Impact of Low Energy Availability on Skeletal Health in Physically Active Adults

Rizzoli R, Bianchi ML, Garabedian M, McKay HA, Moreno LA (2010) Maximizing bone mineral mass gain during growth for the prevention of fractures in the adolescents and the elderly. Bone 46:294–305 Fuchs RK, Bauer JJ, Snow CM (2001) Jumping improves hip and lumbar spine bone mass in prepubescent children: a randomized controlled trial. J Bone Miner Res 16:148–156 Baxter-Jones AD, Faulkner RA, Forwood MR, Mirwald RL, Bailey DA (2011) Bone mineral accrual from 8 to 30 years of age: an estimation of peak bone mass. J Bone Miner Res 26:1729–1739 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 39:1867–1882 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 48:491 Jones BH, Thacker SB, Gilchrist J, Kimsey CD Jr, Sosin DM (2002) Prevention of lower extremity stress fractures in athletes and soldiers: a systematic review. Epidemiol Rev 24:228–247 Mountjoy M, Sundgot-Borgen JK, Burke LM, Ackerman KE, Blauwet C, Constantini N, Lebrun C, Lundy B, Melin AK, Meyer NL, Sherman RT, Tenforde AS, Klungland Torstveit M, Budgett R (2018) IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update. Br J Sports Med 52:687–697 Nattiv A, De Souza MJ, Koltun KJ, Misra M, Kussman A, Williams NI, Barrack MT, Kraus E, Joy E, Fredericson M (2021) The male athlete triad-a consensus statement from the female and male athlete triad coalition part 1: definition and scientific basis. Clin J Sport Med 31:335–348 Nattiv A, Agostini R, Drinkwater B, Yeager KK (1994) The female athlete triad. The inter-relatedness of disordered eating, amenorrhea, and osteoporosis. Clin Sports Med 13:405–418 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 42:949–958 O’Leary TJ, Wardle SL, Greeves JP (2020) Energy deficiency in soldiers: the risk of the athlete triad and relative energy deficiency in sport syndromes in the military. Front Nutr 7:142 Burr DB, Forwood MR, Fyhrie DP, Martin RB, Schaffler MB, Turner CH (1997) Bone microdamage and skeletal fragility in osteoporotic and stress fractures. J Bone Miner Res 12:6–15 Hughes JM, Popp KL, Yanovich R, Bouxsein ML, Matheny RW Jr (2017) The role of adaptive bone formation in the etiology of stress fracture. Exp Biol Med (Maywood) 242:897–906 Warden SJ, Hurst JA, Sanders MS, Turner CH, Burr DB, Li J (2005) Bone adaptation to a mechanical loading program significantly increases skeletal fatigue resistance. J Bone Miner Res 20:809–816 Robertson GA, Wood AM (2015) Return to sports after stress fractures of the tibial diaphysis: a systematic review. Br Med Bull 114:95–111 Rizzone KH, Ackerman KE, Roos KG, Dompier TP, Kerr ZY (2017) The epidemiology of stress fractures in collegiate student-athletes, 2004–2005 through 2013–2014 academic years. J Athl Train 52:966–975 Saunier J, Chapurlat R (2018) Stress fracture in athletes. Joint Bone Spine 85:307–310 McDonnell LK, Hume PA, Nolte V (2011) Rib stress fractures among rowers: definition, epidemiology, mechanisms, risk factors and effectiveness of injury prevention strategies. Sports Med 41:883–901 Bennell KL, Malcolm SA, Thomas SA, Reid SJ, Brukner PD, Ebeling PR, Wark JD (1996) Risk factors for stress fractures in track and field athletes. A twelve-month prospective study. Am J Sports Med 24:810–818 Knapik J, Montain S, McGraw S, Grier T, Ely M, Jones B (2012) Stress fracture risk factors in basic combat training. Int J Sports Med 33:940–946 Waterman BR, Gun B, Bader JO, Orr JD, Belmont PJ Jr (2016) Epidemiology of lower extremity stress fractures in the United States Military. Mil Med 181:1308–1313 Beck B, Drysdale L (2021) Risk factors, diagnosis and management of bone stress injuries in adolescent athletes: a narrative review. Sports (Basel) 9:52 Kardouni JR, McKinnon CJ, Taylor KM, Hughes JM (2021) Timing of stress fracture in soldiers during the first 6 career months: a retrospective cohort study. J Athl Train 56:1278–1284 Milgrom C, Giladi M, Chisin R, Dizian R (1985) The long-term followup of soldiers with stress fractures. Am J Sports Med 13:398–400 Nattiv A, Kennedy G, Barrack MT, Abdelkerim A, Goolsby MA, Arends JC, Seeger LL (2013) Correlation of MRI grading of bone stress injuries with clinical risk factors and