Bone health and the female athlete triad in adolescent athletes

Physician and Sportsmedicine

Volumn 39, Issue 1, 2011, Pages 131-141

  Ackerman, Kathryn E ^a,b   Misra, Madhusmita ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Adolescent; Athlete; Bone density; Bone microarchitecture; Cortisol; Estrogen; Female athlete triad; Growth hormone; Hormones; Hypogonadism; Leptin; Nutrition; Physical activity

Indexed keywords

CALCIUM; CALCIUM CARBONATE; CALCIUM PHOSPHATE; CITRATE CALCIUM; ESTROGEN; GHRELIN; HYDROCORTISONE; SOMATOMEDIN B; SOMATOMEDIN BINDING PROTEIN 2; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN BINDING PROTEIN 4; SOMATOMEDIN BINDING PROTEIN 5; SOMATOMEDIN C; TESTOSTERONE; VITAMIN D;

ANOREXIA NERVOSA; BLOATING; BONE DENSITY; BONE GROWTH; BONE MASS; BONE METABOLISM; BONE MINERALIZATION; CALCIUM INTAKE; CONSTIPATION; FEMALE ATHLETE TRIAD; GROWTH RATE; HUMAN; NUTRITIONAL ASSESSMENT; OSSIFICATION; PHYSICAL ACTIVITY; REVIEW; SEX DIFFERENCE; VITAMIN BLOOD LEVEL; VITAMIN D DEFICIENCY;

EID: 79952239085     PISSN: 00913847     EISSN: None     Source Type: Journal    
DOI: 10.3810/psm.2011.02.1871     Document Type: Review

References (146)

1. Melton LJ 3rd. Adverse outcomes of osteoporotic fractures in the general population. J Bone Miner Res. 2003;18(6):1139-1141.
2. Johnston CC Jr, Slemenda CW. Peak bone mass, bone loss and risk of fracture. Osteoporos Int. 1994;4(suppl 1):43-45.
3. Cummings SR, Black DM, Nevitt MC, et al. Bone density at various sites for prediction of hip fractures. The Study of Osteoporotic Fractures Research Group. Lancet. 1993;341(8837):72-75.
4. Recker RR, Davies KM, Hinders SM, Heaney RP, Stegman MR, Kimmel DB. Bone gain in young adult women. JAMA. 1992;268(17):2403-2408.
5. Henry YM, Fatayerji D, Eastell R. Attainment of peak bone mass at the lumbar spine, femoral neck and radius in men and women: relative contributions of bone size and volumetric bone mineral density. Osteoporos Int. 2004;15(4):263-273. (Pubitemid 38543944)
6. Bailey DA, Martin AD, McKay HA, Whiting S, Mirwald R. Calcium accretion in girls and boys during puberty: a longitudinal analysis. J Bone Miner Res. 2000;15(11):2245-2250.
7. Rizzoli R, Bianchi ML, Garabédian M, McKay HA, Moreno LA. Maximizing bone mineral mass gain during growth for the prevention of fractures in the adolescents and the elderly. Bone. 2010;46(2): 294-305.
8. Bonjour JP, Chevalley T, Rizzoli R, Ferrari S. Gene-environment interactions in the skeletal response to nutrition and exercise during growth. Med Sport Sci. 2007;51:64-80.
9. Davies JH, Evans BA, Gregory JW. Bone mass acquisition in healthy children. Arch Dis Child. 2005;90(4):373-378. (Pubitemid 40488675)
10. Hopper JL, Green RM, Nowson CA, et al. Genetic, common environment, and individual specific components of variance for bone mineral density in 10- to 26-year-old females: a twin study. Am J Epidemiol. 1998;147(1):17-29. (Pubitemid 28034608)
11. Maimoun L, Sultan C. Effects of physical activity on bone remodeling [published online ahead of print March 20, 2010]. Metabolism.
