Low Energy Availability Is Difficult to Assess but Outcomes Have Large Impact on Bone Injury Rates in Elite Distance Athletes

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Ida A. Heikura Australian Catholic University
Australian Institute of Sport

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Arja L.T. Uusitalo University of Helsinki
Foundation for Sports and Exercise Medicine
Finnish Institute for Occupational Health

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Trent Stellingwerff Canadian Sport Institute Pacific

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Dan Bergland Hypo2 High Performance Sport Center

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Antti A. Mero University of Jyväskylä

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Louise M. Burke Australian Catholic University
Australian Institute of Sport

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We aimed to (a) report energy availability (EA), metabolic/reproductive function, bone mineral density, and injury/illness rates in national/world-class female and male distance athletes and (b) investigate the robustness of various diagnostic criteria from the Female Athlete Triad (Triad), Low Energy Availability in Females Questionnaire, and relative energy deficiency in sport (RED-S) tools to identify risks associated with low EA. Athletes were distinguished according to benchmarks of reproductive function (amenorrheic [n = 13] vs. eumenorrheic [n = 22], low [lowest quartile of reference range; n = 10] versus normal testosterone [n = 14]), and EA calculated from 7-day food and training diaries (< or >30 kcal·kg−1 fat-free mass·day−1). Sex hormones (p < .001), triiodothyronine (p < .05), and bone mineral density (females, p < .05) were significantly lower in amenorrheic (37%) and low testosterone (40%; 15.1 ± 3.0 nmol/L) athletes, and bone injuries were ∼4.5-fold more prevalent in amenorrheic (effect size = 0.85, large) and low testosterone (effect size = 0.52, moderate) groups compared with others. Categorization of females and males using Triad or RED-S tools revealed that higher risk groups had significantly lower triiodothyronine (female and male Triad and RED-S: p < .05) and higher number of all-time fractures (male Triad: p < .001; male RED-S and female Triad: p < .01) as well as nonsignificant but markedly (up to 10-fold) higher number of training days lost to bone injuries during the preceding year. Based on the cross-sectional analysis, current reproductive function (questionnaires/blood hormone concentrations) appears to provide a more objective and accurate marker of optimal energy for health than the more error-prone and time-consuming dietary and training estimation of EA. This study also offers novel findings that athlete health is associated with EA indices.

Heikura and Burke are with the Mary MacKillop Institute for Health Research, Australian Catholic University, Melbourne, Victoria, Australia; and Sports Nutrition, Australian Institute of Sport, Bruce, Australian Capital Territory, Australia. Uusitalo is with the Dept. of Sports and Exercise Medicine, Institute of Clinical Medicine, University of Helsinki, Helsinki, Finland; Clinic for Sports and Exercise Medicine, Foundation for Sports and Exercise Medicine, Helsinki, Finland; and Finnish Institute of Occupational Health, Helsinki, Finland. Stellingwerff is with Canadian Sport Institute Pacific, Victoria, Canada. Bergland is with Hypo2 High Performance Sport Center, Flagstaff, AZ. Mero is with the Biology of Physical Activity, Faculty of Sport and Health Sciences, University of Jyväskylä, Jyväskylä, Finland.

Address author correspondence to Ida A. Heikura at ida.heikura@myacu.edu.au.
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  • Ainsworth, B.E., Haskell, W.L., Whitt, M.C., Irwin, M.L., Swartz, A.M., Strath, S.J., … Leon, A.S. (2000). Compendium of physical activities: An update of activity codes and MET intensities. Medicine & Science in Sports & Exercise, 32(Suppl. 9), 498504. PubMed ID: 10993420 doi:10.1097/00005768-200009001-00009

    • Search Google Scholar
    • Export Citation
  • Barrack, M.T., Gibbs, J.C., De Souza, M.J., Williams, N.I., Nichols, J.F., Rauh, M.J., & 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. The American Journal of Sports Medicine, 42(4), 949958. PubMed ID: 24567250 doi:10.1177/0363546513520295

