Reviews in Endocrine and Metabolic Disorders

, Volume 9, Issue 2, pp 139–144

Bone density in the adolescent athlete

Article

Abstract

Adolescence is a critical time for bone mass accrual, and increases in bone mass through puberty are dependent on rising levels of gonadal steroids, growth hormone and insulin like growth factor-1. Many high school girls are involved in athletic activities, and as many as 23.5% of adolescent athletes have been reported to develop amenorrhea. This review focuses on (1) factors that determine which athletes are likely to develop amenorrhea, such as a negative energy balance state, low levels of leptin and high levels of ghrelin, and (2) the impact of hypogonadism in athletes on bone metabolism. Beneficial effects of increased mechanical loading from athletic activity do not appear to protect against the deleterious effects of hypogonadism in adolescent athletes.

Keywords

Athletes Adolescents Bone Density Bone Turnover Markers Estradiol IGF-1 Ghrelin Leptin Body Composition 

References

  1. 1.
    Bachrach L. Acquisition of optimal bone mass in childhood and adolescence. Trends Endocrinol Metab. 2001;12(1):22–8.PubMedCrossRefGoogle Scholar
  2. 2.
    Theintz G, Buchs B, Rizzoli R, Slosman D, Clavien H, Sizonenko P, et al. Longitudinal monitoring of bone mass accumulation in healthy adolescents: evidence for a marked reduction after 16 years of age at the levels of lumbar spine and femoral neck in female subjects. J Clin Endocrinol Metab. 1992;75(4):1060–5.PubMedCrossRefGoogle Scholar
  3. 3.
    Ohlsson C, Bengtsson B, Isaksson O, Andreassen T, Slootweg M. Growth hormone and bone. Endocr Rev. 1998;19:55–79.PubMedCrossRefGoogle Scholar
  4. 4.
    Rauch F. Bone accrual in children: adding substance to surfaces. Pediatrics 2007;119(Suppl 2):S137–40.PubMedCrossRefGoogle Scholar
  5. 5.
    Misra M, Aggarwal A, Miller KK, Almazan C, Worley M, Soyka LA, et al. Effects of anorexia nervosa on clinical, hematologic, biochemical, and bone density parameters in community-dwelling adolescent girls. Pediatrics 2004;114(6):1574–83.PubMedCrossRefGoogle Scholar
  6. 6.
    Lehtonen-Veromaa MK, Mottonen TT, Nuotio IO, Irjala KM, Leino AE, Viikari JS. Vitamin D and attainment of peak bone mass among peripubertal Finnish girls: a 3-y prospective study. Am J Clin Nutr. 2002;76(6):1446–53.PubMedGoogle Scholar
  7. 7.
    Chan GM. Dietary calcium and bone mineral status of children and adolescents. Am J Dis Child. 1991;145(6):631–4.PubMedGoogle Scholar
  8. 8.
    Greene DA, Naughton GA, Briody JN, Kemp A, Woodhead H, Corrigan L. Bone strength index in adolescent girls: does physical activity make a difference? Br J Sports Med. 2005;39(9):622–7, discussion 7.PubMedCrossRefGoogle Scholar
  9. 9.
    Barkai HS, Nichols JF, Rauh MJ, Barrack MT, Lawson MJ, Levy SS. Influence of sports participation and menarche on bone mineral density of female high school athletes. J Sci Med Sport. 2007;10(3):170–9.PubMedCrossRefGoogle Scholar
  10. 10.
    Nichols JF, Rauh MJ, Barrack MT, Barkai HS, Pernick Y. Disordered eating and menstrual irregularity in high school athletes in lean-build and nonlean-build sports. Int J Sport Nutr Exerc Metab. 2007;17(4):364–77.PubMedGoogle Scholar
  11. 11.
    Rautava E, Lehtonen-Veromaa M, Kautiainen H, Kajander S, Heinonen OJ, Viikari J, et al. The reduction of physical activity reflects on the bone mass among young females: a follow-up study of 142 adolescent girls. Osteoporos Int. 2007;18(7):915–22.PubMedCrossRefGoogle Scholar
  12. 12.
    Linden C, Ahlborg HG, Besjakov J, Gardsell P, Karlsson MK. A school curriculum-based exercise program increases bone mineral accrual and bone size in prepubertal girls: two-year data from the pediatric osteoporosis prevention (POP) study. J Bone Miner Res. 2006;21(6):829–35.PubMedCrossRefGoogle Scholar