12. Munns CF, Cowell CT. Prevention and treatment of osteoporosis in chronically ill children. J Musculoskelet Neuronal Interact. 2005;5(3): 262-272. (Pubitemid 41684175)
13. Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP; American College of Sports Medicine. American College of Sports Medicine position stand. The female athlete triad. Med Sci Sports Exerc. 2007;39(10):1867-1882.
14. Holick MF. Vitamin D deficiency. N Engl J Med. 2007;357(3):266-281.
15. Christo K, Prabhakaran R, Lamparello B, et al. Bone metabolism in adolescent athletes with amenorrhea, athletes with eumenorrhea, and control subjects. Pediatrics. 2008;121(6):1127-1136.
16. Bonjour JP, Theintz G, Law F, Slosman D, Rizzoli R. Peak bone mass. Osteoporos Int. 1994;4(suppl 1):7-13.
17. Cooper C. Review: developmental origins of osteoporotic fracture. Osteoporos Int. 2006;17(3):337-347.
18. Bass S, Delmas PD, Pearce G, Hendrich E, Tabensky A, Seeman E. The differing tempo of growth in bone size, mass, and density in girls is region-specific. J Clin Invest. 1999;104(6):795-804. (Pubitemid 29536365)
19. Bradney M, Karlsson MK, Duan Y, Stuckey S, Bass S, Seeman E. Heterogeneity in the growth of the axial and appendicular skeleton in boys: implications for the pathogenesis of bone fragility in men. J Bone Miner Res. 2000;15(10):1871-1878.
20. Bailey DA, McKay HA, Mirwald RL, Crocker PR, Faulkner RA. A six-year longitudinal study of the relationship of physical activity to bone mineral accrual in growing children: the University of Saskatchewan Bone Mineral Accrual Study. J Bone Miner Res. 1999;14(10):1672-1679. (Pubitemid 29455815)
21. Veldhuis JD, Roemmich JN, Richmond EJ, et al. Endocrine control of body composition in infancy, childhood, and puberty. Endocr Rev. 2005;26(1):114-146. (Pubitemid 40209389)
22. Riggs BL, Khosla S, Melton LJ 3rd. The assembly of the adult skeleton during growth and maturation: implications for senile osteoporosis. J Clin Invest. 1999;104(6):671-672. (Pubitemid 29536349)
23. Theintz G, Buchs B, Rizzoli R, 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):1060-1065.
24. Mora S, Gilsanz V. Establishment of peak bone mass. Endocrinol Metab Clin North Am. 2003;32(1):39-63. (Pubitemid 36378634)
25. Gilsanz V, Gibbens DT, Carlson M, Boechat MI, Cann CE, Schulz EE. Peak trabecular vertebral density: a comparison of adolescent and adult females. Calcif Tissue Int. 1988;43(4):260-262.
26. Weaver JK, Chalmers J. Cancellous bone: its strength and changes with aging and an evaluation of some methods for measuring its mineral content. J Bone Joint Surg Am. 1966;48(2):289-298.
27. Marcus R, Kosek J, Pfefferbaum A, Horning S. Age-related loss of trabecular bone in premenopausal women: a biopsy study. Calcif Tissue Int. 1983;35(4-5):406-409. (Pubitemid 13028604)
28. Mosekilde L, Mosekilde L. Sex differences in age-related changes in vertebral body size, density and biomechanical competence in normal individuals. Bone. 1990;11(2):67-73. (Pubitemid 20226564)
29. Gilsanz V, Boechat MI, Roe TF, Loro ML, Sayre JW, Goodman WG. Gender differences in vertebral body sizes in children and adolescents. Radiology. 1994;190(3):673-677. (Pubitemid 24071027)
30. Gilsanz V, Boechat MI, Gilsanz R, Loro ML, Roe TF, Goodman WG. Gender differences in vertebral sizes in adults: biomechanical implications. Radiology. 1994;190(3):678-682. (Pubitemid 24071028)
31. Burrows M, Liu D, McKay H. High-resolution peripheral QCT imaging of bone micro-structure in adolescents. Osteoporos Int. 2010;21(3):515-520.