return to play: a 5-year prospective study in collegiate track and field athletes. Am J Sports Med 41:1930–1941 Ekstrand J, van Dijk CN (2013) Fifth metatarsal fractures among male professional footballers: a potential career-ending disease. Br J Sports Med 47:754–758 Popp KL, Ackerman KE, Rudolph SE, Johannesdottir F, Hughes JM, Tenforde AS, Bredella MA, Xu C, Unnikrishnan G, Reifman J, Bouxsein ML (2020) Changes in volumetric bone mineral density over 12 months after a tibial bone stress injury diagnosis: implications for return to sports and military duty. Am J Sports Med 49(1):226–235 Loucks AB (2004) Energy balance and body composition in sports and exercise. J Sports Sci 22:1–14 Loucks AB, Kiens B, Wright HH (2011) Energy availability in athletes. J Sports Sci 29(Suppl 1):S7-15 Ihle R, Loucks AB (2004) Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res 19:1231–1240 Loucks AB, Verdun M, Heath EM (1998) Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. J Appl Physiol 84:37–46 Myerson M, Gutin B, Warren MP, May MT, Contento I, Lee M, Pi-Sunyer FX, Pierson RN Jr, Brooks-Gunn J (1991) Resting metabolic rate and energy balance in amenorrheic and eumenorrheic runners. Med Sci Sports Exerc 23:15–22 Stubbs RJ, O’Reilly LM, Whybrow S, Fuller Z, Johnstone AM, Livingstone MB, Ritz P, Horgan GW (2014) Measuring the difference between actual and reported food intakes in the context of energy balance under laboratory conditions. Br J Nutr 111:2032–2043 Shephard RJ, Aoyagi Y (2012) Measurement of human energy expenditure, with particular reference to field studies: an historical perspective. Eur J Appl Physiol 112:2785–2815 Siddall AG, Powell SD, Needham-Beck SC, Edwards VC, Thompson JES, Kefyalew SS, Singh PA, Orford ER, Venables MC, Jackson S, Greeves JP, Blacker SD, Myers SD (2019) Validity of energy expenditure estimation methods during 10 days of military training. Scand J Med Sci Sports 29:1313–1321 Murakami H, Kawakami R, Nakae S, Nakata Y, Ishikawa-Takata K, Tanaka S, Miyachi M (2016) Accuracy of wearable devices for estimating total energy expenditure: comparison with metabolic chamber and doubly labeled water method. JAMA Intern Med 176:702–703 Braakhuis AJ, Meredith K, Cox GR, Hopkins WG, Burke LM (2003) Variability in estimation of self-reported dietary intake data from elite athletes resulting from coding by different sports dietitians. Int J Sport Nutr Exerc Metab 13:152–165 Heikura IA, Uusitalo ALT, Stellingwerff T, Bergland D, Mero AA, Burke LM (2018) 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 28:403–411 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:E29-39 Melin A, Tornberg AB, Skouby S, Faber J, Ritz C, Sjodin A, Sundgot-Borgen J (2014) The LEAF questionnaire: a screening tool for the identification of female athletes at risk for the female athlete triad. Br J Sports Med 48:540–545 Mond JM, Hay PJ, Rodgers B, Owen C, Beumont PJ (2004) Validity of the Eating Disorder Examination Questionnaire (EDE-Q) in screening for eating disorders in community samples. Behav Res Ther 42:551–567 Condo D, Lohman R, Kelly M, Carr A (2019) Nutritional intake, sports nutrition knowledge and energy availability in female australian rules football players. Nutrients 11:971 Civil R, Lamb A, Loosmore D, Ross L, Livingstone K, Strachan F, Dick JR, Stevenson EJ, Brown MA, Witard OC (2018) Assessment of dietary intake, energy status, and factors associated with RED-S in vocational female ballet students. Front Nutr 5:136 Brown MA, Howatson G, Quin E, Redding E, Stevenson EJ (2017) Energy intake and energy expenditure of pre-professional female contemporary dancers. PLoS ONE 12:e0171998 Zanders BR, Currier BS, Harty PS, Zabriskie HA, Smith CR, Stecker RA, Richmond SR, Jagim AR, Kerksick CM (2021) Changes in energy expenditure, dietary intake, and energy availability across an entire collegiate women’s basketball season. J Strength Cond Res 35:804–810 Zabriskie HA, Currier BS, Harty PS, Stecker RA, Jagim AR, Kerksick CM (2019) Energy status and body composition across a collegiate women’s lacrosse season. Nutrients 11:470 Redman LM, Loucks AB (2005) Menstrual disorders in athletes. Sports Med 35:747–755 Schneider MB, Fisher M, Friedman SB, Bijur PE, Toffler