  13. 13.
    Heinonen A, Sievanen H, Kannus P, Oja P, Pasanen M, Vuori I. High-impact exercise and bones of growing girls: a 9-month controlled trial. Osteoporos Int 2000;11(12):1010–7.PubMedCrossRefGoogle Scholar
  14. 14.
    Markou KB, Mylonas P, Theodoropoulou A, Kontogiannis A, Leglise M, Vagenakis AG, et al. The influence of intensive physical exercise on bone acquisition in adolescent elite female and male artistic gymnasts. J Clin Endocrinol Metab. 2004;89(9):4383–7.PubMedCrossRefGoogle Scholar
  15. 15.
    Loucks A, Horvath S. Athletic amenorrhea: a review. Med Sci Sports Exerc. 1985;17(1):56–72.PubMedGoogle Scholar
  16. 16.
    Otis C. Exercise-associated amenorrhea. Clin Sports Med. 1992;11(2):351–62.PubMedGoogle Scholar
  17. 17.
    Shangold M, Rebar R, Wentz A, Schiff I. Evaluation and management of menstrual dysfunction in athletes. JAMA 1990;263(12):1665–9.PubMedCrossRefGoogle Scholar
  18. 18.
    Nichols JF, Rauh MJ, Lawson MJ, Ji M, Barkai HS. Prevalence of the female athlete triad syndrome among high school athletes. Arch Pediatr Adolesc Med. 2006;160(2):137–42.PubMedCrossRefGoogle Scholar
  19. 19.
    De Souza MJ, Van Heest J, Demers LM, Lasley BL. Luteal phase deficiency in recreational runners: evidence for a hypometabolic state. J Clin Endocrinol Metab. 2003;88(1):337–46.PubMedCrossRefGoogle Scholar
  20. 20.
    Loucks AB. The response of luteinizing hormone pulsatility to 5 days of low energy availability disappears by 14 years of gynecological age. J Clin Endocrinol Metab. 2006;91(8):3158–64.PubMedCrossRefGoogle Scholar
  21. 21.
    Dueck CA, Matt KS, Manore MM, Skinner JS. Treatment of athletic amenorrhea with a diet and training intervention program. Int J Sport Nutr. 1996;6(1):24–40.PubMedGoogle Scholar
  22. 22.
    Haines J, Neumark-Sztainer D, Eisenberg ME, Hannan PJ. Weight teasing and disordered eating behaviors in adolescents: longitudinal findings from Project EAT (Eating Among Teens). Pediatrics 2006;117(2):e209–15.PubMedCrossRefGoogle Scholar
  23. 23.
    Christo K, Prabhakaran R, Lamparello B, Cord J, Miller K, Goldstein M, et al. Bone metabolism in adolescent amenorrheic and eumenorrheic athletes and controls. Pediatrics 2008;in press.Google Scholar
  24. 24.
    Welt CK, Chan JL, Bullen J, Murphy R, Smith P, DePaoli AM, et al. Recombinant human leptin in women with hypothalamic amenorrhea. N Engl J Med. 2004;351(10):987–97.PubMedCrossRefGoogle Scholar
  25. 25.
    Kluge M, Schussler P, Uhr M, Yassouridis A, Steiger A. Ghrelin suppresses secretion of luteinizing hormone in humans. J Clin Endocrinol Metab. 2007;92(8):3202–5.PubMedCrossRefGoogle Scholar
  26. 26.
    Vulliemoz NR, Xiao E, Xia-Zhang L, Germond M, Rivier J, Ferin M. Decrease in luteinizing hormone pulse frequency during a five-hour peripheral ghrelin infusion in the ovariectomized rhesus monkey. J Clin Endocrinol Metab. 2004;89(11):5718–23.PubMedCrossRefGoogle Scholar
  27. 27.
    De Souza MJ, Leidy HJ, O’Donnell E, Lasley B, Williams NI. Fasting ghrelin levels in physically active women: relationship with menstrual disturbances and metabolic hormones. J Clin Endocrinol Metab. 2004;89(7):3536–42.PubMedCrossRefGoogle Scholar
  28. 28.
    Christo K, Cord J, Mendes N, Miller KK, Goldstein MA, Klibanski A, Misra M. Acylated ghrelin and leptin in adolescent athletes with amenorrhea, eumenorrheic athletes and controls: a cross sectional study. Clin Endocrinol (Oxf). 2008 (March 10); in press.Google Scholar
  29. 29.
    Raastad T, Bjoro T, Hallen J. Hormonal responses to high- and moderate-intensity strength exercise. Eur J Appl Physiol. 2000;82(1–2):121–8.PubMedCrossRefGoogle Scholar
  30. 30.
    Laughlin G, Yen S. Nutritional and endocrine-metabolic aberrations in amenorrheic athletes. J Clin Endocrinol Metab. 1996;81(12):4301–9.PubMedCrossRefGoogle Scholar
