Mountjoy M, Sundgot-Borgen J, Burke L, Carter S, Constantini N, Lebrun C, et al. The IOC consensus statement: beyond the Female Athlete Triad-Relative Energy Deficiency in Sport (RED-S). Br J Sports Med. 2014;48:491–7.
Burke LM, Kiens B, Ivy JL. Carbohydrates and fat for training and recovery. J Sports Sci. 2004;22:15–30. https://doi.org/10.1080/0264041031000140527.
Loucks AB, Kiens B, Wright HH. Energy availability in athletes. J Sports Sci. 2011;29(Suppl 1):S7–15.
De Souza MJ, Nattiv A, Joy E, Misra M, Williams NI, Mallinson RJ, et al. 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. M Br J Sports Med. 2014;48:289.
Heikura IA, Uusitalo ALT, Stellingwerff T, Bergland D, Mero AA, Burke LM. Low energy availability is difficult to assess but outcomes have large impact on bone injury rates in elite distance athletes. Int J Sport Nutr Exerc Metab. 2018;28:403–11.
Loucks AB, Thuma JR. Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. J Clin Endocrinol Metab. 2003;88:297–311.
Koehler K, Hoerner NR, Gibbs JC, Zinner C, Braun H, De Souza MJ, et al. Low energy availability in exercising men is associated with reduced leptin and insulin but not with changes in other metabolic hormones. J Sports Sci. 2016;34:1921–9.
Elliott-Sale KJ, Tenforde AS, Parziale AL, Holtzman B, Ackerman KE. Endocrine effects of relative energy deficiency in sport. Int J Sport Nutr Exerc Metab [Internet]. 2018;28:335–49. Available from: https://journals.humankinetics.com/view/journals/ijsnem/28/4/article-p335.xml.
Chen XX, Yang T. Roles of leptin in bone metabolism and bone diseases. J Bone Miner Metab. 2015;33:474–85. https://doi.org/10.1007/s00774-014-0569-7.
Papageorgiou M, Elliott-Sale KJ, Parsons A, Tang JCY, Greeves JP, Fraser WD, et al. Effects of reduced energy availability on bone metabolism in women and men. Bone. 2017;105:191–9.
Tenforde AS, Nattiv A, Barrack M, Kraus E, Kim B, Kussman A, et al. Distribution of bone stress injuries in elite male and female collegiate runners. Med Sci Sport Exerc [Internet]. 2015;47:905. Available from: http://journals.lww.com/00005768-201505001-02795.
Bennell KL, Malcolm SA, Thomas SA, Wark JD, Brukner PD. The incidence and distribution of stress fractures in competitive track and field athletes: a twelve-month prospective study. Am J Sports Med. 1996;24:211–7.
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 Sport Exerc [Internet]. 2007;39:1457–63. Available from: https://insights.ovid.com/crossref?an=00005768-200709000-00003.
Duckham RL, Brooke-Wavell K, Summers GD, Cameron N, Peirce N. Stress fracture injury in female endurance athletes in the United Kingdom: a 12-month prospective study. Scand J Med Sci Sports. 2015;25:854–9. https://doi.org/10.1111/sms.12453.
Barrack MT, Gibbs JC, De Souza MJ, Williams NI, Nichols JF, Rauh MJ, et al. Higher incidence of bone stress injuries with increasing Female Athlete Triad-related risk factors. Am J Sports Med. 2014;42:949–58. https://doi.org/10.1177/0363546513520295.
Kraus E, Tenforde AS, Nattiv A, Sainani KL, Kussman A, Deakins-Roche M, et al. Bone stress injuries in male distance runners: higher modified Female Athlete Triad cumulative risk assessment scores predict increased rates of injury. Br J Sports Med. 2019;53:237–42. https://doi.org/10.1136/bjsports-2018-099861.
Williams NI, Helmreich DL, Parfitt DB, Caston-Balderrama A, Cameron JL. Evidence for a causal role of low energy availability in the induction of menstrual cycle disturbances during strenuous exercise training. J Clin Endocrinol Metab. 2001;86:5184–93.
Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP. American College of Sports Medicine position. stand The Female Athlete Triad. Med Sci Sports Exerc. 2007;39:1867–82.
Melin A, Tornberg ÅB, Skouby S, Møller SS, Sundgot-Borgen J, Faber J, et al. Energy availability and the Female Athlete Triad in elite endurance athletes. Scand J Med Sci Sports. 2015;25:610–22.
