Prevalence of Surrogate Markers of Relative Energy Deficiency in Male Norwegian Olympic-Level Athletes

in International Journal of Sport Nutrition and Exercise Metabolism
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  • 1 Faculty of Health and Sport Science, Department of Sport Science and Physical Education, University of Agder, Kristiansand, Norway
  • | 2 Department of Sport Science, Linnaeus University, Kalmar/Växjö, Sweden
  • | 3 Norwegian Olympic and Paralympic Committee and Confederation of Sports, Oslo, Norway
  • | 4 School of Health and Behavioural Sciences, University of the Sunshine Coast, Maroochydore, Queensland, Australia
  • | 5 Norwegian School of Sport Sciences, Oslo, Norway
  • | 6 Iraki Nutrition, Fjerdingby, Norway
  • | 7 Research institute for Sport and Exercise Sciences, Liverpool John Moores University, Liverpool, United Kingdom
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The syndrome of Relative Energy Deficiency in Sport (RED-S) includes wide-ranging effects on physiological and psychological functioning, performance, and general health. However, RED-S is understudied among male athletes at the highest performance levels. This cross-sectional study aimed to investigate surrogate RED-S markers prevalence in Norwegian male Olympic-level athletes. Athletes (n = 44) aged 24.7 ± 3.8 years, body mass 81.3 ± 15.9 kg, body fat 13.7% ± 5.8%, and training volume 76.1 ± 22.9 hr/month were included. Assessed parameters included resting metabolic rate (RMR), body composition, and bone mineral density by dual-energy X-ray absorptiometry and venous blood variables (testosterone, free triiodothyronine, cortisol, and lipids). Seven athletes (16%) grouped by the presence of low RMR (RMRratio < 0.90) (0.81 ± 0.07 vs. 1.04 ± 0.09, p < .001, effect size 2.6), also showed lower testosterone (12.9 ± 5.3 vs. 19.0 ± 5.3 nmol/L, p = .020) than in normal RMR group. In low RMRratio individuals, prevalence of other RED-S markers (—subclinical—low testosterone, low free triiodothyronine, high cortisol, and elevated low-density lipoprotein) was (N/number of markers): 2/0, 2/1, 2/2, 1/3. Low bone mineral density (z-score < −1) was found in 16% of the athletes, all with normal RMR. Subclinical low testosterone and free triiodothyronine levels were found in nine (25%) and two (5%) athletes, respectively. Subclinical high cortisol was found in 23% of athletes while 34% had elevated low-density lipoprotein cholesterol levels. Seven of 12 athletes with two or more RED-S markers had normal RMR. In conclusion, this study found that multiple RED-S markers also exist in male Olympic-level athletes. This highlights the importance of regular screening of male elite athletes, to ensure early detection and treatment of RED-S.

Conflicts of interest: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

  • Arce, J.C., De Souza, M.J., Pescatello, L.S., & Luciano, A.A. (1993). Subclinical alterations in hormone and semen profile in athletes. Fertility and Sterility, 59(2), 398404.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Areta, J.L., Iraki, J., Garthe, I., Paulsen, G., & Slater, G. (2019). Steady state of respiratory gases is not necessary to achieve reliable resting metabolic rate measurements: a reliability study using the Vyntus CPX system. Paper presented at the Physiology 2019, Aberdeen, United Kingdom. Retrieved from https://www.physoc.org/abstracts/steady-state-of-respiratory-gases-is-not-necessary-to-achieve-reliable-resting-metabolic-rate-measurements-a-reliability-study-using-the-vyntus-cpx-system/

    • Search Google Scholar
    • Export Citation
  • Areta, J.L., Taylor, H.L., & Koehler, K. (2021). Low energy availability: History, definition and evidence of its endocrine, metabolic and physiological effects in prospective studies in females and males. European Journal of Applied Physiology, 121(1), 121. https://doi.org/10.1007/s00421-020-04516-0

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Barrack, M.T., Fredericson, M., Tenforde, A.S., & Nattiv, A. (2017). Evidence of a cumulative effect for risk factors predicting low bone mass among male adolescent athletes. British Journal of Sports Medicine, 51(3), 200205. https://doi.org/10.1136/bjsports-2016-096698