  31. 31.
    Riggs BL, Khosla S, Melton LJ III. Sex steroids and the construction and conservation of the adult skeleton. Endocr Rev. 2002;23(3):279–302.PubMedCrossRefGoogle Scholar
  32. 32.
    Lanyon L, Skerry T. Postmenopausal osteoporosis as a failure of bone’s adaptation to functional loading: a hypothesis. J Bone Miner Res. 2001;16(11):1937–47.PubMedCrossRefGoogle Scholar
  33. 33.
    Lee KC, Lanyon LE. Mechanical loading influences bone mass through estrogen receptor alpha. Exerc Sport Sci Rev. 2004;32(2):64–8.PubMedCrossRefGoogle Scholar
  34. 34.
    von Stengel S, Kemmler W, Kalender WA, Engelke K, Lauber D. Differential effects of strength versus power training on bone mineral density in postmenopausal women: a 2-year longitudinal study. Br J Sports Med. 2007;41(10):649–55, discussion 55.CrossRefGoogle Scholar
  35. 35.
    Valdimarsson O, Linden C, Johnell O, Gardsell P, Karlsson MK. Daily physical education in the school curriculum in prepubertal girls during 1 year is followed by an increase in bone mineral accrual and bone width—data from the prospective controlled Malmo pediatric osteoporosis prevention study. Calcif Tissue Int. 2006;78(2):65–71.PubMedCrossRefGoogle Scholar
  36. 36.
    Kaga M, Takahashi K, Ishihara T, Suzuki H, Tanaka H, Seino Y, et al. Bone assessment of female long-distance runners. J Bone Miner Metab. 2004;22(5):509–13.PubMedCrossRefGoogle Scholar
  37. 37.
    Bellew JW, Gehrig L. A comparison of bone mineral density in adolescent female swimmers, soccer players, and weight lifters. Pediatr Phys Ther. 2006;18(1):19–22.PubMedCrossRefGoogle Scholar
  38. 38.
    Bemben DA, Buchanan TD, Bemben MG, Knehans AW. Influence of type of mechanical loading, menstrual status, and training season on bone density in young women athletes. J Strength Cond Res. 2004;18(2):220–6.PubMedCrossRefGoogle Scholar
  39. 39.
    Robinson TL, Snow-Harter C, Taaffe DR, Gillis D, Shaw J, Marcus R. Gymnasts exhibit higher bone mass than runners despite similar prevalence of amenorrhea and oligomenorrhea. J Bone Miner Res. 1995;10(1):26–35.PubMedCrossRefGoogle Scholar
  40. 40.
    Nichols JF, Rauh MJ, Barrack MT, Barkai HS. Bone mineral density in female high school athletes: interactions of menstrual function and type of mechanical loading. Bone 2007;41(3):371–7.PubMedCrossRefGoogle Scholar
  41. 41.
    Gremion G, Rizzoli R, Slosman D, Theintz G, Bonjour J. Oligo-amenorrheic long-distance runners may lose more bone in spine than in femur. Med Sci Sports Exerc. 2001;33(1):15–21.PubMedGoogle Scholar
  42. 42.
    De Souza MJ, Williams NI. Beyond hypoestrogenism in amenorrheic athletes: energy deficiency as a contributing factor for bone loss. Curr Sports Med Rep. 2005;4(1):38–44.PubMedCrossRefGoogle Scholar
  43. 43.
    Cobb K, Bachrach L, Greendale G, Marcus R, Neer R, Nieves J, et al. Disordered eating, menstrual irregularity, and bone mineral density in female runners. Med Sci Sports Exerc. 2003;35(5):711–9.PubMedCrossRefGoogle Scholar
  44. 44.
    Iacopino L, Siani V, Melchiorri G, Orlandi C, De Luna A, Cervelli V, et al. Body composition differences in adolescent female athletes and anorexic patients. Acta Diabetol. 2003;40(Suppl 1):S180–2.PubMedCrossRefGoogle Scholar
  45. 45.
    Abad V, Chrousos G, Reynolds J, Nieman L, Hill S, Weinstein R, et al. Glucocorticoid excess during adolescence leads to a major persistent deficit in bone mass and an increase in central body fat. J Bone Miner Res. 2001;16(10):1879–85.PubMedCrossRefGoogle Scholar
  46. 46.
    Di Somma C, Pivonello R, Loche S, Faggiano A, Marzullo P, Di Sarno A, et al. Severe impairment of bone mass and turnover in Cushing’s disease: comparison between childhood-onset and adulthood-onset disease. Clin Endocrinol (Oxf). 2002;56(2):153–8.CrossRefGoogle Scholar