32. Finkelstein JS, Neer RM, Biller BM, Crawford JD, Klibanski A. Osteopenia in men with a history of delayed puberty. N Engl J Med. 1992;326(9):600-604.
33. Finkelstein JS, Klibanski A, Neer RM. A longitudinal evaluation of bone mineral density in adult men with histories of delayed puberty. J Clin Endocrinol Metab. 1996;81(3):1152-1155. (Pubitemid 26083985)
34. Bertelloni S, Baroncelli GI, Battini R, Perri G, Saggese G. Short-term effect of testosterone treatment on reduced bone density in boys with constitutional delay of puberty. J Bone Miner Res. 1995;10(10):1488-1495.
35. Soyka LA, Grinspoon S, Levitsky LL, Herzog DB, Klibanski A. The effects of anorexia nervosa on bone metabolism in female adolescents. J Clin Endocrinol Metab. 1999;84(12):4489-4496.
36. Bredella MA, Ghomi RH, Thomas BJ, et al. Comparison of DXA and CT in the assessment of body composition in premenopausal women with obesity and anorexia nervosa. Obesity (Silver Spring). 2010;18(11):2227-2233.
37. Misra M, Aggarwal A, Miller KK, et al. Effects of anorexia nervosa on clinical, hematologic, biochemical, and bone density parameters in community-dwelling adolescent girls. Pediatrics. 2004;114(6):574-583.
38. DiVasta AD, Beck TJ, Petit MA, Feldman HA, LeBoff MS, Gordon CM. Bone cross-sectional geometry in adolescents and young women with anorexia nervosa: a hip structural analysis study. Osteoporos Int. 2007;18(6):797-804. (Pubitemid 46684785)
39. Ecklund K, Vajapeyam S, Feldman HA, et al. Bone marrow changes in adolescent girls with anorexia nervosa. J Bone Miner Res. 2010;25(2):298-304.
40. Bredella MA, Misra M, Miller KK, et al. Distal radius in adolescent girls with anorexia nervosa: trabecular structure analysis with high-resolution flat-panel volume CT. Radiology. 2008;249(3):938-946.
41. Slemenda CW, Reister TK, Hui SL, Miller JZ, Christian JC, Johnston CC Jr. Influences on skeletal mineralization in children and adolescents: evidence for varying effects of sexual maturation and physical activity. J Pediatr. 1994;125(2):201-207. (Pubitemid 24252998)
42. Kasperk CH, Wakley GK, Hierl T, Ziegler R. Gonadal and adrenal androgens are potent regulators of human bone cell metabolism in vitro. J Bone Miner Res. 1997;12(3):464-471. (Pubitemid 27120484)
43. Smith EP, Boyd J, Frank GR, et al. Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. N Engl J Med. 1994;331(16):1056-1061. (Pubitemid 24317698)
44. Morishima A, Grumbach MM, Simpson ER, Fisher C, Qin K. Aromatase deficiency in male and female siblings caused by a novel mutation and the physiological role of estrogens. J Clin Endocrinol Metab. 1995;80(12):3689-3698.
45. Bilezikian JP, Morishima A, Bell J, Grumbach MM. Increased bone mass as a result of estrogen therapy in a man with aromatase deficiency. N Engl J Med. 1998;339(9):599-603. (Pubitemid 28385657)
46. Bouillon R, Bex M, Vanderschueren D, Boonen S. Estrogens are essential for male pubertal periosteal bone expansion. J Clin Endocrinol Metab. 2004;89(12):6025-6029. (Pubitemid 39628410)
47. Eriksson S, Eriksson A, Stege R, Carlström K. Bone mineral density in patients with prostatic cancer treated with orchidectomy and with estrogens. Calcif Tissue Int. 1995;57(2):97-99.
