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Published in: European Journal of Nutrition 3/2018

Open Access 01-04-2018 | Review

Reduced energy availability: implications for bone health in physically active populations

Authors: Maria Papageorgiou, Eimear Dolan, Kirsty J. Elliott-Sale, Craig Sale

Published in: European Journal of Nutrition | Issue 3/2018

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Abstract

Purpose

The present review critically evaluates existing literature on the effects of short- and long-term low energy availability (EA) on bone metabolism and health in physically active individuals.

Methods

We reviewed the literature on the short-term effects of low EA on markers of bone metabolism and the long-term effects of low EA on outcomes relating to bone health (bone mass, microarchitecture and strength, bone metabolic markers and stress fracture injury risk) in physically active individuals.

Results

Available evidence indicates that short-term low EA may increase markers of bone resorption and decrease markers of bone formation in physically active women. Bone metabolic marker responses to low EA are less well known in physically active men. Cross-sectional studies investigating the effects of long-term low EA suggest that physically active individuals who have low EA present with lower bone mass, altered bone metabolism (favouring bone resorption), reduced bone strength and increased risk for stress fracture injuries.

Conclusions

Reduced EA has a negative influence on bone in both the short- and long-term, and every effort should be made to reduce its occurrence in physically active individuals. Future interventions are needed to explore the effects of long-term reduced EA on bone health outcomes, while short-term low EA studies are also required to give insight into the pathophysiology of bone alterations.
Literature
3.
go back to reference Ackerman KE, Nazem T, Chapko D, Russell M, Mendes N, Taylor AP, Bouxsein ML, Misra M (2011) Bone microarchitecture is impaired in adolescent amenorrheic athletes compared with eumenorrheic athletes and nonathletic controls. J Clin Endocrinol Metab 96(10):3123–3133. doi:10.1210/jc.2011-1614 CrossRef Ackerman KE, Nazem T, Chapko D, Russell M, Mendes N, Taylor AP, Bouxsein ML, Misra M (2011) Bone microarchitecture is impaired in adolescent amenorrheic athletes compared with eumenorrheic athletes and nonathletic controls. J Clin Endocrinol Metab 96(10):3123–3133. doi:10.​1210/​jc.​2011-1614 CrossRef
4.
go back to reference Ackerman KE, Putman M, Guereca G, Taylor AP, Pierce L, Herzog DB, Klibanski A, Bouxsein M, Misra M (2012) Cortical microstructure and estimated bone strength in young amenorrheic athletes, eumenorrheic athletes and non-athletes. Bone 51(4):680–687. doi:10.1016/j.bone.2012.07.019 CrossRef Ackerman KE, Putman M, Guereca G, Taylor AP, Pierce L, Herzog DB, Klibanski A, Bouxsein M, Misra M (2012) Cortical microstructure and estimated bone strength in young amenorrheic athletes, eumenorrheic athletes and non-athletes. Bone 51(4):680–687. doi:10.​1016/​j.​bone.​2012.​07.​019 CrossRef
5.
go back to reference Burt LA, Greene DA, Ducher G, Naughton GA (2013) Skeletal adaptations associated with pre-pubertal gymnastics participation as determined by DXA and pQCT: a systematic review and meta-analysis. J Sci Med Sport 16(3):231–239. doi:10.1016/j.jsams.2012.07.006 CrossRef Burt LA, Greene DA, Ducher G, Naughton GA (2013) Skeletal adaptations associated with pre-pubertal gymnastics participation as determined by DXA and pQCT: a systematic review and meta-analysis. J Sci Med Sport 16(3):231–239. doi:10.​1016/​j.​jsams.​2012.​07.​006 CrossRef
6.
go back to reference Erlandson MC, Kontulainen SA, Chilibeck PD, Arnold CM, Faulkner RA, Baxter-Jones AD (2012) Higher premenarcheal bone mass in elite gymnasts is maintained into young adulthood after long-term retirement from sport: a 14-year follow-up. J Bone Miner Res 27(1):104–110. doi:10.1002/jbmr.514 CrossRef Erlandson MC, Kontulainen SA, Chilibeck PD, Arnold CM, Faulkner RA, Baxter-Jones AD (2012) Higher premenarcheal bone mass in elite gymnasts is maintained into young adulthood after long-term retirement from sport: a 14-year follow-up. J Bone Miner Res 27(1):104–110. doi:10.​1002/​jbmr.​514 CrossRef
8.
go back to reference Dolan E, McGoldrick A, Davenport C, Kelleher G, Byrne B, Tormey W, Smith D, Warrington GD (2012) An altered hormonal profile and elevated rate of bone loss are associated with low bone mass in professional horse-racing jockeys. J Bone Miner Metab 30(5):534–542. doi:10.1007/s00774-012-0354-4 CrossRef Dolan E, McGoldrick A, Davenport C, Kelleher G, Byrne B, Tormey W, Smith D, Warrington GD (2012) An altered hormonal profile and elevated rate of bone loss are associated with low bone mass in professional horse-racing jockeys. J Bone Miner Metab 30(5):534–542. doi:10.​1007/​s00774-012-0354-4 CrossRef
9.
go back to reference Dolan E, Crabtree N, McGoldrick A, Ashley DT, McCaffrey N, Warrington GD (2012) Weight regulation and bone mass: a comparison between professional jockeys, elite amateur boxers, and age, gender and BMI matched controls. J Bone Miner Metab 30(2):164–170. doi:10.1007/s00774-011-0297-1 CrossRef Dolan E, Crabtree N, McGoldrick A, Ashley DT, McCaffrey N, Warrington GD (2012) Weight regulation and bone mass: a comparison between professional jockeys, elite amateur boxers, and age, gender and BMI matched controls. J Bone Miner Metab 30(2):164–170. doi:10.​1007/​s00774-011-0297-1 CrossRef
10.