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Burke, L.M., Lundy, B., Fahrenholtz, I.L., & Melin, A.K. (2018). Pitfalls of conducting and interpreting estimates of energy availability in free-living athletes. International Journal of Sport Nutrition and Exercise Metabolism, 28(4), 350363. https://doi.org/10.1123/ijsnem.2018-0142

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Compher, C., Frankenfield, D., Keim, N., Roth-Yousey, L., & Evidence Analysis Working Group. (2006). Best practice methods to apply to measurement of resting metabolic rate in adults: A systematic review. Journal of the American Dietetic Association, 106(6), 881903. https://doi.org/10.1016/j.jada.2006.02.009

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Cunningham, J.J. (1980). A reanalysis of the factors influencing basal metabolic rate in normal adults. The American Journal of Clinical Nutrition, 33(11), 23722374. https://doi.org/10.1093/ajcn/33.11.2372

    • Crossref
    • Search Google Scholar
    • Export Citation
  • De Souza, M.J., Arce, J.C., Pescatello, L.S., Scherzer, H.S., & Luciano, A.A. (1994). Gonadal hormones and semen quality in male runners. A volume threshold effect of endurance training. International Journal of Sports Medicine, 15(7), 383391. https://doi.org/10.1055/s-2007-1021075

    • Crossref
    • Search Google Scholar
    • Export Citation
  • De Souza, M.J., Koltun, K.J., & Williams, N.I. (2019). 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. Sports Medicine, 49(Suppl. 2), 125137. https://doi.org/10.1007/s40279-019-01217-3

    • Crossref
    • Search Google Scholar
    • Export Citation
  • De Souza, M.J., Nattiv, A., Joy, E., Misra, M., Williams, N.I., Mallinson, R.J., Gibbs, J.C., Olmsted, M., Goolsby, M., & Matheson, G. (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. British Journal of Sports Medicine, 48(4), 289289.

    • Search Google Scholar
    • Export Citation
  • De Souza, M.J., West, S.L., Jamal, S.A., Hawker, G.A., Gundberg, C.M., & Williams, N.I. (2008). The presence of both an energy deficiency and estrogen deficiency exacerbate alterations of bone metabolism in exercising women. Bone, 43(1), 140148.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Drew, M., Vlahovich, N., Hughes, D., Appaneal, R., Burke, L.M., Lundy, B., Rogers, M., Toomey, M., Watts, D., Lovell, G., Praet, S., Halson, S.L., Colbey, C., Manzanero, S., Welvaert, M., West, N.P., Pyne, D.B., & Waddington, G. (2018). Prevalence of illness, poor mental health and sleep quality and low energy availability prior to the 2016 Summer Olympic Games. British Journal of Sports Medicine, 52(1), 4753. https://doi.org/10.1136/bjsports-2017-098208

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Drew, M.K., Vlahovich, N., Hughes, D., Appaneal, R., Peterson, K., Burke, L., Lundy, B., Toomey, M., Watts, D., Lovell, G., Praet, S., Halson, S., Colbey, C., Manzanero, S., Welvaert, M., West, N., Pyne, D.B., & Waddington, G. (2017). A multifactorial evaluation of illness risk factors in athletes preparing for the Summer Olympic Games. The Journal of Science and Medicine in Sport, 20(8), 745750. https://doi.org/10.1016/j.jsams.2017.02.010

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Elliott-Sale, K.J., Tenforde, A.S., Parziale, A.L., Holtzman, B., & Ackerman, K.E. (2018). Endocrine effects of relative energy deficiency in sport. International Journal of Sport Nutrition and Exercise Metabolism, 28(4), 335349. https://doi.org/10.1123/ijsnem.2018-0127

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Filaire, E., Maso, F., Degoutte, F., Jouanel, P., & Lac, G. (2001). Food restriction, performance, psychological state and lipid values in judo athletes. International Journal of Sports Medicine, 22(6), 454459. https://doi.org/10.1055/s-2001-16244