48. Reutrakul S, Ongphiphadhanakul B, Piaseu N, et al. The effects of oestrogen exposure on bone mass in male to female transsexuals. Clin Endocrinol (Oxf). 1998;49(6):811-814. (Pubitemid 29009512)
49. Orwoll ES. Men, bone and estrogen: unresolved issues. Osteoporos Int. 2003;14(2):93-98. (Pubitemid 40824222)
50. Khosla S, Melton LJ 3rd, Riggs BL. Clinical review 144: estrogen and the male skeleton. J Clin Endocrinol Metab. 2002;87(4):1443-1450. (Pubitemid 34615219)
51. Simpson E, Rubin G, Clyne C, et al. The role of local estrogen biosynthesis in males and females. Trends Endocrinol Metab. 2000;11(5): 184-188. (Pubitemid 30457139)
52. Turner RT, Wakley GK, Hannon KS. Differential effects of androgens on cortical bone histomorphometry in gonadectomized male and female rats. J Orthop Res. 1990;8(4):612-617. (Pubitemid 20319518)
53. Gordon CM, Glowacki J, LeBoff MS. DHEA and the skeleton (through the ages). Endocrine. 1999;11(1):1-11.
54. Labrie F, Bélanger A, Cusan L, Candas B. Physiological changes in dehydroepiandrosterone are not reflected by serum levels of active androgens and estrogens but of their metabolites: intracrinology. J Clin Endocrinol Metab. 1997;82(8):2403-2409. (Pubitemid 27337847)
55. Ohlsson C, Bengtsson BA, Isaksson OG, Andreassen TT, Slootweg MC. Growth hormone and bone. Endocr Rev. 1998;19(1):55-79. (Pubitemid 29122074)
56. Bonjour JP, Ammann P, Chevalley T, Rizzoli R. Protein intake and bone growth. Can J Appl Physiol. 2001;26(suppl):S153-S166.
57. High WB, Capen CC, Black HE. Effects of thyroxine on cortical bone remodeling in adult dogs: a histomorphometric study. Am J Pathol. 1981;102(3):438-446. (Pubitemid 11143437)
58. Gennari C. Differential effect of glucocorticoids on calcium absorption and bone mass. Br J Rheumatol. 1993;32(suppl 2):11-14. (Pubitemid 23179589)
59. O'Brien CA, Jia D, Plotkin LI, et al. Glucocorticoids act directly on osteoblasts and osteocytes to induce their apoptosis and reduce bone formation and strength. Endocrinology. 2004;145(4):1835-1841. (Pubitemid 38402392)
60. Kim HJ, Zhao H, Kitaura H, et al. Glucocorticoids suppress bone formation via the osteoclast. J Clin Invest. 2006;116(8):2152-2160. (Pubitemid 44162324)
61. Driessler F, Baldock PA. Hypothalamic regulation of bone. J Mol Endocrinol. 2010;45(4):175-181.
62. Fukushima N, Hanada R, Teranishi H, et al. Ghrelin directly regulates bone formation. J Bone Miner Res. 2005;20(5):790-798. (Pubitemid 40571636)
63. Kim SW, Her SJ, Park SJ, et al. Ghrelin stimulates proliferation and differentiation and inhibits apoptosis in osteoblastic MC3T3-E1 cells. Bone. 2005;37(3):359-369. (Pubitemid 41160494)
64. Wang DH, Hu YS, Du JJ, Hu YY, Zhong WD, Qin WJ. Ghrelin stimulates proliferation of human osteoblastic TE85 cells via NO/cGMP signaling pathway. Endocrine. 2009;35(1):112-117.
65. Russell M, Stark J, Nayak S, et al. Peptide YY in adolescent athletes with amenorrhea, eumenorrheic athletes and non-athletic controls. Bone. 2009;45(1):104-109.
66. Baldock PA, Sainsbury A, Couzens M, et al. Hypothalamic Y2 receptors regulate bone formation. J Clin Invest. 2002;109(7):915-921. (Pubitemid 34275112)
67. Sayers A, Timpson NJ, Sattar N, et al. Adiponectin and its association with bone mass accrual in childhood. J Bone Miner Res. 2010;25(10): 2212-2220.