11.
go back to reference Zanker CL, Swaine IL (2000) Responses of bone turnover markers to repeated endurance running in humans under conditions of energy balance or energy restriction. Eur J Appl Physiol 83(4–5):434–440. doi:10.1007/s004210000293 CrossRef Zanker CL, Swaine IL (2000) Responses of bone turnover markers to repeated endurance running in humans under conditions of energy balance or energy restriction. Eur J Appl Physiol 83(4–5):434–440. doi:10.​1007/​s004210000293 CrossRef
14.
go back to reference Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP, American College of Sports M (2007) American College of Sports Medicine position stand. The female athlete triad. Med Sci Sports Exerc 39(10):1867–1882. doi:10.1249/mss.0b013e318149f111 CrossRef Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP, American College of Sports M (2007) American College of Sports Medicine position stand. The female athlete triad. Med Sci Sports Exerc 39(10):1867–1882. doi:10.​1249/​mss.​0b013e318149f111​ CrossRef
15.
go back to reference De Souza MJ, Nattiv A, Joy E, Misra M, Williams NI, Mallinson RJ, Gibbs JC, Olmsted M, Goolsby M, Matheson G, Expert P (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, California, May 2012 and 2nd International Conference held in Indianapolis, Indiana, May 2013. Br J Sports Med 48(4):289. doi:10.1136/bjsports-2013-093218 CrossRef De Souza MJ, Nattiv A, Joy E, Misra M, Williams NI, Mallinson RJ, Gibbs JC, Olmsted M, Goolsby M, Matheson G, Expert P (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, California, May 2012 and 2nd International Conference held in Indianapolis, Indiana, May 2013. Br J Sports Med 48(4):289. doi:10.​1136/​bjsports-2013-093218 CrossRef
16.
go back to reference Loucks AB (2007) Low energy availability in the marathon and other endurance sports. Sports Med 37(4–5):348–352CrossRef Loucks AB (2007) Low energy availability in the marathon and other endurance sports. Sports Med 37(4–5):348–352CrossRef
17.
go back to reference Barrack MT, Gibbs JC, De Souza MJ, Williams NI, Nichols JF, Rauh MJ, Nattiv A (2014) Higher incidence of bone stress injuries with increasing female athlete triad-related risk factors: a prospective multisite study of exercising girls and women. Am J Sports Med 42(4):949–958. doi:10.1177/0363546513520295 CrossRef Barrack MT, Gibbs JC, De Souza MJ, Williams NI, Nichols JF, Rauh MJ, Nattiv A (2014) Higher incidence of bone stress injuries with increasing female athlete triad-related risk factors: a prospective multisite study of exercising girls and women. Am J Sports Med 42(4):949–958. doi:10.​1177/​0363546513520295​ CrossRef
18.
go back to reference 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. doi:10.1136/bjsports-2014-093502 CrossRef 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. doi:10.​1136/​bjsports-2014-093502 CrossRef
20.
go back to reference Vasikaran S, Eastell R, Bruyere O, Foldes AJ, Garnero P, Griesmacher A, McClung M, Morris HA, Silverman S, Trenti T, Wahl DA, Cooper C, Kanis JA, Group I-IBMSW (2011) Markers of bone turnover for the prediction of fracture risk and monitoring of osteoporosis treatment: a need for international reference standards. Osteoporos Int 22(2):391–420. doi:10.1007/s00198-010-1501-1 CrossRef Vasikaran S, Eastell R, Bruyere O, Foldes AJ, Garnero P, Griesmacher A, McClung M, Morris HA, Silverman S, Trenti T, Wahl DA, Cooper C, Kanis JA, Group I-IBMSW (2011) Markers of bone turnover for the prediction of fracture risk and monitoring of osteoporosis treatment: a need for international reference standards. Osteoporos Int 22(2):391–420. doi:10.​1007/​s00198-010-1501-1 CrossRef
21.
22.
go back to reference Villareal DT, Fontana L, Weiss EP, Racette SB, Steger-May K, Schechtman KB, Klein S, Holloszy JO (2006) Bone mineral density response to caloric restriction-induced weight loss or exercise-induced weight loss: a randomized controlled trial. Arch Intern Med 166(22):2502–2510. doi:10.1001/archinte.166.22.2502 CrossRef Villareal DT, Fontana L, Weiss EP, Racette SB, Steger-May K, Schechtman KB, Klein S, Holloszy JO (2006) Bone mineral density response to caloric restriction-induced weight loss or exercise-induced weight loss: a randomized controlled trial. Arch Intern Med 166(22):2502–2510. doi:10.​1001/​archinte.​166.​22.​2502 CrossRef
24.
go back to reference Buchholz AC, Schoeller DA (2004) Is a calorie a calorie? Am J Clin Nutr 79(5):899S–906SCrossRef Buchholz AC, Schoeller DA (2004) Is a calorie a calorie? Am J Clin Nutr 79(5):899S–906SCrossRef
25.
go back to reference Hall KD, Heymsfield SB, Kemnitz JW, Klein S, Schoeller DA, Speakman JR (2012) Energy balance and its components: implications for body weight regulation. Am J Clin Nutr 95(4):989–994. doi:10.3945/ajcn.112.036350 CrossRef Hall KD, Heymsfield SB, Kemnitz JW, Klein S, Schoeller DA, Speakman JR (2012) Energy balance and its components: implications for body weight regulation. Am J Clin Nutr 95(4):989–994. doi:10.​3945/​ajcn.​112.​036350 CrossRef
26.
go back to reference Trabulsi J, Schoeller DA (2001) Evaluation of dietary assessment instruments against doubly labeled water, a biomarker of habitual energy intake. Am J Physiol Endocrinol Metab 281(5):E891–E899CrossRef Trabulsi J, Schoeller DA (2001) Evaluation of dietary assessment instruments against doubly labeled water, a biomarker of habitual energy intake. Am J Physiol Endocrinol Metab 281(5):E891–E899CrossRef
27.
go back to reference Hill RJ, Davies PS (2001) The validity of self-reported energy intake as determined using the doubly labelled water technique. Brit J Nutr 85(4):415–430CrossRef Hill RJ, Davies PS (2001) The validity of self-reported energy intake as determined using the doubly labelled water technique. Brit J Nutr 85(4):415–430CrossRef
29.
go back to reference Stubbs RJ, Hughes DA, Johnstone AM, Whybrow S, Horgan GW, King N, Blundell J (2004) Rate and extent of compensatory changes in energy intake and expenditure in response to altered exercise and diet composition in humans. Am J Physiol Regul Integr Comp Physiol 286(2):R350–R358. doi:10.1152/ajpregu.00196.2003 CrossRef Stubbs RJ, Hughes DA, Johnstone AM, Whybrow S, Horgan GW, King N, Blundell J (2004) Rate and extent of compensatory changes in energy intake and expenditure in response to altered exercise and diet composition in humans. Am J Physiol Regul Integr Comp Physiol 286(2):R350–R358. doi:10.​1152/​ajpregu.​00196.​2003 CrossRef
30.