  47. 47.
    Maccarinelli G, Sibilia V, Torsello A, Raimondo F, Pitto M, Giustina A, et al. Ghrelin regulates proliferation and differentiation of osteoblastic cells. J Endocrinol. 2005;184(1):249–56.PubMedCrossRefGoogle Scholar
  48. 48.
    Ducy P, Amling M, Takeda S, Priemel M, Schilling AF, Beil FT, et al. Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell 2000;100(2):197–207.PubMedCrossRefGoogle Scholar
  49. 49.
    Chen KT, Yang RS. Effects of exercise on lipid metabolism and musculoskeletal fitness in female athletes. World J Gastroenterol. 2004;10(1):122–6.PubMedGoogle Scholar
  50. 50.
    Loud KJ, Gordon CM, Micheli LJ, Field AE. Correlates of stress fractures among preadolescent and adolescent girls. Pediatrics 2005;115(4):e399–406.PubMedCrossRefGoogle Scholar
  51. 51.
    Loud KJ, Micheli LJ, Bristol S, Austin SB, Gordon CM. Family history predicts stress fracture in active female adolescents. Pediatrics 2007;120(2):e364–72.PubMedCrossRefGoogle Scholar
  52. 52.
    Kelsey JL, Bachrach LK, Procter-Gray E, Nieves J, Greendale GA, Sowers M, et al. Risk factors for stress fracture among young female cross-country runners. Med Sci Sports Exerc. 2007;39(9):1457–63.PubMedCrossRefGoogle Scholar
  53. 53.
    Guest NS, Barr SI. Cognitive dietary restraint is associated with stress fractures in women runners. Int J Sport Nutr Exerc Metab. 2005;15(2):147–59.PubMedGoogle Scholar
  54. 54.
    Nikander R, Sievanen H, Uusi-Rasi K, Heinonen A, Kannus P. Loading modalities and bone structures at nonweight-bearing upper extremity and weight-bearing lower extremity: a pQCT study of adult female athletes. Bone 2006;39(4):886–94.PubMedCrossRefGoogle Scholar
  55. 55.
    Castelo-Branco C, Vicente JJ, Pons F, Martinez de Osaba MJ, Casals E, Vanrell JA. Bone mineral density in young, hypothalamic oligoamenorrheic women treated with oral contraceptives. J Reprod Med. 2001;46(10):875–9.PubMedGoogle Scholar
  56. 56.
    Hergenroeder AC, Smith EO, Shypailo R, Jones LA, Klish WJ, Ellis K. Bone mineral changes in young women with hypothalamic amenorrhea treated with oral contraceptives, medroxyprogesterone, or placebo over 12 months. Am J Obstet Gynecol. 1997;176(5):1017–25.PubMedCrossRefGoogle Scholar
  57. 57.
    Klibanski A, Biller B, Schoenfeld D, Herzog D, Saxe V. The effects of estrogen administration on trabecular bone loss in young women with anorexia nervosa. J Clin Endocrinol Metab. 1995;80(3):898–904.PubMedCrossRefGoogle Scholar
  58. 58.
    Strokosch GR, Friedman AJ, Wu SC, Kamin M. Effects of an oral contraceptive (norgestimate/ethinyl estradiol) on bone mineral density in adolescent females with anorexia nervosa: a double-blind, placebo-controlled study. J Adolesc Health. 2006;39(6):819–27.PubMedCrossRefGoogle Scholar
  59. 59.
    Burr DB, Yoshikawa T, Teegarden D, Lyle R, McCabe G, McCabe LD, et al. Exercise and oral contraceptive use suppress the normal age-related increase in bone mass and strength of the femoral neck in women 18–31 years of age. Bone 2000;27(6):855–63.PubMedCrossRefGoogle Scholar
  60. 60.
    Hartard M, Kleinmond C, Kirchbichler A, Jeschke D, Wiseman M, Weissenbacher ER, et al. Age at first oral contraceptive use as a major determinant of vertebral bone mass in female endurance athletes. Bone 2004;35(4):836–41.PubMedCrossRefGoogle Scholar
  61. 61.
    Cobb KL, Bachrach LK, Sowers M, Nieves J, Greendale GA, Kent KK, et al. The effect of oral contraceptives on bone mass and stress fractures in female runners. Med Sci Sports Exerc. 2007;39(9):1464–73.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  1. 1.Neuroendocrine and Pediatric Endocrine UnitsMassachusetts General HospitalBostonUSA
  2. 2.BUL 457, Neuroendocrine UnitMassachusetts General HospitalBostonUSA

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