Dusek T. Influence of high intensity training on menstrual cycle disorders in athletes. Croat Med J. 2001;42:79–82.
Mitchell DM, Tuck P, Ackerman KE, Cano Sokoloff N, Woolley R, Slattery M, et al. Altered trabecular bone morphology in adolescent and young adult athletes with menstrual dysfunction. Bone. 2015;81:24–30.
Ackerman KE, Cano Sokoloff N, De Nardo Maffazioli G, Clarke HM, Lee H, Misra M. Fractures in relation to menstrual status and bone parameters in young athletes. Med Sci Sport Exerc [Internet]. 2015;47:1577–86. Available from: https://insights.ovid.com/crossref?an=00005768-201508000-00004.
Hart NH, Nimphius S, Rantalainen T, Ireland A, Siafarikas A, Newton RU. Mechanical basis of bone strength: influence of bone material, bone structure and muscle action. J Musculoskelet Neuronal Interact. 2017;17:114–39.
Kato T, Terashima T, Yamashita T, Hatanaka Y, Honda A, Umemura Y. Effect of low-repetition jump training on bone mineral density in young women. J Appl Physiol. 2006;100:839–43. https://doi.org/10.1152/japplphysiol.00666.2005.
Bennell KL, Malcolm SA, Thomas SA, Reid SJ, Brukner PD, Ebeling PR, et al. Risk factors for stress fractures in track and field athletes. Am J Sports Med. 1996;24:810–8. https://doi.org/10.1177/036354659602400617.
Nattiv A. Stress fractures and bone health in track and field athletes. J Sci Med Sport. 2000;3:268–79.
Nattiv A, Kennedy G, Barrack MT, Abdelkerim A, Goolsby MA, Arends JC, et al. Correlation of MRI grading of bone stress injuries with clinical risk factors and return to play. Am J Sports Med. 2013;41:1930–41. https://doi.org/10.1177/0363546513490645.
Tenforde AS, Kraus E, Fredericson M. Bone stress injuries in runners. Phys Med Rehabil Clin N Am. 2016;27:139–49.
Singhal V, Reyes KC, Pfister B, Ackerman K, Slattery M, Cooper K, et al. Bone accrual in oligo-amenorrheic athletes, eumenorrheic athletes and non-athletes. Bone. 2019;120:305–13.
Ackerman KE, Putman M, Guereca G, Taylor AP, Pierce L, Herzog DB, et al. Cortical microstructure and estimated bone strength in young amenorrheic athletes, eumenorrheic athletes and non-athletes. Bone. 2012;51:680–7.
Pollock N, Grogan C, Perry M, Pedlar C, Cooke K, Morrissey D, et al. Bone-mineral density and other features of the Female Athlete Triad in elite endurance runners: a longitudinal and cross-sectional observational study. Int J Sport Nutr Exerc Metab [Internet]. 2010;20:418–26. Available from: https://journals.humankinetics.com/view/journals/ijsnem/20/5/article-p418.xml.
Baxter-Jones AD, Faulkner RA, Forwood MR, Mirwald RL, Bailey DA. Bone mineral accrual from 8 to 30 years of age: an estimation of peak bone mass. J Bone Miner Res. 2011;26:1729–39. https://doi.org/10.1002/jbmr.412.
Burke LM, Lundy B, Fahrenholtz IL, Melin AK. Pitfalls of conducting and interpreting estimates of energy availability in free-living athletes. Int J Sport Nutr Exerc Metab. 2018;28:350–63.
Duckham RL, Peirce N, Bailey CA, Summers G, Cameron N, Brooke-Wavell K. Bone geometry according to menstrual function in female endurance athletes. Calcif Tissue Int. 2013;92:444–50. https://doi.org/10.1007/s00223-013-9700-3.
Ackerman KE, Nazem T, Chapko D, Russell M, Mendes N, Taylor AP, et al. Bone microarchitecture is impaired in adolescent amenorrheic athletes compared with eumenorrheic athletes and nonathletic controls. J Clin Endocrinol Metab [Internet]. 2011;96:3123–33. Available from: https://academic.oup.com/jcem/article/96/10/3123/2834899.
Piasecki J, Ireland A, Piasecki M, Cameron J, McPhee JS, Degens H. The strength of weight-bearing bones is similar in amenorrheic and eumenorrheic elite long-distance runners. Scand J Med Sci Sports. 2018;28:1559–68. https://doi.org/10.1111/sms.13062.