go back to reference Loucks AB, Verdun M, Heath EM (1998) Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. J Appl Physiol 84(1):37–46CrossRef Loucks AB, Verdun M, Heath EM (1998) Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. J Appl Physiol 84(1):37–46CrossRef
31.
go back to reference 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. doi:10.1210/jc.2002-020369 CrossRef 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. doi:10.​1210/​jc.​2002-020369 CrossRef
32.
go back to reference Williams NI, Leidy HJ, Hill BR, Lieberman JL, Legro RS, De Souza MJ (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(1):E29–E39. doi:10.1152/ajpendo.00386.2013 CrossRef Williams NI, Leidy HJ, Hill BR, Lieberman JL, Legro RS, De Souza MJ (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(1):E29–E39. doi:10.​1152/​ajpendo.​00386.​2013 CrossRef
33.
go back to reference Yeager KK, Agostini R, Nattiv A, Drinkwater B (1993) The female athlete triad: disordered eating, amenorrhea, osteoporosis. Med Sci Sports Exerc 25(7):775–777CrossRef Yeager KK, Agostini R, Nattiv A, Drinkwater B (1993) The female athlete triad: disordered eating, amenorrhea, osteoporosis. Med Sci Sports Exerc 25(7):775–777CrossRef
34.
go back to reference 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–ixCrossRef 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–ixCrossRef
35.
go back to reference De Souza MJ, Williams NI, Nattiv A, Joy E, Misra M, Loucks AB, Matheson G, Olmsted MP, Barrack M, Mallinson RJ, Gibbs JC, Goolsby M, Nichols JF, Drinkwater B, Sanborn C, Agostini R, Otis CL, Johnson MD, Hoch AZ, Alleyne JM, Wadsworth LT, Koehler K, VanHeest J, Harvey P, Kelly AK, Fredericson M, Brooks GA, O’Donnell E, Callahan LR, Putukian M, Costello L, Hecht S, Rauh MJ, McComb J (2014) Misunderstanding the female athlete triad: refuting the IOC consensus statement on Relative Energy Deficiency in Sport (RED-S). Br Sports Med 48(20):1461–1465. doi:10.1136/bjsports-2014-093958 CrossRef De Souza MJ, Williams NI, Nattiv A, Joy E, Misra M, Loucks AB, Matheson G, Olmsted MP, Barrack M, Mallinson RJ, Gibbs JC, Goolsby M, Nichols JF, Drinkwater B, Sanborn C, Agostini R, Otis CL, Johnson MD, Hoch AZ, Alleyne JM, Wadsworth LT, Koehler K, VanHeest J, Harvey P, Kelly AK, Fredericson M, Brooks GA, O’Donnell E, Callahan LR, Putukian M, Costello L, Hecht S, Rauh MJ, McComb J (2014) Misunderstanding the female athlete triad: refuting the IOC consensus statement on Relative Energy Deficiency in Sport (RED-S). Br Sports Med 48(20):1461–1465. doi:10.​1136/​bjsports-2014-093958 CrossRef
36.
go back to reference Mountjoy M, Sundgot-Borgen J, Burke L, Carter S, Constantini N, Lebrun C, Meyer N, Sherman R, Steffen K, Budgett R, Ljungqvist A (2015) Authors’ 2015 additions to the IOC consensus statement: relative Energy Deficiency in Sport (RED-S). Br Sports Med 49(7):417–420CrossRef Mountjoy M, Sundgot-Borgen J, Burke L, Carter S, Constantini N, Lebrun C, Meyer N, Sherman R, Steffen K, Budgett R, Ljungqvist A (2015) Authors’ 2015 additions to the IOC consensus statement: relative Energy Deficiency in Sport (RED-S). Br Sports Med 49(7):417–420CrossRef
37.
38.
go back to reference Grinspoon S, Thomas E, Pitts S, Gross E, Mickley D, Miller K, Herzog D, Klibanski A (2000) Prevalence and predictive factors for regional osteopenia in women with anorexia nervosa. Ann Intern Med 133(10):790–794CrossRef Grinspoon S, Thomas E, Pitts S, Gross E, Mickley D, Miller K, Herzog D, Klibanski A (2000) Prevalence and predictive factors for regional osteopenia in women with anorexia nervosa. Ann Intern Med 133(10):790–794CrossRef
39.
go back to reference Misra M, Aggarwal A, Miller KK, Almazan C, Worley M, Soyka LA, Herzog DB, Klibanski A (2004) Effects of anorexia nervosa on clinical, hematologic, biochemical, and bone density parameters in community-dwelling adolescent girls. Pediatrics 114(6):1574–1583. doi:10.1542/peds.2004-0540 CrossRef Misra M, Aggarwal A, Miller KK, Almazan C, Worley M, Soyka LA, Herzog DB, Klibanski A (2004) Effects of anorexia nervosa on clinical, hematologic, biochemical, and bone density parameters in community-dwelling adolescent girls. Pediatrics 114(6):1574–1583. doi:10.​1542/​peds.​2004-0540 CrossRef
40.
go back to reference Robinson L, Aldridge V, Clark EM, Misra M, Micali N (2016) A systematic review and meta-analysis of the association between eating disorders and bone density. Osteoporos Int 27(6):1953–1966. doi:10.1007/s00198-015-3468-4 CrossRef Robinson L, Aldridge V, Clark EM, Misra M, Micali N (2016) A systematic review and meta-analysis of the association between eating disorders and bone density. Osteoporos Int 27(6):1953–1966. doi:10.​1007/​s00198-015-3468-4 CrossRef
41.
go back to reference Soyka LA, Misra M, Frenchman A, Miller KK, Grinspoon S, Schoenfeld DA, Klibanski A (2002) Abnormal bone mineral accrual in adolescent girls with anorexia nervosa. J Clin Endocrinol Metab 87(9):4177–4185. doi:10.1210/jc.2001-011889 CrossRef Soyka LA, Misra M, Frenchman A, Miller KK, Grinspoon S, Schoenfeld DA, Klibanski A (2002) Abnormal bone mineral accrual in adolescent girls with anorexia nervosa. J Clin Endocrinol Metab 87(9):4177–4185. doi:10.​1210/​jc.​2001-011889 CrossRef
42.