68. Richards JB, Valdes AM, Burling K, Perks UC, Spector TD. Serum adiponectin and bone mineral density in women. J Clin Endocrinol Metab. 2007;92(4):1517-1523. (Pubitemid 46556433)
69. Kanazawa I, Yamaguchi T, Yano S, Yamauchi M, Yamamoto M, Sugimoto T. Adiponectin and AMP kinase activator stimulate proliferation, differentiation, and mineralization of osteoblastic MC3T3-E1 cells. BMC Cell Biol. 2007;8:51.
70. Luo XH, Guo LJ, Xie H, et al. Adiponectin stimulates RANKL and inhibits OPG expression in human osteoblasts through the MAPK signaling pathway. J Bone Miner Res. 2006;21(10):1648-1656. (Pubitemid 44484610)
71. Misra M, Miller KK, Almazan C, et al. Alterations in cortisol secretory dynamics in adolescent girls with anorexia nervosa and effects on bone metabolism. J Clin Endocrinol Metab. 2004;89(10):4972-4980. (Pubitemid 39391436)
72. Ahmed ML, Ong KK, Morrell DJ, et al. Longitudinal study of leptin concentrations during puberty: sex differences and relationship to changes in body composition. J Clin Endocrinol Metab. 1999;84(3):899-905. (Pubitemid 29138215)
73. Pomerants T, Tillmann V, Jürimäe J, Jürimäe T. Relationship between ghrelin and anthropometrical, body composition parameters and testosterone levels in boys at different stages of puberty. J Endocrinol Invest. 2006;29(11):962-967. (Pubitemid 46344229)
74. Lloyd B, Ravi P, Mendes N, Klibanski A, Misra M. Peptide YY levels across pubertal stages and associations with growth hormone. J Clin Endocrinol Metab. 2010;95(6):2957-2962.
75. Jürimäe J, Jürimäe T, Purge P. Plasma ghrelin is altered after maximal exercise in elite male rowers. Exp Biol Med (Maywood). 2007;232(7): 904-909. (Pubitemid 47026796)
76. Warrick JI, Wittert GA. Exercise and the hypothalamic-pituitary-adrenal axis. In: The Endocrine System in Sports and Exercise. Kraemer WJ, Rogol AD, eds. Blackweil Publishing Inc.; Malden, MA; 2005:217-231.
77. Jayasinghe Y, Grover SR, Zacharin M. Current concepts in bone and reproductive health in adolescents with anorexia nervosa. BJOG. 2008;115(3):304-315.
78. Wolfe BE, Jimerson DC, Orlova C, Mantzoros CS. Effect of dieting on plasma leptin, soluble leptin receptor, adiponectin and resistin levels in healthy volunteers. Clin Endocrinol (Oxf). 2004;61(3):332-338. (Pubitemid 39287062)
79. Misra M, Miller KK, Bjornson J, et al. Alterations in growth hormone secretory dynamics in adolescent girls with anorexia nervosa and effects on bone metabolism. J Clin Endocrinol Metab. 2003;88(12): 5615-5623. (Pubitemid 38033024)
80. Misra M, Klibanski A. Neuroendocrine consequences of anorexia nervosa in adolescents. Endocr Dev. 2010;17:197-214.
81. Christo K, Cord J, Mendes N, et al. Acylated ghrelin and leptin in adolescent athletes with amenorrhea, eumenorrheic athletes and controls: a cross-sectional study. Clin Endocrinol (Oxf). 2008;69(4):628-633.
82. 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. (Pubitemid 40956533)
83. De Souza MJ. Menstrual disturbances in athletes: a focus on luteal phase defects. Med Sci Sports Exerc. 2003;35(9):1553-1563. (Pubitemid 37087587)
84. 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):137-142. (Pubitemid 43213857)
85. 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. (Pubitemid 38057639)
86. Estok PJ, Rudy EB. The relationship between eating disorders and running in women. Res Nurs Health. 1996;19(5):377-387. (Pubitemid 126702591)
87. Lebrun CM. The female athlete triad: what's a doctor to do? Curr Sports Med Rep. 2007;6(6):397-404.
88. Steen SN, Brownell KD. Patterns of weight loss and regain in wrestlers: has the tradition changed? Med Sci Sports Exerc. 1990;22(6):762-768.