    • Search Google Scholar
    • Export Citation
  • Byrne, N.M., Hills, A.P., Hunter, G.R., Weinsier, R.L., & Schutz, Y. (2005). Metabolic equivalent: One size does not fit all. Journal of Applied Physiology, 99(3), 11121119. PubMed ID: 15831804 doi:10.1152/japplphysiol.00023.2004

    • Search Google Scholar
    • Export Citation
  • Cunningham, J.J. (1991). Body composition as a determinant of energy expenditure: A synthetic review and a proposed general prediction equation. The American Journal of Clinical Nutrition, 54(6), 963969. PubMed ID: 1957828 doi:10.1093/ajcn/54.6.963

    • Search Google Scholar
    • Export Citation
  • Fagerberg, P. (2017). Negative consequences of low energy availability in natural male bodybuilding: A review. International Journal of Sport Nutrition and Exercise Metabolism, 131. PubMed ID: 28530498 doi:10.1123/ijsnem.2016-0332

    • Search Google Scholar
    • Export Citation
  • Gibbs, J.C., Nattiv, A., Barrack, M.T., Williams, N.I., Rauh, M.J., Nichols, J.F., & De Souza, M.J. (2014). Low bone density risk is higher in exercising women with multiple triad risk factors. Medicine & Science in Sports & Exercise, 46(1), 167176. PubMed ID: 23783260 doi:10.1249/MSS.0b013e3182a03b8b

    • Search Google Scholar
    • Export Citation
  • Gomez-Merino, D., Chennaoui, M., Drogou, C., Bonneau, D., & Guezennec, C.Y. (2002). Decrease in serum leptin after prolonged physical activity in men. Medicine & Science in Sports & Exercise, 34(10), 15941599. PubMed ID: 12370560 doi:10.1249/01.MSS.0000031097.37179.42

    • Search Google Scholar
    • Export Citation
  • Heikura, I.A., Burke, L.M., Bergland, D., Uusitalo, A.L.T., Mero, A.A., & Stellingwerff, T. (2018). Impact of energy availability, health and sex on hemoglobin mass responses following LHTH altitude training in elite female and male distance athletes. International Journal of Sports Physiology and Performance, 12, 126. doi:10.1123/ijspp.2017-0547

    • Search Google Scholar
    • Export Citation
  • Hills, A.P., Mokhtar, N., & Byrne, N.M. (2014). Assessment of physical activity and energy expenditure: An overview of objective measures. Frontiers in Nutrition, 1, 5. PubMed ID: 25988109 doi:10.3389/fnut.2014.00005

    • Search Google Scholar
    • Export Citation
  • Hopkins, W.G., Marshall, S.W., Batterham, A.M., & Hanin, J. (2009). Progressive statistics for studies in sports medicine and exercise science. Medicine & Science in Sports & Exercise, 41(1), 313. PubMed ID: 19092709 doi:10.1249/MSS.0b013e31818cb278

    • Search Google Scholar
    • Export Citation
  • Ihle, R., & Loucks, A.B. (2004). Dose-response relationships between energy availability and bone turnover in young exercising women. Journal of Bone and Mineral Research, 19(8), 12311240. PubMed ID: 15231009 doi:10.1359/JBMR.040410

    • Search Google Scholar
    • Export Citation
  • The International Society of Clinical Densitometry. (2017, September 15). 2015 ISCD official positions—Adult. Retrieved from https://www.iscd.org/official-positions/2015-iscd-official-positions-adult/

    • Search Google Scholar
    • Export Citation
  • Joy, E., De Souza, M.J., Nattiv, A., Misra, M., Williams, N.I., Mallinson, R.J., … Borgen, J.S. (2014). 2014 female athlete triad coalition consensus statement on treatment and return to play of the female athlete triad. Current Sports Medicine Reports, 13(4), 219232. PubMed ID: 25014387 doi:10.1249/JSR.0000000000000077

    • Search Google Scholar
    • Export Citation
  • Koehler, K., Achtzehn, S., Braun, H., Mester, J., & Schaenzer, W. (2013). Comparison of self-reported energy availability and metabolic hormones to assess adequacy of dietary energy intake in young elite athletes. Applied Physiology, Nutrition, and Metabolism, 38(7), 725733. PubMed ID: 23980730 doi:10.1139/apnm-2012-0373