go back to reference Faje AT, Karim L, Taylor A, Lee H, Miller KK, Mendes N, Meenaghan E, Goldstein MA, Bouxsein ML, Misra M, Klibanski A (2013) Adolescent girls with anorexia nervosa have impaired cortical and trabecular microarchitecture and lower estimated bone strength at the distal radius. J Clin Endocrinol Metab 98(5):1923–1929. doi:10.1210/jc.2012-4153 CrossRef Faje AT, Karim L, Taylor A, Lee H, Miller KK, Mendes N, Meenaghan E, Goldstein MA, Bouxsein ML, Misra M, Klibanski A (2013) Adolescent girls with anorexia nervosa have impaired cortical and trabecular microarchitecture and lower estimated bone strength at the distal radius. J Clin Endocrinol Metab 98(5):1923–1929. doi:10.​1210/​jc.​2012-4153 CrossRef
43.
go back to reference Lawson EA, Miller KK, Bredella MA, Phan C, Misra M, Meenaghan E, Rosenblum L, Donoho D, Gupta R, Klibanski A (2010) Hormone predictors of abnormal bone microarchitecture in women with anorexia nervosa. Bone 46(2):458–463. doi:10.1016/j.bone.2009.09.005 CrossRef Lawson EA, Miller KK, Bredella MA, Phan C, Misra M, Meenaghan E, Rosenblum L, Donoho D, Gupta R, Klibanski A (2010) Hormone predictors of abnormal bone microarchitecture in women with anorexia nervosa. Bone 46(2):458–463. doi:10.​1016/​j.​bone.​2009.​09.​005 CrossRef
44.
go back to reference Solmi M, Veronese N, Correll CU, Favaro A, Santonastaso P, Caregaro L, Vancampfort D, Luchini C, De Hert M, Stubbs B (2016) Bone mineral density, osteoporosis, and fractures among people with eating disorders: a systematic review and meta-analysis. Acta Psychiatr Scand 133(5):341–351. doi:10.1111/acps.12556 CrossRef Solmi M, Veronese N, Correll CU, Favaro A, Santonastaso P, Caregaro L, Vancampfort D, Luchini C, De Hert M, Stubbs B (2016) Bone mineral density, osteoporosis, and fractures among people with eating disorders: a systematic review and meta-analysis. Acta Psychiatr Scand 133(5):341–351. doi:10.​1111/​acps.​12556 CrossRef
45.
go back to reference Misra M, Katzman DK, Cord J, Manning SJ, Mendes N, Herzog DB, Miller KK, Klibanski A (2008) Bone metabolism in adolescent boys with anorexia nervosa. J Clin Endocrinol Metab 93(8):3029–3036. doi:10.1210/jc.2008-0170 CrossRef Misra M, Katzman DK, Cord J, Manning SJ, Mendes N, Herzog DB, Miller KK, Klibanski A (2008) Bone metabolism in adolescent boys with anorexia nervosa. J Clin Endocrinol Metab 93(8):3029–3036. doi:10.​1210/​jc.​2008-0170 CrossRef
47.
go back to reference Lawson EA, Donoho D, Miller KK, Misra M, Meenaghan E, Lydecker J, Wexler T, Herzog DB, Klibanski A (2009) Hypercortisolemia is associated with severity of bone loss and depression in hypothalamic amenorrhea and anorexia nervosa. J Clin Endocrinol Metab 94(12):4710–4716. doi:10.1210/jc.2009-1046 CrossRef Lawson EA, Donoho D, Miller KK, Misra M, Meenaghan E, Lydecker J, Wexler T, Herzog DB, Klibanski A (2009) Hypercortisolemia is associated with severity of bone loss and depression in hypothalamic amenorrhea and anorexia nervosa. J Clin Endocrinol Metab 94(12):4710–4716. doi:10.​1210/​jc.​2009-1046 CrossRef
48.
go back to reference Misra M, Miller KK, Cord J, Prabhakaran R, Herzog DB, Goldstein M, Katzman DK, Klibanski A (2007) Relationships between serum adipokines, insulin levels, and bone density in girls with anorexia nervosa. J Clin Endocrinol Metab 92(6):2046–2052. doi:10.1210/jc.2006-2855 CrossRef Misra M, Miller KK, Cord J, Prabhakaran R, Herzog DB, Goldstein M, Katzman DK, Klibanski A (2007) Relationships between serum adipokines, insulin levels, and bone density in girls with anorexia nervosa. J Clin Endocrinol Metab 92(6):2046–2052. doi:10.​1210/​jc.​2006-2855 CrossRef
49.
go back to reference Young N, Formica C, Szmukler G, Seeman E (1994) Bone density at weight-bearing and nonweight-bearing sites in ballet dancers: the effects of exercise, hypogonadism, and body weight. J Clin Endocrinol Metab 78(2):449–454. doi:10.1210/jcem.78.2.8106634 Young N, Formica C, Szmukler G, Seeman E (1994) Bone density at weight-bearing and nonweight-bearing sites in ballet dancers: the effects of exercise, hypogonadism, and body weight. J Clin Endocrinol Metab 78(2):449–454. doi:10.​1210/​jcem.​78.​2.​8106634
50.
go back to reference Robinson TL, Snow-Harter C, Taaffe DR, Gillis D, Shaw J, Marcus R (1995) Gymnasts exhibit higher bone mass than runners despite similar prevalence of amenorrhea and oligomenorrhea. J Bone Miner Res 10(1):26–35. doi:10.1002/jbmr.5650100107 CrossRef Robinson TL, Snow-Harter C, Taaffe DR, Gillis D, Shaw J, Marcus R (1995) Gymnasts exhibit higher bone mass than runners despite similar prevalence of amenorrhea and oligomenorrhea. J Bone Miner Res 10(1):26–35. doi:10.​1002/​jbmr.​5650100107 CrossRef
51.
go back to reference Talbott SM, Shapses SA (1998) Fasting and energy intake influence bone turnover in lightweight male rowers. Int J Sport Nutr 8(4):377–387CrossRef Talbott SM, Shapses SA (1998) Fasting and energy intake influence bone turnover in lightweight male rowers. Int J Sport Nutr 8(4):377–387CrossRef
52.