AP (1999) Menstrual and premenstrual issues in female military cadets: a unique population with significant concerns. J Pediatr Adolesc Gynecol 12:195–201 Papageorgiou M, Dolan E, Elliott-Sale KJ, Sale C (2018) Reduced energy availability: implications for bone health in physically active populations. Eur J Nutr 57:847–859 Loucks AB, Thuma JR (2003) Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. J Clin Endocrinol Metab 88:297–311 Filicori M, Tabarelli C, Casadio P, Ferlini F, Gessa G, Pocognoli P, Cognigni G, Pecorari R (1998) Interaction between menstrual cyclicity and gonadotropin pulsatility. Horm Res 49:169–172 Gordon CM, Ackerman KE, Berga SL, Kaplan JR, Mastorakos G, Misra M, Murad MH, Santoro NF, Warren MP (2017) Functional hypothalamic amenorrhea: an endocrine society clinical practice guideline. J Clin Endocrinol Metab 102:1413–1439 Lewis KJ, Cabahug-Zuckerman P, Boorman-Padgett JF, Basta-Pljakic J, Louie J, Stephen S, Spray DC, Thi MM, Seref-Ferlengez Z, Majeska RJ, Weinbaum S, Schaffler MB (2021) Estrogen depletion on In vivo osteocyte calcium signaling responses to mechanical loading. Bone 152:116072 Weitzmann MN, Pacifici R (2006) Estrogen deficiency and bone loss: an inflammatory tale. J Clin Invest 116:1186–1194 Allison H, Holdsworth G, McNamara LM (2020) Scl-Ab reverts pro-osteoclastogenic signalling and resorption in estrogen deficient osteocytes. BMC Mol Cell Biol 21:78 Drinkwater BL, Nilson K, Chesnut CH 3rd, Bremner WJ, Shainholtz S, Southworth MB (1984) Bone mineral content of amenorrheic and eumenorrheic athletes. N Engl J Med 311:277–281 Ackerman KE, Cano Sokoloff N, De Nardo MG, Clarke HM, Lee H, Misra M (2015) Fractures in relation to menstrual status and bone parameters in young athletes. Med Sci Sports Exerc 47:1577–1586 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 96:3123–3133 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 35:711–719 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 51:680–687 Lane AR, Hackney AC (2014) Reproductive dysfunction from the stress of exercise training is not gender specific: the “exercise-hypogonadal male condition.” J Endocrinol Diabetes 1(2):4 Mohamad NV, Soelaiman IN, Chin KY (2016) A concise review of testosterone and bone health. Clin Interv Aging 11:1317–1324 Hackney AC (2020) Hypogonadism in exercising males: dysfunction or adaptive-regulatory adjustment? Front Endocrinol (Lausanne) 11:11 Varanoske AN, Margolis LM, Pasiakos SM (2020) Effects of testosterone on serum concentrations, fat-free mass, and physical performance by population: a meta-analysis. J Endocr Soc 4:bvaa090 Nindl BC, Barnes BR, Alemany JA, Frykman PN, Shippee RL, Friedl KE (2007) Physiological consequences of U.S. Army Ranger training. Med Sci Sports Exerc 39:1380–1387 Bhasin S, Cunningham GR, Hayes FJ, Matsumoto AM, Snyder PJ, Swerdloff RS, Montori VM (2006) Testosterone therapy in adult men with androgen deficiency syndromes: an endocrine society clinical practice guideline. J Clin Endocrinol Metab 91:1995–2010 Hughes JM, Smith MA, Henning PC, Scofield DE, Spiering BA, Staab JS, Hydren JR, Nindl BC, Matheny RW Jr (2014) Bone formation is suppressed with multi-stressor military training. Eur J Appl Physiol 114:2251–2259 Vandenput L, Ohlsson C (2009) Estrogens as regulators of bone health in men. Nat Rev Endocrinol 5:437–443 Vandenput L, Ohlsson C (2010) Sex steroid metabolism in the regulation of bone health in men. J Steroid Biochem Mol Biol 121:582–588 Khosla S, Melton LJ 3rd, Robb RA, Camp JJ, Atkinson EJ, Oberg AL, Rouleau PA, Riggs BL (2005) Relationship of volumetric BMD and structural parameters at different skeletal sites to sex steroid levels in men. J Bone Miner Res 20:730–740 Ackerman KE, Skrinar GS, Medvedova E, Misra M, Miller KK (2012) Estradiol levels predict bone mineral density in male collegiate athletes: a pilot study. Clin Endocrinol (Oxf) 76:339–345 Falahati-Nini A, Riggs BL, Atkinson EJ, O’Fallon WM, Eastell R, Khosla S (2000) Relative contributions of testosterone and estrogen in regulating bone resorption and formation in normal elderly men. J Clin Invest 106:1553–1560 Zanker CL, Swaine IL (1998) Relation between bone turnover, oestradiol, and energy balance in women distance