Bone health and osteoporosis. Clin Sports Med 19(2):233–249

    Article  CAS  Google Scholar 

  34. Bass SL, Saxon L, Daly RM, Turner CH, Robling AG, Seeman E, Stuckey S (2002) The effect of mechanical loading on the size and shape of bone in pre-, peri-, and postpubertal girls: A study in tennis players. J Bone Miner Res 17(12):2274–2280. https://doi.org/10.1359/jbmr.2002.17.12.2274

    Article  CAS  PubMed  Google Scholar 

  35. Calbet JA, Moysi JS, Dorado C, Rodriguez LP (1998) Bone mineral content and density in professional tennis players. Calcif Tissue Int 62(6):491–496

    Article  CAS  Google Scholar 

  36. Myburgh KH, Bachrach LK, Lewis B, Kent K, Marcus R (1993) Low bone mineral density at axial and appendicular sites in amenorrheic athletes. Med Sci Sports Exerc 25(11):1197–1202

    Article  CAS  Google Scholar 

  37. Ballard TL, Clapper JA, Specker BL, Binkley TL, Vukovich MD (2005) Effect of protein supplementation during a 6-mo strength and conditioning program on insulin-like growth factor I and markers of bone turnover in young adults. Am J Clin Nutr 81(6):1442–1448. https://doi.org/10.1093/ajcn/81.6.1442

    Article  CAS  PubMed  Google Scholar 

  38. Lombardi G, Ziemann E, Banfi G (2019) Physical activity and bone health: What is the role of immune system? A narrative review of the third way. Front Endocrinol (Lausanne) 7(10):60. https://doi.org/10.3389/fendo.2019.00060

    Article  Google Scholar 

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Skarakis, N.S., Mastorakos, G., Georgopoulos, N. et al. Energy deficiency, menstrual disorders, and low bone mineral density in female athletes: a systematic review. Hormones 20, 439–448 (2021). https://doi.org/10.1007/s42000-021-00288-0

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