go back to reference Nishiyama S, Tomoeda S, Ohta T, Higuchi A, Matsuda I (1988) Differences in basal and postexercise osteocalcin levels in athletic and nonathletic humans. Calcif Tissue Int 43(3):150–154CrossRef Nishiyama S, Tomoeda S, Ohta T, Higuchi A, Matsuda I (1988) Differences in basal and postexercise osteocalcin levels in athletic and nonathletic humans. Calcif Tissue Int 43(3):150–154CrossRef
53.
go back to reference Singhal V, de Lourdes Eguiguren M, Eisenbach L, Clarke H, Slattery M, Eddy K, Ackerman KE, Misra M (2014) Body composition, hemodynamic, and biochemical parameters of young female normal-weight oligo-amenorrheic and eumenorrheic athletes and nonathletes. Ann Nutrition Metab 65(4):264–271. doi:10.1159/000366024 CrossRef Singhal V, de Lourdes Eguiguren M, Eisenbach L, Clarke H, Slattery M, Eddy K, Ackerman KE, Misra M (2014) Body composition, hemodynamic, and biochemical parameters of young female normal-weight oligo-amenorrheic and eumenorrheic athletes and nonathletes. Ann Nutrition Metab 65(4):264–271. doi:10.​1159/​000366024 CrossRef
55.
56.
go back to reference Thomas DM, Udagawa N, Hards DK, Quinn JM, Moseley JM, Findlay DM, Best JD (1998) Insulin receptor expression in primary and cultured osteoclast-like cells. Bone 23(3):181–186CrossRef Thomas DM, Udagawa N, Hards DK, Quinn JM, Moseley JM, Findlay DM, Best JD (1998) Insulin receptor expression in primary and cultured osteoclast-like cells. Bone 23(3):181–186CrossRef
57.
go back to reference Cornish J, Callon KE, Reid IR (1996) Insulin increases histomorphometric indices of bone formation In vivo. Calcif Tissue Int 59(6):492–495CrossRef Cornish J, Callon KE, Reid IR (1996) Insulin increases histomorphometric indices of bone formation In vivo. Calcif Tissue Int 59(6):492–495CrossRef
58.
go back to reference Bjarnason NH, Henriksen EE, Alexandersen P, Christgau S, Henriksen DB, Christiansen C (2002) Mechanism of circadian variation in bone resorption. Bone 30(1):307–313CrossRef Bjarnason NH, Henriksen EE, Alexandersen P, Christgau S, Henriksen DB, Christiansen C (2002) Mechanism of circadian variation in bone resorption. Bone 30(1):307–313CrossRef
60.
go back to reference Prouteau S, Benhamou L, Courteix D (2006) Relationships between serum leptin and bone markers during stable weight, weight reduction and weight regain in male and female judoists. Eur J Endocrinol 154(3):389–395. doi:10.1530/eje.1.02103 CrossRef Prouteau S, Benhamou L, Courteix D (2006) Relationships between serum leptin and bone markers during stable weight, weight reduction and weight regain in male and female judoists. Eur J Endocrinol 154(3):389–395. doi:10.​1530/​eje.​1.​02103 CrossRef
61.
go back to reference Hickey MS, Houmard JA, Considine RV, Tyndall GL, Midgette JB, Gavigan KE, Weidner ML, McCammon MR, Israel RG, Caro JF (1997) Gender-dependent effects of exercise training on serum leptin levels in humans. Am J Physiol 272(4 Pt 1):E562–E566 Hickey MS, Houmard JA, Considine RV, Tyndall GL, Midgette JB, Gavigan KE, Weidner ML, McCammon MR, Israel RG, Caro JF (1997) Gender-dependent effects of exercise training on serum leptin levels in humans. Am J Physiol 272(4 Pt 1):E562–E566
62.
go back to reference Dubuc GR, Phinney SD, Stern JS, Havel PJ (1998) Changes of serum leptin and endocrine and metabolic parameters after 7 days of energy restriction in men and women. Metabolism 47(4):429–434CrossRef Dubuc GR, Phinney SD, Stern JS, Havel PJ (1998) Changes of serum leptin and endocrine and metabolic parameters after 7 days of energy restriction in men and women. Metabolism 47(4):429–434CrossRef
63.
go back to reference Robbeson JGH-NL, Wright HH (2013) The female athlete triad in student track and field athletes. S Afr J Clin Nutr 26(2):19–24CrossRef Robbeson JGH-NL, Wright HH (2013) The female athlete triad in student track and field athletes. S Afr J Clin Nutr 26(2):19–24CrossRef
64.
go back to reference Goodwin YMM, De Ridder JH, Boit MK, Mwangi FM, Wachira JL, Mwihaki MG, Toriola AL (2014) Profile of the female athlete triad among elite Kenyan endurance athletes and non-athletes: sport science and medicine. Afr J Phys Health Educ Recr Dance 20(22):610–625 Goodwin YMM, De Ridder JH, Boit MK, Mwangi FM, Wachira JL, Mwihaki MG, Toriola AL (2014) Profile of the female athlete triad among elite Kenyan endurance athletes and non-athletes: sport science and medicine. Afr J Phys Health Educ Recr Dance 20(22):610–625
65.
go back to reference Melin A, Tornberg AB, Skouby S, Moller SS, Sundgot-Borgen J, Faber J, Sidelmann JJ, Aziz M, Sjodin A (2015) Energy availability and the female athlete triad in elite endurance athletes. Scand J Med Sci Sports 25(5):610–622. doi:10.1111/sms.12261 CrossRef Melin A, Tornberg AB, Skouby S, Moller SS, Sundgot-Borgen J, Faber J, Sidelmann JJ, Aziz M, Sjodin A (2015) Energy availability and the female athlete triad in elite endurance athletes. Scand J Med Sci Sports 25(5):610–622. doi:10.​1111/​sms.​12261 CrossRef
66.
go back to reference 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. doi:10.1097/JSM.0b013e3181b8c136 CrossRef 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. doi:10.​1097/​JSM.​0b013e3181b8c136​ CrossRef
68.
go back to reference De Souza MJ, West SL, Jamal SA, Hawker GA, Gundberg CM, Williams NI (2008) The presence of both an energy deficiency and estrogen deficiency exacerbate alterations of bone metabolism in exercising women. Bone 43(1):140–148. doi:10.1016/j.bone.2008.03.013 CrossRef De Souza MJ, West SL, Jamal SA, Hawker GA, Gundberg CM, Williams NI (2008) The presence of both an energy deficiency and estrogen deficiency exacerbate alterations of bone metabolism in exercising women. Bone 43(1):140–148. doi:10.​1016/​j.​bone.​2008.​03.​013 CrossRef
69.