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Friedl, K.E., Moore, R.J., Hoyt, R.W., Marchitelli, L.J., Martinez-Lopez, L.E., & Askew, E.W. (2000). Endocrine markers of semistarvation in healthy lean men in a multistressor environment. The Journal of Applied Physiology, 88(5), 18201830. https://doi.org/10.1152/jappl.2000.88.5.1820

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Gibbs, J.C., Williams, N.I., & De Souza, M.J. (2013). Prevalence of individual and combined components of the female athlete triad. Medicine & Science in Sports & Exercise, 45(5), 985996. https://doi.org/10.1249/MSS.0b013e31827e1bdc

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hackney, A.C. (2020). Hypogonadism in exercising males: Dysfunction or adaptive-regulatory adjustment? Frontiers in Endocrinology, 11, 11. https://doi.org/10.3389/fendo.2020.00011

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hackney, A.C., Anderson, T., & Dobridge, J. (2017). Exercise and male hypogonadism: Testosterone, the hypothalamic-pituitary-testicular axis, and exercise training. In S. Winters & I. Huhtaniemi (Eds.), Male hypogonadism (pp. 257280). Springer.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hackney, A.C., & Lane, A.R. (2018). Low testosterone in male endurance-trained distance runners: Impact of years in training. Hormones, 17(1), 137139. https://doi.org/10.1007/s42000-018-0010-z

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Heikura, I.A., Burke, L.M., Bergland, D., Uusitalo, A.L.T., Mero, A.A., & Stellingwerff, T. (2018a). Impact of energy availability, health, and sex on hemoglobin-mass responses following live-high-train-high altitude training in elite female and male distance athletes. The International Journal of Sports Physiology and Performance, 13(8), 10901096. https://doi.org/10.1123/ijspp.2017-0547

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Heikura, I.A., Uusitalo, A.L.T., Stellingwerff, T., Bergland, D., Mero, A.A., & Burke, L.M. (2018b). Low energy availability is difficult to assess but outcomes have large impact on bone injury rates in elite distance athletes. International Journal of Sport Nutrition and Exercise Metabolism, 28(4), 403411. https://doi.org/10.1123/ijsnem.2017-0313

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hooper, D.R., Kraemer, W.J., Saenz, C., Schill, K.E., Focht, B.C., Volek, J.S., & Maresh, C.M. (2017). The presence of symptoms of testosterone deficiency in the exercise-hypogonadal male condition and the role of nutrition. European Journal of Applied Physiology, 117(7), 13491357. https://doi.org/10.1007/s00421-017-3623-z

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Keay, N., Francis, G., & Hind, K. (2018). Low energy availability assessed by a sport-specific questionnaire and clinical interview indicative of bone health, endocrine profile and cycling performance in competitive male cyclists. BMJ Open Sports & Exercise Medicine, 4(1), e000424. https://doi.org/10.1136/bmjsem-2018-000424

    • Search Google Scholar
    • Export Citation
  • Kerr, A., Slater, G.J., Byrne, N., & Nana, A. (2016). Reliability of 2 different positioning protocols for dual-energy X-ray absorptiometry measurement of body composition in healthy adults. Journal of Clinical Densitometry, 19(3), 282289. https://doi.org/10.1016/j.jocd.2015.08.002

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Klomsten Andersen, O., Clarsen, B., Garthe, I., Morland, M., & Stensrud, T. (2018). Bone health in elite Norwegian endurance cyclists and runners: A cross-sectional study. BMJ Open Sports & Exercise Medicine, 4(1), e000449. https://doi.org/10.1136/bmjsem-2018-000449

    • 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 Science, 34(20), 19211929. https://doi.org/10.1080/02640414.2016.1142109

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Kojima, C., Ishibashi, A., Tanabe, Y., Iwayama, K., Kamei, A., Takahashi, H., & Goto, K. (2020). Muscle glycogen content during endurance training under low energy availability. Medicine & Science in Sports & Exercise, 52(1), 187195. https://doi.org/10.1249/MSS.0000000000002098