Lieberman JL, De Souza MJ, Wagstaff DA, Williams NI. Menstrual disruption with exercise is not linked to an energy availability threshold. Med Sci Sport Exerc. 2018;50:551–61.
De Souza MJ, Koltun KJ, Williams NI. The role of energy availability in reproductive function in the Female Athlete Triad and extension of its effects to men: an initial working model of a similar syndrome in male athletes. Sport Med. 2019;48(Suppl 2):S125-137. https://doi.org/10.1007/s40279-019-01217-3.
Hackney AC. Hypogonadism in exercising males: dysfunction or adaptive-regulatory adjustment? Front Endocrinol (Lausanne). 2020;11:11. https://doi.org/10.3389/fendo.2020.00011/full.
Logue DM, Madigan SM, Melin A, Delahunt E, Heinen M, Donnell S-JM, et al. Low energy availability in athletes 2020: an updated narrative review of prevalence, risk, within-day energy balance, knowledge, and impact on sports performance. Nutrients [Internet]. 2020;12:835. Available from: https://www.mdpi.com/2072-6643/12/3/835.
Tenforde AS, Barrack MT, Nattiv A, Fredericson M. Parallels with the Female Athlete Triad in male athletes. Sports Med. 2016;46:171–82.
Tenforde AS, Fredericson M, Sayres LC, Cutti P, Sainani KL. Identifying sex-specific risk factors for low bone mineral density in adolescent runners. Am J Sports Med. 2015;43:1494–504.
Mallinson RJ, Southmayd EA, De Souza MJ. Geometric and “true” densitometric characteristics of bones in athletes with stress fracture and menstrual disturbances: a systematic review. Sport Med. 2019;49:1059–78. https://doi.org/10.1007/s40279-019-01109-6.
Duckham RL, Bialo SR, Machan J, Kriz P, Gordon CM. A case-control pilot study of stress fracture in adolescent girls: the discriminative ability of two imaging technologies to classify at-risk athletes. Osteoporos Int. 2019;30:1573–80. https://doi.org/10.1007/s00198-019-05001-x.
Schnackenburg KE, Macdonald HM, Ferber R, Wiley JP, Boyd SK. Bone quality and muscle strength in female athletes with lower limb stress fractures. Med Sci Sport Exerc [Internet]. 2011;43:2110–9. Available from: http://journals.lww.com/00005768-201111000-00012.
Southmayd EA, Mallinson RJ, Williams NI, Mallinson DJ, De Souza MJ. Unique effects of energy versus estrogen deficiency on multiple components of bone strength in exercising women. Osteoporos Int. 2017;28:1365–76. https://doi.org/10.1007/s00198-016-3887-x.
Popp KL, Frye AC, Stovitz SD, Hughes JM. Bone geometry and lower extremity bone stress injuries in male runners. J Sci Med Sport. 2020;23:145–50.
Ackerman KE, Pierce L, Guereca G, Slattery M, Lee H, Goldstein M, et al. Hip structural analysis in adolescent and young adult oligoamenorrheic and eumenorrheic athletes and nonathletes. J Clin Endocrinol Metab [Internet]. 2013;98:1742–9. Available from: https://academic.oup.com/jcem/article/98/4/1742/2537074.
Beck T, Ruff C, Shaffer R, Betsinger K, Trone D, Brodine S. Stress fracture in military recruits: gender differences in muscle and bone susceptibility factors. Bone. 2000;27:437–44.
Ruffing JA, Nieves JW, Zion M, Tendy S, Garrett P, Lindsay R, et al. The influence of lifestyle, menstrual function and oral contraceptive use on bone mass and size in female military cadets. Nutr Metab (Lond). 2007;4:17. https://doi.org/10.1186/1743-7075-4-17.
Pistoia W, van Rietbergen B, Lochmüller E-M, Lill C, Eckstein F, Rüegsegger P. Estimation of distal radius failure load with micro-finite element analysis models based on three-dimensional peripheral quantitative computed tomography images. Bone. 2002;30:842–8.
Sale C, Elliott-Sale KJ. Nutrition and athlete bone health. Sport Med. 2019. https://doi.org/10.1007/s40279-019-01161-2.
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;43:140–8.
McGrath C, Sankaran JS, Misaghian-Xanthos N, Sen B, Xie Z, Styner MA, et al. Exercise degrades bone in caloric restriction, despite suppression of marrow adipose tissue (MAT). J Bone Miner Res. 2020;35:106–15.