go back to reference Southmayd EA, Mallinson RJ, Williams NI, Mallinson DJ, De Souza MJ (2017) Unique effects of energy versus estrogen deficiency on multiple components of bone strength in exercising women. Osteoporos Int 28(4):1365–1376. doi:10.1007/s00198-016-3887-x CrossRef Southmayd EA, Mallinson RJ, Williams NI, Mallinson DJ, De Souza MJ (2017) Unique effects of energy versus estrogen deficiency on multiple components of bone strength in exercising women. Osteoporos Int 28(4):1365–1376. doi:10.​1007/​s00198-016-3887-x CrossRef
70.
go back to reference Wilson G, Hill J, Sale C, Morton JP, Close GL (2015) Elite male Flat jockeys display lower bone density and lower resting metabolic rate than their female counterparts: implications for athlete welfare. Appl Physiol Nutr Metab 40(12):1318–1320. doi:10.1139/apnm-2015-0354 CrossRef Wilson G, Hill J, Sale C, Morton JP, Close GL (2015) Elite male Flat jockeys display lower bone density and lower resting metabolic rate than their female counterparts: implications for athlete welfare. Appl Physiol Nutr Metab 40(12):1318–1320. doi:10.​1139/​apnm-2015-0354 CrossRef
71.
go back to reference Zanker CL, Swaine IL (1998) Relation between bone turnover, oestradiol, and energy balance in women distance runners. Br J Sports Med 32(2):167–171CrossRef Zanker CL, Swaine IL (1998) Relation between bone turnover, oestradiol, and energy balance in women distance runners. Br J Sports Med 32(2):167–171CrossRef
72.
go back to reference Leydon MA, Wall C (2002) New Zealand jockeys’ dietary habits and their potential impact on health. Int J Sport Nutr Exerc Metab 12(2):220–237CrossRef Leydon MA, Wall C (2002) New Zealand jockeys’ dietary habits and their potential impact on health. Int J Sport Nutr Exerc Metab 12(2):220–237CrossRef
73.
go back to reference Moore JM, Timperio AF, Crawford DA, Burns CM, Cameron-Smith D (2002) Weight management and weight loss strategies of professional jockeys. Int J Sport Nutr Exerc Metab 12(1):1–13CrossRef Moore JM, Timperio AF, Crawford DA, Burns CM, Cameron-Smith D (2002) Weight management and weight loss strategies of professional jockeys. Int J Sport Nutr Exerc Metab 12(1):1–13CrossRef
75.
go back to reference Warrington G, Dolan E, McGoldrick A, McEvoy J, Macmanus C, Griffin M, Lyons D (2009) Chronic weight control impacts on physiological function and bone health in elite jockeys. J Sports Sci 27(6):543–550. doi:10.1080/02640410802702863 CrossRef Warrington G, Dolan E, McGoldrick A, McEvoy J, Macmanus C, Griffin M, Lyons D (2009) Chronic weight control impacts on physiological function and bone health in elite jockeys. J Sports Sci 27(6):543–550. doi:10.​1080/​0264041080270286​3 CrossRef
76.
go back to reference Greene DA, Naughton GA, Jander CB, Cullen SJ (2013) Bone health of apprentice jockeys using peripheral quantitative computed tomography. Int J Sports Med 34(8):688–694. doi:10.1055/s-0032-1333213 CrossRef Greene DA, Naughton GA, Jander CB, Cullen SJ (2013) Bone health of apprentice jockeys using peripheral quantitative computed tomography. Int J Sports Med 34(8):688–694. doi:10.​1055/​s-0032-1333213 CrossRef
77.
go back to reference Wilson G, Drust B, Morton JP, Close GL (2014) Weight-making strategies in professional jockeys: implications for physical and mental health and well-being. Sports Med 44(6):785–796. doi:10.1007/s40279-014-0169-7 CrossRef Wilson G, Drust B, Morton JP, Close GL (2014) Weight-making strategies in professional jockeys: implications for physical and mental health and well-being. Sports Med 44(6):785–796. doi:10.​1007/​s40279-014-0169-7 CrossRef
78.
go back to reference Dolan E, Swinton P, Sale C, Healy A, O’Reilly J (2017) Does adipose tissue mass positively or negatively influence bone mass in an overweight or obese population? A systematic review and meta-analysis. Nutr Rev (in press) Dolan E, Swinton P, Sale C, Healy A, O’Reilly J (2017) Does adipose tissue mass positively or negatively influence bone mass in an overweight or obese population? A systematic review and meta-analysis. Nutr Rev (in press)
80.
go back to reference Nelson LR, Bulun SE (2001) Estrogen production and action. J Am Acad Dermatol 45(3 Suppl):S116–S124CrossRef Nelson LR, Bulun SE (2001) Estrogen production and action. J Am Acad Dermatol 45(3 Suppl):S116–S124CrossRef
81.
go back to reference Christo K, Prabhakaran R, Lamparello B, Cord J, Miller KK, Goldstein MA, Gupta N, Herzog DB, Klibanski A, Misra M (2008) Bone metabolism in adolescent athletes with amenorrhea, athletes with eumenorrhea, and control subjects. Pediatrics 121(6):1127–1136. doi:10.1542/peds.2007-2392 CrossRef Christo K, Prabhakaran R, Lamparello B, Cord J, Miller KK, Goldstein MA, Gupta N, Herzog DB, Klibanski A, Misra M (2008) Bone metabolism in adolescent athletes with amenorrhea, athletes with eumenorrhea, and control subjects. Pediatrics 121(6):1127–1136. doi:10.​1542/​peds.​2007-2392 CrossRef
82.
go back to reference 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. doi:10.1249/01.MSS.0000064935.68277.E7 CrossRef 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. doi:10.​1249/​01.​MSS.​0000064935.​68277.​E7 CrossRef
84.
go back to reference Stacey E, Korkia P, Hukkanen MV, Polak JM, Rutherford OM (1998) Decreased nitric oxide levels and bone turnover in amenorrheic athletes with spinal osteopenia. J Clin Endocrinol Metab 83(9):3056–3061. doi:10.1210/jcem.83.9.5106 Stacey E, Korkia P, Hukkanen MV, Polak JM, Rutherford OM (1998) Decreased nitric oxide levels and bone turnover in amenorrheic athletes with spinal osteopenia. J Clin Endocrinol Metab 83(9):3056–3061. doi:10.​1210/​jcem.​83.​9.​5106
85.