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Kraus, E., Tenforde, A.S., Nattiv, A., Sainani, K.L., Kussman, A., Deakins-Roche, M., Singh, S., Kim, B.Y., Barrack, M.T., & Fredericson, M. (2019). Bone stress injuries in male distance runners: Higher modified female athlete triad cumulative risk assessment scores predict increased rates of injury. British Journal of Sports Medicine, 53(4), 237242. https://doi.org/10.1136/bjsports-2018-099861

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Langan-Evans, C., Germaine, M., Artukovic, M., Oxborough, D.L., Areta, J.L., Close, G.L., & Morton, J.P. (2021). The psychological and physiological consequences of low energy availability in a male combat sport athlete. Medicine & Science in Sports & Exercise, 53(4), 673683.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Lee, S., Kuniko, M., Han, S., Oh, T., & Taguchi, M. (2020). Association of low energy availability and suppressed metabolic status in korean male collegiate soccer players: A pilot study. American Journal of Mens Health, 14(6), 1557988320982186. https://doi.org/10.1177/1557988320982186

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Logue, D.M., Madigan, S.M., Melin, A., Delahunt, E., Heinen, M., Donnell, S.M., & Corish, C.A. (2020). Low energy availability in athletes 2020: An updated narrative review of prevalence, risk, within-day energy balance, knowledge, and impact on sports performance. Nutrients, 12(3), 835. https://doi.org/10.3390/nu12030835

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Logue, D.M., Madigan, S.M., Melin, A., McDonnell, S.J., Delahunt, E., Heinen, M., & Corish, C.A. (2021). Self-reported reproductive health of athletic and recreationally active males in Ireland: Potential health effects interfering with performance. European Journal of Sport Science, 21(2), 275284. https://doi.org/10.1080/17461391.2020.1748116

    • Crossref
    • 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 and Metabolism, 88(1), 297311. https://doi.org/10.1210/jc.2002-020369

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Marra, M., Polito, A., De Filippo, E., Cuzzolaro, M., Ciarapica, D., Contaldo, F., & Scalfi, L. (2002). Are the general equations to predict BMR applicable to patients with anorexia nervosa? Eating and Weight Disorders, 7(1), 5359. https://doi.org/10.1007/BF03354430

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Martinsen, M., Bratland-Sanda, S., Eriksson, A.K., & Sundgot-Borgen, J. (2010). Dieting to win or to be thin? A study of dieting and disordered eating among adolescent elite athletes and non-athlete controls. British Journal of Sports Medicine, 44(1), 7076. https://doi.org/10.1136/bjsm.2009.068668

    • Crossref
    • Search Google Scholar
    • Export Citation
  • McCall, L.M., & Ackerman, K.E. (2019). Endocrine and metabolic repercussions of relative energy deficiency in sport. Current Opinion in Endocrine and Metabolic Research, 9, 5665. https://doi.org/10.1016/j.coemr.2019.07.005

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Meczekalski, B., Podfigurna-Stopa, A., & Katulski, K. (2013). Long-term consequences of anorexia nervosa. Maturitas, 75(3), 215220. https://doi.org/10.1016/j.maturitas.2013.04.014

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

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Melin, A.K., Heikura, I.A., Tenforde, A., & Mountjoy, M. (2019). Energy availability in athletics: Health, performance, and physique. The International Journal of Sport Nutrition and Exercise Metabolism, 29(2), 152164. https://doi.org/10.1123/ijsnem.2018-0201

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Mountjoy, M., Sundgot-Borgen, J., Burke, L., Ackerman, K.E., Blauwet, C., Constantini, N., Lebrun, C., Lundy, B., Melin, A., Meyer, N., Sherman, R., Tenforde, A.S., Torstveit, M.K., & Budgett, R. (2018). International Olympic Committee (IOC) consensus statement on relative energy deficiency in sport (RED-S): 2018 Update. The International Journal of Sport Nutrition and Exercise Metabolism, 28(4), 316331. https://doi.org/10.1123/ijsnem.2018-0136

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 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). British Journal of Sports Medicine, 48(7), 491497. https://doi.org/10.1136/bjsports-2014-093502