Frost HM. Bone “mass” and the “mechanostat”: a proposal. Anat Rec. 1987;219:1–9. https://doi.org/10.1002/ar.1092190104.
Burr DB, Robling AG, Turner CH. Effects of biomechanical stress on bones in animals. Bone. 2002;30:781–6.
Rubin CT, Lanyon LE. Regulation of bone formation by applied dynamic loads. J Bone Joint Surg Am. 1984;66:397–402.
Vlachopoulos D, Barker AR, Ubago-Guisado E, Williams CA, Gracia-Marco L. A 9-month jumping intervention to improve bone geometry in adolescent male athletes. Med Sci Sport Exerc. 2018;50:2544–54.
Vlachopoulos D, Barker AR, Ubago-Guisado E, Williams CA, Gracia-Marco L. The effect of a high-impact jumping intervention on bone mass, bone stiffness and fitness parameters in adolescent athletes. Arch Osteoporos. 2018;13:128. https://doi.org/10.1007/s11657-018-0543-4.
Hinton PS, Nigh P, Thyfault J. Effectiveness of resistance training or jumping-exercise to increase bone mineral density in men with low bone mass: a 12-month randomized, clinical trial. Bone. 2015;79:203–12.
Fredericson M, Chew K, Ngo J, Cleek T, Kiratli J, Cobb K. Regional bone mineral density in male athletes: a comparison of soccer players, runners and controls. Br J Sports Med. 2007;41:664–8.
Niu K, Ahola R, Guo H, Korpelainen R, Uchimaru J, Vainionpää A, et al. Effect of office-based brief high-impact exercise on bone mineral density in healthy premenopausal women: the Sendai Bone Health Concept Study. J Bone Miner Metab. 2010;28:568–77. https://doi.org/10.1007/s00774-010-0163-6.
Bailey CA, Brooke-Wavell K. Optimum frequency of exercise for bone health: randomised controlled trial of a high-impact unilateral intervention. Bone. 2010;46:1043–9.
Heinonen A, Mäntynen J, Kannus P, Uusi-Rasi K, Nikander R, Kontulainen S, et al. Effects of high-impact training and detraining on femoral neck structure in premenopausal women: a hip structural analysis of an 18-month randomized controlled exercise intervention with 3.5-year follow-up. Physiother Canada. 2012;64:98–105. https://doi.org/10.3138/ptc.2010-37.
Petit MA, Mckay HA, Mackelvie KJ, Heinonen A, Khan KM, Beck TJ. A randomized school-based jumping intervention confers site and maturity-specific benefits on bone structural properties in girls: a hip structural analysis study. J Bone Miner Res. 2002;17:363–72. https://doi.org/10.1359/jbmr.2002.17.3.363.
Tucker LA, Strong JE, LeCheminant JD, Bailey BW. Effect of two jumping programs on hip bone mineral density in premenopausal women: a randomized controlled trial. Am J Health Promot. 2015;29:158–64. https://doi.org/10.4278/ajhp.130430-QUAN-200.
Suominen TH, Korhonen MT, Alén M, Heinonen A, Mero A, Törmäkangas T, et al. Effects of a 20-week high-intensity strength and sprint training program on tibial bone structure and strength in middle-aged and older male sprint athletes: a randomized controlled trial. Osteoporos Int. 2017;28:2663–73. https://doi.org/10.1007/s00198-017-4107-z.
Lambert C, Beck BR, Harding AT, Watson SL, Weeks BK. Regional changes in indices of bone strength of upper and lower limbs in response to high-intensity impact loading or high-intensity resistance training. Bone. 2020;132:115192.
Piasecki J, McPhee JS, Hannam K, Deere KC, Elhakeem A, Piasecki M, et al. Hip and spine bone mineral density are greater in master sprinters, but not endurance runners compared with non-athletic controls. Arch Osteoporos. 2018;13:72. https://doi.org/10.1007/s11657-018-0486-9.
Sundh D, Nilsson M, Zoulakis M, Pasco C, Yilmaz M, Kazakia GJ, et al. High-impact mechanical loading increases bone material strength in postmenopausal women-a 3-month intervention study. J Bone Miner Res. 2018;33:1242–51. https://doi.org/10.1002/jbmr.3431.