go back to reference Mitchell DM, Tuck P, Ackerman KE, Cano Sokoloff N, Woolley R, Slattery M, Lee H, Bouxsein ML, Misra M (2015) Altered trabecular bone morphology in adolescent and young adult athletes with menstrual dysfunction. Bone 81:24–30. doi:10.1016/j.bone.2015.06.021 CrossRef Mitchell DM, Tuck P, Ackerman KE, Cano Sokoloff N, Woolley R, Slattery M, Lee H, Bouxsein ML, Misra M (2015) Altered trabecular bone morphology in adolescent and young adult athletes with menstrual dysfunction. Bone 81:24–30. doi:10.​1016/​j.​bone.​2015.​06.​021 CrossRef
86.
go back to reference Kaufman BA, Warren MP, Dominguez JE, Wang J, Heymsfield SB, Pierson RN (2002) Bone density and amenorrhea in ballet dancers are related to a decreased resting metabolic rate and lower leptin levels. J Clin Endocrinol Metab 87(6):2777–2783. doi:10.1210/jcem.87.6.8565 CrossRef Kaufman BA, Warren MP, Dominguez JE, Wang J, Heymsfield SB, Pierson RN (2002) Bone density and amenorrhea in ballet dancers are related to a decreased resting metabolic rate and lower leptin levels. J Clin Endocrinol Metab 87(6):2777–2783. doi:10.​1210/​jcem.​87.​6.​8565 CrossRef
87.
go back to reference Dotti A, Fioravanti M, Balotta M, Tozzi F, Cannella C, Lazzari R (2002) Eating behavior of ballet dancers. Eat Weight Disord 7(1):60–67CrossRef Dotti A, Fioravanti M, Balotta M, Tozzi F, Cannella C, Lazzari R (2002) Eating behavior of ballet dancers. Eat Weight Disord 7(1):60–67CrossRef
89.
go back to reference Viner RT, Harris M, Berning JR, Meyer NL (2015) Energy availability and dietary patterns of adult male and female competitive cyclists with lower than expected bone mineral density. Int J Sport Nutr Exerc Metab 25(6):594–602. doi:10.1123/ijsnem.2015-0073 CrossRef Viner RT, Harris M, Berning JR, Meyer NL (2015) Energy availability and dietary patterns of adult male and female competitive cyclists with lower than expected bone mineral density. Int J Sport Nutr Exerc Metab 25(6):594–602. doi:10.​1123/​ijsnem.​2015-0073 CrossRef
91.
go back to reference Fogelholm M (1994) Effects of bodyweight reduction on sports performance. Sports Med 18(4):249–267CrossRef Fogelholm M (1994) Effects of bodyweight reduction on sports performance. Sports Med 18(4):249–267CrossRef
92.
go back to reference Trutschnigg B, Chong C, Habermayerova L, Karelis AD, Komorowski J (2008) Female boxers have high bone mineral density despite low body fat mass, high energy expenditure, and a high incidence of oligomenorrhea. Appl Physiol Nutr Metab 33(5):863–869. doi:10.1139/H08-071 CrossRef Trutschnigg B, Chong C, Habermayerova L, Karelis AD, Komorowski J (2008) Female boxers have high bone mineral density despite low body fat mass, high energy expenditure, and a high incidence of oligomenorrhea. Appl Physiol Nutr Metab 33(5):863–869. doi:10.​1139/​H08-071 CrossRef
94.
go back to reference 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 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
95.
go back to reference Klentrou P, Plyley M (2003) Onset of puberty, menstrual frequency, and body fat in elite rhythmic gymnasts compared with normal controls. Br J Sports Med 37(6):490–494CrossRef Klentrou P, Plyley M (2003) Onset of puberty, menstrual frequency, and body fat in elite rhythmic gymnasts compared with normal controls. Br J Sports Med 37(6):490–494CrossRef
96.
go back to reference Tenforde AS, Carlson JL, Chang A, Sainani KL, Shultz R, Kim JH, Cutti P, Golden NH, Fredericson M (2017) Association of the Female Athlete Triad risk assessment stratification to the development of bone stress injuries in collegiate athletes. Am J Sports Med 45(2):302–310. doi:10.1177/0363546516676262 CrossRef Tenforde AS, Carlson JL, Chang A, Sainani KL, Shultz R, Kim JH, Cutti P, Golden NH, Fredericson M (2017) Association of the Female Athlete Triad risk assessment stratification to the development of bone stress injuries in collegiate athletes. Am J Sports Med 45(2):302–310. doi:10.​1177/​0363546516676262​ CrossRef
97.
go back to reference Bergouignan A, Momken I, Schoeller DA, Normand S, Zahariev A, Lescure B, Simon C, Blanc S (2010) Regulation of energy balance during long-term physical inactivity induced by bed rest with and without exercise training. J Clin Endocrinol Metab 95(3):1045–1053. doi:10.1210/jc.2009-1005 CrossRef Bergouignan A, Momken I, Schoeller DA, Normand S, Zahariev A, Lescure B, Simon C, Blanc S (2010) Regulation of energy balance during long-term physical inactivity induced by bed rest with and without exercise training. J Clin Endocrinol Metab 95(3):1045–1053. doi:10.​1210/​jc.​2009-1005 CrossRef
98.
99.
go back to reference Kinzig KP, Coughlin JW, Redgrave GW, Moran TH, Guarda AS (2007) Insulin, glucose, and pancreatic polypeptide responses to a test meal in restricting type anorexia nervosa before and after weight restoration. Am J Physiol Endocrinol Metab 292(5):E1441–E1446. doi:10.1152/ajpendo.00347.2006 CrossRef Kinzig KP, Coughlin JW, Redgrave GW, Moran TH, Guarda AS (2007) Insulin, glucose, and pancreatic polypeptide responses to a test meal in restricting type anorexia nervosa before and after weight restoration. Am J Physiol Endocrinol Metab 292(5):E1441–E1446. doi:10.​1152/​ajpendo.​00347.​2006 CrossRef
100.