    • Search Google Scholar
    • Export Citation
  • Koehler, K., Hoerner, N.R., Gibbs, J.C., Zinner, C., Braun, H., De Souza, M.J., & Schaenzer, W. (2016). Low energy availability in exercising men is associated with reduced leptin and insulin but not with changes in other metabolic hormones. Journal of Sports Sciences, 34(20), 19211929. PubMed ID: 26852783 doi:10.1080/02640414.2016.1142109

    • Search Google Scholar
    • Export Citation
  • Loucks, A.B., & Callister, R. (1993). Induction and prevention of low-T3 syndrome in exercising women. The American Journal of Physiology, 264(5, Pt. 2), R924R930. PubMed ID: 8498602 doi:10.1152/ajpregu.1993.264.5.R924

    • Search Google Scholar
    • Export Citation
  • Loucks, A.B., & Heath, E.M. (1994). Dietary restriction reduces luteinizing hormone (LH) pulse frequency during waking hours and increases LH pulse amplitude during sleep in young menstruating women. The Journal of Clinical Endocrinology & Metabolism, 78(4), 910915. PubMed ID: 8157720 doi:10.1210/jcem.78.4.8157720

    • Search Google Scholar
    • Export Citation
  • Loucks, A.B., Kiens, B., & Wright, H.H. (2011). Energy availability in athletes. Journal of Sports Sciences, 29(Suppl. 1), S7S15. PubMed ID: 21793767 doi:10.1080/02640414.2011.588958

    • Search Google Scholar
    • Export Citation
  • Loucks, A.B., & Thuma, J.R. (2003). Luteinizing hormone pulsatility is disrupted at a threshold of energy availability in regularly menstruating women. The Journal of Clinical Endocrinology & Metabolism, 88(1), 297311. PubMed ID: 12519869 doi:10.1210/jc.2002-020369

    • Search Google Scholar
    • Export Citation
  • Melin, A., Tornberg, A.B., 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. British Journal of Sports Medicine, 48(7), 540545. PubMed ID: 24563388 doi:10.1136/bjsports-2013-093240

    • Search Google Scholar
    • Export Citation
  • Melin, A., Tornberg, A.B., Skouby, S., Moller, S.S., Faber, J., Sundgot-Borgen, J., & Sjodin, A. (2016). Low-energy density and high fiber intake are dietary concerns in female endurance athletes. Scandinavian Journal of Medicine & Science in Sports, 26(9), 10601071. PubMed ID: 26148242 doi:10.1111/sms.12516

    • Search Google Scholar
    • Export Citation
  • Melin, A., Tornberg, A.B., Skouby, S., Moller, S.S., Sundgot-Borgen, J., Faber, J., … Sjodin, A. (2015). Energy availability and the female athlete triad in elite endurance athletes. Scandinavian Journal of Medicine & Science in Sports, 25(5), 610622. PubMed ID: 24888644 doi:10.1111/sms.12261

    • Search Google Scholar
    • Export Citation
  • Mountjoy, M., Sundgot-Borgen, J., Burke, L., Carter, S., Constantini, N., Lebrun, C., … Ljungqvist, A. (2014). The IOC consensus statement: Beyond the female athlete triad—Relative energy deficiency in sport (RED-S). British Journal of Sports Medicine, 48(7), 491497. PubMed ID: 24620037 doi:10.1136/bjsports-2014-093502

    • Search Google Scholar
    • Export Citation
  • 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 Internal Medicine, 176(5), 702703. PubMed ID: 26999758 doi:10.1001/jamainternmed.2016.0152

    • Search Google Scholar
    • Export Citation
  • Nana, A., Slater, G.J., Stewart, A.D., & Burke, L.M. (2015). Methodology review: Using dual-energy X-ray absorptiometry (DXA) for the assessment of body composition in athletes and active people. International Journal of Sport Nutrition and Exercise Metabolism, 25(2), 198215. PubMed ID: 25029265 doi:10.1123/ijsnem.2013-0228