89. 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.
90. Loud KJ, Gordon CM. Adolescent bone health. Arch Pediatr Adolesc Med. 2006;160(10):1026-1032. (Pubitemid 44520632)
91. Nichols DL, Bonnick SL, Sanborn CF. Bone health and osteoporosis. Clin Sports Med. 2000;19(2):233-249. (Pubitemid 30159948)
92. Nichols DL, Sanborn CF, Essery EV. Bone density and young athletic women. An update. Sports Med. 2007;37(11):1001-1014.
93. Nordström A, Karlsson C, Nyquist F, Olsson T, Nordström P, Karlsson M. Bone loss and fracture risk after reduced physical activity. J Bone Miner Res. 2005;20(2):202-207.
94. Kanis JA, Johnell O, Oden A, Dawson A, De Laet C, Jonsson B. Ten year probabilities of osteoporotic fractures according to BMD and diagnostic thresholds. Osteoporos Int. 2001;12(12):989-995. (Pubitemid 34105967)
95. 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):371-377. (Pubitemid 47199150)
96. Fehling PC, Alekel L, Clasey J, Rector A, Stillman RJ. A comparison of bone mineral densities among female athletes in impact loading and active loading sports. Bone. 1995;17(3):205-210.
97. 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. (Pubitemid 44309948)
98. Slemenda CW, Miller JZ, Hui SL, Reister TK, Johnston CC Jr. Role of physical activity in the development of skeletal mass in children. J Bone Miner Res. 1991;6(11):1227-1233.
99. Duncan CS, Blimkie CJ, Cowell CT, Burke ST, Briody JN, Howman-Giles R. Bone mineral density in adolescent female athletes: relationship to exercise type and muscle strength. Med Sci Sports Exerc. 2002;34(2): 286-294. (Pubitemid 34132034)
100. Greene DA, Naughton GA. Adaptive skeletal responses to mechanical loading during adolescence. Sports Med. 2006;36(9):723-732. (Pubitemid 44338174)
101. Ducher G, Tournaire N, Meddahi-Pellé A, Benhamou CL, Courteix D. Short-term and long-term site-specific effects of tennis playing on trabecular and cortical bone at the distal radius. J Bone Miner Metab. 2006;24(6):484-490. (Pubitemid 44663421)
102. Lorentzon M, Mellström D, Ohlsson C. Association of amount of physical activity with cortical bone size and trabecular volumetric BMD in young adult men: the GOOD study. J Bone Miner Res. 2005;20(11):1936-1943. (Pubitemid 41532779)
103. Nilsson M, Ohlsson C, Mellström D, Lorentzon M. Previous sport activity during childhood and adolescence is associated with increased cortical bone size in young adult men. J Bone Miner Res. 2009;24(1):125-133.
104. Bennell KL, Malcolm SA, Khan KM, et al. Bone mass and bone turnover in power athletes, endurance athletes, and controls: a 12-month longitudinal study Bone. 1997;20(5):477-484.
105. Kato T, Yamashita T, Mizutani S, Honda A, Matumoto M, Umemura Y Adolescent exercise associated with long-term superior measures of bone geometry: a cross-sectional DXA and MRI study. Br J Sports Med. 2009;43(12):932-935.
106. Korpelainen R, Keinänen-Kiukaanniemi S, Nieminen P, Heikkinen J, Väänänen K, Korpelainen J. Long-term outcomes of exercise: follow-up of a randomized trial in older women with osteopenia. Arch Intern Med. 2010;170(17):1548-1556.
107. Kohrt WM, Bloomfield SA, Little KD, Nelson ME, Yingling VR; American College of Sports Medicine. American College of Sports Medicine Position Stand: physical activity and bone health. Med Sci Sports Exerc. 2004;36(11):1985-1996.