101.
go back to reference Barrack MT, Rauh MJ, Barkai HS, Nichols JF (2008) Dietary restraint and low bone mass in female adolescent endurance runners. Am J Clin Nutr 87(1):36–43CrossRef Barrack MT, Rauh MJ, Barkai HS, Nichols JF (2008) Dietary restraint and low bone mass in female adolescent endurance runners. Am J Clin Nutr 87(1):36–43CrossRef
104.
go back to reference Heaney RP, Layman DK (2008) Amount and type of protein influences bone health. Am J Clin Nutr 87(5):1567S–1570SCrossRef Heaney RP, Layman DK (2008) Amount and type of protein influences bone health. Am J Clin Nutr 87(5):1567S–1570SCrossRef
105.
go back to reference Krieger NS, Frick KK, Bushinsky DA (2004) Mechanism of acid-induced bone resorption. Curr Opin Nephrol Hypertens 13(4):423–436CrossRef Krieger NS, Frick KK, Bushinsky DA (2004) Mechanism of acid-induced bone resorption. Curr Opin Nephrol Hypertens 13(4):423–436CrossRef
106.
go back to reference Heer M, Baecker N, Frings-Meuthen P, Graf S, Zwart SR, Biolo G, Smith SM (2017) Effects of high-protein intake on bone turnover in long-term bed rest in women. Appl Physiol Nutr Metab 42(5):537–546. doi:10.1139/apnm-2016-0292 CrossRef Heer M, Baecker N, Frings-Meuthen P, Graf S, Zwart SR, Biolo G, Smith SM (2017) Effects of high-protein intake on bone turnover in long-term bed rest in women. Appl Physiol Nutr Metab 42(5):537–546. doi:10.​1139/​apnm-2016-0292 CrossRef
107.
go back to reference Mangano KM, Sahni S, Kerstetter JE (2014) Dietary protein is beneficial to bone health under conditions of adequate calcium intake: an update on clinical research. Curr Opin Clin Nutr Metab Care 17(1):69–74. doi:10.1097/MCO.0000000000000013 Mangano KM, Sahni S, Kerstetter JE (2014) Dietary protein is beneficial to bone health under conditions of adequate calcium intake: an update on clinical research. Curr Opin Clin Nutr Metab Care 17(1):69–74. doi:10.​1097/​MCO.​0000000000000013​
108.
go back to reference Josse AR, Atkinson SA, Tarnopolsky MA, Phillips SM (2012) Diets higher in dairy foods and dietary protein support bone health during diet- and exercise-induced weight loss in overweight and obese premenopausal women. J Clin Endocrinol Metab 97(1):251–260. doi:10.1210/jc.2011-2165 CrossRef Josse AR, Atkinson SA, Tarnopolsky MA, Phillips SM (2012) Diets higher in dairy foods and dietary protein support bone health during diet- and exercise-induced weight loss in overweight and obese premenopausal women. J Clin Endocrinol Metab 97(1):251–260. doi:10.​1210/​jc.​2011-2165 CrossRef
109.
go back to reference La Bounty PM, Campbell BI, Wilson J, Galvan E, Berardi J, Kleiner SM, Kreider RB, Stout JR, Ziegenfuss T, Spano M, Smith A, Antonio J (2011) International Society of Sports Nutrition position stand: meal frequency. J Int Soc Sports Nutr 8:4. doi:10.1186/1550-2783-8-4 CrossRef La Bounty PM, Campbell BI, Wilson J, Galvan E, Berardi J, Kleiner SM, Kreider RB, Stout JR, Ziegenfuss T, Spano M, Smith A, Antonio J (2011) International Society of Sports Nutrition position stand: meal frequency. J Int Soc Sports Nutr 8:4. doi:10.​1186/​1550-2783-8-4 CrossRef
110.
go back to reference Iwao S, Mori K, Sato Y (1996) Effects of meal frequency on body composition during weight control in boxers. Scand J Med Sci Sports 6(5):265–272CrossRef Iwao S, Mori K, Sato Y (1996) Effects of meal frequency on body composition during weight control in boxers. Scand J Med Sci Sports 6(5):265–272CrossRef
111.
go back to reference Li F, Muhlbauer RC (1999) Food fractionation is a powerful tool to increase bone mass in growing rats and to decrease bone loss in aged rats: modulation of the effect by dietary phosphate. J Bone Miner Res 14(8):1457–1465. doi:10.1359/jbmr.1999.14.8.1457 CrossRef Li F, Muhlbauer RC (1999) Food fractionation is a powerful tool to increase bone mass in growing rats and to decrease bone loss in aged rats: modulation of the effect by dietary phosphate. J Bone Miner Res 14(8):1457–1465. doi:10.​1359/​jbmr.​1999.​14.​8.​1457 CrossRef
112.
go back to reference Manore MM (2002) Dietary recommendations and athletic menstrual dysfunction. Sports Med 32(14):887–901CrossRef Manore MM (2002) Dietary recommendations and athletic menstrual dysfunction. Sports Med 32(14):887–901CrossRef
114.
go back to reference Sunyecz JA (2008) The use of calcium and vitamin D in the management of osteoporosis. Ther Clin Risk Manag 4(4):827–836CrossRef Sunyecz JA (2008) The use of calcium and vitamin D in the management of osteoporosis. Ther Clin Risk Manag 4(4):827–836CrossRef
116.
go back to reference Lee SK, Gardner AE, Kalinowski JF, Jastrzebski SL, Lorenzo JA (2006) RANKL-stimulated osteoclast-like cell formation in vitro is partially dependent on endogenous interleukin-1 production. Bone 38(5):678–685. doi:10.1016/j.bone.2005.10.011 CrossRef Lee SK, Gardner AE, Kalinowski JF, Jastrzebski SL, Lorenzo JA (2006) RANKL-stimulated osteoclast-like cell formation in vitro is partially dependent on endogenous interleukin-1 production. Bone 38(5):678–685. doi:10.​1016/​j.​bone.​2005.​10.​011 CrossRef
117.
go back to reference Sheweita SA, Khoshhal KI (2007) Calcium metabolism and oxidative stress in bone fractures: role of antioxidants. Curr Drug Metab 8(5):519–525CrossRef Sheweita SA, Khoshhal KI (2007) Calcium metabolism and oxidative stress in bone fractures: role of antioxidants. Curr Drug Metab 8(5):519–525CrossRef
Metadata
Title
Reduced energy availability: implications for bone health in physically active populations
Authors
Maria Papageorgiou
Eimear Dolan
Kirsty J. Elliott-Sale
Craig Sale
Publication date
01-04-2018
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 3/2018
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-017-1498-8

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