runners. Br J Sports Med 32:167–171 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 28:1365–1376 Guntur AR, Rosen CJ (2013) IGF-1 regulation of key signaling pathways in bone. Bonekey Rep 2:437 Chou SH, Chamberland JP, Liu X, Matarese G, Gao C, Stefanakis R, Brinkoetter MT, Gong H, Arampatzi K, Mantzoros CS (2011) Leptin is an effective treatment for hypothalamic amenorrhea. Proc Natl Acad Sci U S A 108:6585–6590 Combs CE, Nicholls JJ, Duncan Bassett JH, Williams GR (2011) Thyroid hormones and bone development. Minerva Endocrinol 36:71–85 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 23:181–186 Cornish J, Callon KE, Reid IR (1996) Insulin increases histomorphometric indices of bone formation In vivo. Calcif Tissue Int 59:492–495 Bjarnason NH, Henriksen EE, Alexandersen P, Christgau S, Henriksen DB, Christiansen C (2002) Mechanism of circadian variation in bone resorption. Bone 30:307–313 Upadhyay J, Farr OM, Mantzoros CS (2015) The role of leptin in regulating bone metabolism. Metabolism 64:105–113 Reed JL, De Souza MJ, Williams NI (2013) Changes in energy availability across the season in Division I female soccer players. J Sports Sci 31:314–324 Richmond VL, Horner FE, Wilkinson DM, Rayson MP, Wright A, Izard R (2014) Energy balance and physical demands during an 8-week arduous military training course. Mil Med 179:421–427 Tassone EC, Baker BA (2017) Body weight and body composition changes during military training and deployment involving the use of combat rations: a systematic literature review. Br J Nutr 117:897–910 Friedl KE, Moore RJ, Hoyt RW, Marchitelli LJ, Martinez-Lopez LE (1985) Askew EW (2000) Endocrine markers of semistarvation in healthy lean men in a multistressor environment. J Appl Physiol 88:1820–1830 Vikmoen O, Teien HK, Raustol M, Aandstad A, Tanso R, Gulliksrud K, Skare M, Raastad T (2020) Sex differences in the physiological response to a demanding military field exercise. Scand J Med Sci Sports 30:1348–1359 O’Leary TJ, Gifford RM, Double RL, Reynolds RM, Woods DR, Wardle SL, Greeves JP (2019) Skeletal responses to an all-female unassisted Antarctic traverse. Bone 121:267–276 O’Leary TJ, Walsh NP, Casey A, Izard RM, Tang JCY, Fraser WD, Greeves JP (2021) Supplementary energy increases bone formation during arduous military training. Med Sci Sports Exerc 53:394–403 Opstad PK, Falch D, Oktedalen O, Fonnum F, Wergeland R (1984) The thyroid function in young men during prolonged exercise and the effect of energy and sleep deprivation. Clin Endocrinol (Oxf) 20:657–669 Gibbs JC, Williams NI, De Souza MJ (2013) Prevalence of individual and combined components of the female athlete triad. Med Sci Sports Exerc 45:985–996 Cosman F, Ruffing J, Zion M, Uhorchak J, Ralston S, Tendy S, McGuigan FE, Lindsay R, Nieves J (2013) Determinants of stress fracture risk in United States Military Academy cadets. Bone 55:359–366 Smathers AM, Bemben MG, Bemben DA (2009) Bone density comparisons in male competitive road cyclists and untrained controls. Med Sci Sports Exerc 41:290–296 Drinkwater BL, Bruemner B, Chesnut CH 3rd (1990) Menstrual history as a determinant of current bone density in young athletes. JAMA 263:545–548 Warren MP, Brooks-Gunn J, Fox RP, Holderness CC, Hyle EP, Hamilton WG (2002) Osteopenia in exercise-associated amenorrhea using ballet dancers as a model: a longitudinal study. J Clin Endocrinol Metab 87:3162–3168 Hosmer WD, Genant HK, Browner WS (2002) Fractures before menopause: a red flag for physicians. Osteoporos Int 13:337–341 Barrack MT, Fredericson M, Tenforde AS, Nattiv A (2017) Evidence of a cumulative effect for risk factors predicting low bone mass among male adolescent athletes. Br J Sports Med 51:200–205 Manore MM (1999) Nutritional needs of the female athlete. Clin Sports Med 18:549–563 Fairburn CG, Beglin SJ (1994) Assessment of eating disorders: interview or self-report questionnaire? Int J Eat Disord 16:363–370 Barrack MT, Rauh MJ, Barkai HS, Nichols JF (2008) Dietary restraint and low bone mass in female adolescent endurance runners. Am J Clin Nutr 87:36–43 Rauh MJ, Barrack M, Nichols JF (2014) Associations between the female athlete triad and injury among high school runners. Int J Sports Phys Ther 9:948–958