108. Hind K, Burrows M. Weight-bearing exercise and bone mineral accrual in children and adolescents: a review of controlled trials. Bone. 2007;40(1):14-27. (Pubitemid 44848417)
109. McKay H, Liu D, Egeli D, Boyd S, Burrows M. Physical activity positively predicts bone architecture and bone strength in adolescent males and females. Acta Paediatr. 2011;100(1):97-101.
110. Fredericson M, Jennings F, Beaulieu C, Matheson GO. Stress fractures in athletes. Top Magn Reson Imaging. 2006;17(5):309-325.
111. Rico H, Revilla M, Villa LF, Gomez-Castresana F, Alvarez del Buergo M. Body composition in postpubertal boy cyclists. J Sports Med Phys Fitness. 1993;33(3):278-281.
112. Hackney AC. Effects of endurance exercise on the reproductive system of men: the "exercise-hypogonadal male condition." J Endocrinol Invest. 2008;31(10):932-938.
113. Grimston SK, Willows ND, Hanley DA. Mechanical loading regime and its relationship to bone mineral density in children. Med Sci Sports Exerc. 1993;25(11):1203-1210. (Pubitemid 23326472)
114. Nigg BM. Biomechanics, load analysis and sports injuries in the lower extremities. Sports Med. 1985;2(5):367-379. (Pubitemid 15020787)
115. 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.
116. Bailey DA, Wedge JH, McCulloch RG, Martin AD, Bernhardson SC. Epidemiology of fractures of the distal end of the radius in children as associated with growth. J Bone Joint Surg Am. 1989;71(8):1225-1231. (Pubitemid 19262372)
117. Greer FR, Krebs NF; American Academy of Pediatrics Committee on Nutrition. Optimizing bone health and calcium intakes of infants, children, and adolescents. Pediatrics. 2006;117(2):578-585.
118. Wyshak G, Frisch RE. Carbonated beverages, dietary calcium, the dietary calcium/phosphorus ratio, and bone fractures in girls and boys. J Adolesc Health. 1994;15(3):210-215. (Pubitemid 24161159)
119. Goulding A, Cannan R, Williams SM, Gold EJ, Taylor RW, Lewis-Barned NJ. Bone mineral density in girls with forearm fractures. J Bone Miner Res. 1998;13(1):143-148. (Pubitemid 28063123)
120. Goulding A, Jones IE, Taylor RW, Manning PJ, Williams SM. More broken bones: a 4-year double cohort study of young girls with and without distal forearm fractures. J Bone Miner Res. 2000;15(10): 2011-2018.
121. Goulding A, Jones IE, Taylor RW, Williams SM, Manning PJ. Bone mineral density and body composition in boys with distal forearm fractures: a dual-energy x-ray absorptiometry study. J Pediatr. 2001;139(4):509-515. (Pubitemid 32977264)
122. Prentice A, Ginty F, Stear SJ, Jones SC, Laskey MA, Cole TJ. Calcium supplementation increases stature and bone mineral mass of 16- to 18-year-old boys. J Clin Endocrinol Metab. 2005;90(6):3153-3161. (Pubitemid 41014268)
123. Rozen GS, Rennert G, Dodiuk-Gad RP, et al. Calcium supplementation provides an extended window of opportunity for bone mass accretion after menarche. Am J Clin Nutr. 2003;78(5):993-998. (Pubitemid 39663477)
124. Recker RR. Calcium absorption and achlorhydria. N Engl J Med. 1985;313(2):70-73. (Pubitemid 15068699)
125. Institute of Medicine. Dietary reference intakes for calcium, phosphorus, magnesium, vitamin D, and fluoride. National Academy Press: Washington DC; 1997.
126. Casey CF, Slawson DC, Neal LR. Vitamin D supplementation in infants, children, and adolescents. Am Fam Physician. 2010;81(6):745-748.