    • Search Google Scholar
    • Export Citation
  • Nattiv, A., Agostini, R., Drinkwater, B., & Yeager, K.K. (1994). The female athlete triad. The inter-relatedness of disordered eating, amenorrhea, and osteoporosis. Clinics in Sports Medicine, 13(2), 405418. PubMed ID: 8013041

    • Search Google Scholar
    • Export Citation
  • Pollock, N., Grogan, C., Perry, M., Pedlar, C., Cooke, K., Morrissey, D., & Dimitriou, L. (2010). Bone-mineral density and other features of the female athlete triad in elite endurance runners: A longitudinal and cross-sectional observational study. International Journal of Sport Nutrition and Exercise Metabolism, 20(5), 418426. PubMed ID: 20975110 doi:10.1123/ijsnem.20.5.418

    • Search Google Scholar
    • Export Citation
  • Reed, J.L., Bowell, J.L., Hill, B.R., Williams, B.A., De Souza, M.J., & Williams, N.I. (2011). Exercising women with menstrual disturbances consume low energy dense foods and beverages. Applied Physiology, Nutrition, and Metabolism, 36(3), 382394. PubMed ID: 21574870 doi:10.1139/h11-030

    • Search Google Scholar
    • Export Citation
  • Schoeller, D.A. (1995). Limitations in the assessment of dietary energy intake by self-report. Metabolism: Clinical and Experimental, 44(2, Suppl. 2), 1822. PubMed ID: 7869932 doi:10.1016/0026-0495(95)90204-X

    • Search Google Scholar
    • Export Citation
  • Stubbs, R.J., O’Reilly, L.M., Whybrow, S., Fuller, Z., Johnstone, A.M., Livingstone, M.B., … Horgan, G.W. (2014). Measuring the difference between actual and reported food intakes in the context of energy balance under laboratory conditions. The British Journal of Nutrition, 111(11), 20322043. PubMed ID: 24635904 doi:10.1017/S0007114514000154

    • Search Google Scholar
    • Export Citation
  • Tenforde, A.S., Barrack, M.T., Nattiv, A., & Fredericson, M. (2016). Parallels with the female athlete triad in male athletes. Sports Medicine, 46(2), 171182. PubMed ID: 26497148 doi:10.1007/s40279-015-0411-y

    • Search Google Scholar
    • Export Citation
  • Tenforde, A.S., Carlson, J.L., Chang, A., Sainani, K.L., Shultz, R., Kim, J.H., … Fredericson, M. (2017). Association of the female athlete triad risk assessment stratification to the development of bone stress injuries in collegiate athletes. The American Journal of Sports Medicine, 45(2), 302310. PubMed ID: 28038316 doi:10.1177/0363546516676262

    • Search Google Scholar
    • Export Citation
  • Tenforde, A.S., Fredericson, M., Sayres, L.C., Cutti, P., & Sainani, K.L. (2015). Identifying sex-specific risk factors for low bone mineral density in adolescent runners. The American Journal of Sports Medicine, 43(6), 14941504. doi:10.1177/0363546515572142

    • Search Google Scholar
    • Export Citation
  • Torstveit, M.K., & Sundgot-Borgen, J. (2005). Low bone mineral density is two to three times more prevalent in non-athletic premenopausal women than in elite athletes: A comprehensive controlled study. British Journal of Sports Medicine, 39(5), 282287; discussion 282–7. PubMed ID: 15849292 doi:10.1136/bjsm.2004.012781

    • Search Google Scholar
    • Export Citation
  • Viner, R.T., Harris, M., Berning, J.R., & Meyer, N.L. (2015). Energy availability and dietary patterns of adult male and female competitive cyclists with lower than expected bone mineral density. International Journal of Sport Nutrition and Exercise Metabolism, 25(6), 594602. PubMed ID: 26131616 doi:10.1123/ijsnem.2015-0073

    • Search Google Scholar
    • Export Citation
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