Hartley C, Folland JP, Kerslake R, Brooke-Wavell K. High-impact exercise increased femoral neck bone density with no adverse effects on imaging markers of knee osteoarthritis in postmenopausal women. J Bone Miner Res. 2020;35:53–63. https://doi.org/10.1002/jbmr.3867.
De Souza MJ, Williams NI. Beyond hypoestrogenism in amenorrheic athletes: energy deficiency as a contributing factor for bone loss. Curr Sports Med Rep. 2005;4:38–44.
Villareal DT. Bone mineral density response to caloric restriction–induced weight loss or exercise-induced weight loss. Arch Intern Med. 2006;166:2502. https://doi.org/10.1001/archinte.166.22.2502.
Seeman E. Bone quality: the material and structural basis of bone strength. J Bone Miner Metab. 2008;26:1–8. https://doi.org/10.1007/s00774-007-0793-5.
Judex S, Zernicke RF. High-impact exercise and growing bone: relation between high strain rates and enhanced bone formation. J Appl Physiol. 2000;88:2183–91.
Schipilow JD, Macdonald HM, Liphardt AM, Kan M, Boyd SK. Bone micro-architecture, estimated bone strength, and the muscle-bone interaction in elite athletes: an HR-pQCT study. Bone. 2013;56:281–9.
Vasikaran S, Eastell R, Bruyère O, Foldes AJ, Garnero P, Griesmacher A, et al. Markers of bone turnover for the prediction of fracture risk and monitoring of osteoporosis treatment: a need for international reference standards. Osteoporos Int. 2011;22:391–420. https://doi.org/10.1007/s00198-010-1501-1.
Zanker CL, Swaine IL. Responses of bone turnover markers to repeated endurance running in humans under conditions of energy balance or energy restriction. Eur J Appl Physiol. 2000;83:434–40. https://doi.org/10.1007/s004210000293.
Papageorgiou M, Martin D, Colgan H, Cooper S, Greeves JP, Tang JCY, et al. Bone metabolic responses to low energy availability achieved by diet or exercise in active eumenorrheic women. Bone. 2018;114:181–8.
Ihle R, Loucks AB. Dose–response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res. 2004;19:1231–40. https://doi.org/10.1359/JBMR.040410.
Hammond KM, Sale C, Fraser W, Tang J, Shepherd SO, Strauss JA, et al. Post-exercise carbohydrate and energy availability induce independent effects on skeletal muscle cell signalling and bone turnover: implications for training adaptation. J Physiol. 2019;597:4779–96. https://doi.org/10.1113/JP278209.
Bennell KL, Malcolm SA, Wark JD, Brukner PD. Models for the pathogenesis of stress fractures in athletes. Br J Sports Med. 1996;30:200–4. https://doi.org/10.1136/bjsm.30.3.200.
Schilcher J, Bernhardsson M, Aspenberg P. Chronic anterior tibial stress fractures in athletes: no crack but intense remodeling. Scand J Med Sci Sports. 2019;29:1521–8. https://doi.org/10.1111/sms.13466.
Bennell KL, Malcolm SA, Brukner PD, Green RM, Hopper JL, Wark JD, et al. A 12-month prospective study of the relationship between stress fractures and bone turnover in athletes. Calcif Tissue Int. 1998;63:80–5. https://doi.org/10.1007/s002239900493.
Yanovich R, Evans RK, Friedman E, Moran DS. Bone turnover markers do not predict stress fracture in elite combat recruits. Clin Orthop Relat Res. 2013;471:1365–72. https://doi.org/10.1007/s11999-012-2727-3.
Hlaing TT, Compston JE. Biochemical markers of bone turnover—uses and limitations. Ann Clin Biochem. 2014;51:189–202. https://doi.org/10.1177/0004563213515190.
Dolan E, Varley I, Ackerman KE, Pereira RMR, Elliott-Sale KJ, Sale C. The bone metabolic response to exercise and nutrition. Exerc Sport Sci Rev. 2020;48:49–58. https://doi.org/10.1249/JES.0000000000000215.
Kishimoto K, Lynch RP, Reiger J, Yingling VR. Short-term jump activity on bone metabolism in female college-aged nonathletes. J Sports Sci Med. 2012;11:31–8.
Martin SPK, Bachrach LK, Golden NH. Controlled pilot study of high-impact low-frequency exercise on bone loss and vital-sign stabilization in adolescents with eating disorders. J Adolesc Health. 2017;60:33–7.