127. Clemens TL, Adams JS, Henderson SL, Holick MF. Increased skin pigment reduces the capacity of skin to synthesise vitamin D3. Lancet. 1982;1(8263):74-76. (Pubitemid 12248649)
128. Larson-Meyer DE, Willis KS. Vitamin D and athletes. Curr Sports Med Rep. 2010;9(4):220-226.
129. Stoffman N, Gordon CM. Vitamin D and adolescents: what do we know? Curr Opin Pediatr. 2009;21(4):465-471.
130. Gordon CM, DePeter KC, Feldman HA, Grace E, Emans SJ. Prevalence of vitamin D deficiency among healthy adolescents. Arch Pediatr Adolesc Med. 2004;158(6):531-537. (Pubitemid 38720483)
131. Moore C, Murphy MM, Keast DR, Holick MF. Vitamin D intake in the United States. J Am Diet Assoc. 2004;104(6):980-983.
132. Wagner CL, Greer FR; American Academy of Pediatrics Section on Breastfeeding; American Academy of Pediatrics Committee on Nutrition. Prevention of rickets and vitamin D deficiency in infants, children, and adolescents. Pediatrics. 2008;122(5):1142-1152.
133. Holick MF. Vitamin D: extraskeletal health. Endocrinol Metab Clin North Am. 2010;39(2):381-400.
134. Willis KS, Peterson NJ, Larson-Meyer DE. Should we be concerned about the vitamin D status of athletes? Int J Sport Nutr Exerc Metab. 2008;18(2):204-224.
135. Nattiv A, Agostini R, Drinkwater B, Yeager KK. The female athlete triad. The inter-relatedness of disordered eating, amenorrhea, and osteoporosis. Clin Sports Med. 1994;13(2):405-418.
136. Loucks AB, Horvath SM. Athletic amenorrhea: a review. Med Sci Sports Exerc. 1985;17(1):56-72. (Pubitemid 15140411)
137. Otis CL. Exercise-associated amenorrhea. Clin Sports Med. 1992;11(2):351-362.
138. Shangold M, Rebar RW, Wentz AC, Schiff I. Evaluation and management of menstrual dysfunction in athletes. JAMA. 1990;263(12):1665-1669. (Pubitemid 20090697)
139. 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):3158-3164. (Pubitemid 44271772)
140. De Souza MJ, West SL, Jamal SA, Hawker GA, Gundberg CM, Williams NI. The presence of both an energy deficiency and estrogen deficiency exacerbate alterations of bone metabolism in exercising women. Bone. 2008;43(1):140-148.
141. Liu SL, Lebrun CM. Effect of oral contraceptives and hormone replacement therapy on bone mineral density in premenopausal and perimenopausal women: a systematic review. Br J Sports Med. 2006;40(1):11-24. (Pubitemid 43028585)
142. Riggs BL. The mechanisms of estrogen regulation of bone resorption. J Clin Invest. 2000;106(10):1203-1204.
143. Chen FP, Lee N, Soong YK, Huang KE. Comparison of transdermal and oral estrogen-progestin replacement therapy: effects on cardiovascular risk factors. Menopause. 2001;8(5):347-352. (Pubitemid 32826167)
144. Vongpatanasin W, Tuncel M, Wang Z, Arbique D, Mehrad B, Jialal I. Differential effects of oral versus transdermal estrogen replacement therapy on C-reactive protein in postmenopausal women. J Am Coll Cardiol. 2003;41(8):1358-1363. (Pubitemid 36438997)
145. Gower BA, Nyman L. Associations among oral estrogen use, free testosterone concentration, and lean body mass among postmenopausal women. J Clin Endocrinol Metab. 2000;85(12):4476-4480. (Pubitemid 32157621)
146. Nabhan ZM, Dimeglio LA, Qi R, Perkins SM, Eugster EA. Conjugated oral versus transdermal estrogen replacement in girls with Turner syndrome: a pilot comparative study. J Clin Endocrinol Metab. 2009;94(6):2009-2014.