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Nattiv, A., Loucks, A.B., Manore, M.M., Sanborn, C.F., Sundgot-Borgen, J., Warren, M.P., & American College of Sports Medicine. (2007). American college of sports medicine position stand. The female athlete triad. Medicine & Science in Sports & Exercise, 39(10), 18671882. https://doi.org/10.1249/mss.0b013e318149f111

    • Search Google Scholar
    • Export Citation
  • Papageorgiou, M., Elliott-Sale, K.J., Parsons, A., Tang, J.C.Y., Greeves, J.P., Fraser, W.D., & Sale, C. (2017). Effects of reduced energy availability on bone metabolism in women and men. Bone, 105, 191199. https://doi.org/10.1016/j.bone.2017.08.019

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Rickenlund, A., Eriksson, M.J., Schenck-Gustafsson, K., & Hirschberg, A.L. (2005). Amenorrhea in female athletes is associated with endothelial dysfunction and unfavorable lipid profile. Journal of Clinical Endocrinology & Metabolism, 90(3), 13541359. https://doi.org/10.1210/jc.2004-1286

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Safarinejad, M.R., Azma, K., & Kolahi, A.A. (2009). The effects of intensive, long-term treadmill running on reproductive hormones, hypothalamus-pituitary-testis axis, and semen quality: A randomized controlled study. Journal of Endocrinology, 200(3), 259271. https://doi.org/10.1677/JOE-08-0477

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Staal, S., Sjodin, A., Fahrenholtz, I., Bonnesen, K., & Melin, A.K. (2018). Low RMR ratio as a surrogate marker for energy deficiency, the choice of predictive equation vital for correctly identifying male and female ballet dancers at risk. The International Journal of Sport Nutrition and Exercise Metabolism, 28(4), 412418. https://doi.org/10.1123/ijsnem.2017-0327

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Strock, N.C., Koltun, K.J., Mallinson, R.J., Williams, N.I., & De Souza, M.J. (2020a). Characterizing the resting metabolic rate ratio in ovulatory exercising women over 12 months. Scandinavian Journal of Medicine and Science in Sports, 30(8), 13371347. https://doi.org/10.1111/sms.13688

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Strock, N.C., Koltun, K.J., Southmayd, E.A., Williams, N.I., & De Souza, M.J. (2020b). Indices of resting metabolic rate accurately reflect energy deficiency in exercising women. The International Journal of Sport Nutrition and Exercise Metabolism, 30(1), 111. https://doi.org/10.1123/ijsnem.2019-0199

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sundgot-Borgen, J. (1993). Prevalence of eating disorders in elite female athletes. The International Journal of Sport Nutrition, 3(1), 2940. https://doi.org/10.1123/ijsn.3.1.29

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sundgot-Borgen, J., Meyer, N.L., Lohman, T.G., Ackland, T.R., Maughan, R.J., Stewart, A.D., & Muller, W. (2013). How to minimise the health risks to athletes who compete in weight-sensitive sports review and position statement on behalf of the Ad Hoc research working group on body composition, health and performance, under the auspices of the IOC Medical Commission. British Journal of Sports Medicine, 47(16), 10121022. https://doi.org/10.1136/bjsports-2013-092966

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sundgot-Borgen, J., & Torstveit, M.K. (2010). Aspects of disordered eating continuum in elite high-intensity sports. Scandinavian Journal of Medicine and Science in Sports, 20(Suppl. 2), 112121. https://doi.org/10.1111/j.1600-0838.2010.01190.x

    • Crossref
    • 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. https://doi.org/10.1007/s40279-015-0411-y

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Tenforde, A.S., Parziale, A.L., Popp, K.L., & Ackerman, K.E. (2018). Low bone mineral density in male athletes is associated with bone stress injuries at anatomic sites with greater trabecular composition. American Journal of Sports Medicine, 46(1), 3036. https://doi.org/10.1177/0363546517730584

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Thompson, J., & Manore, M.M. (1996). Predicted and measured resting metabolic rate of male and female endurance athletes. Journal of the American Dietetic Association, 96(1), 3034. https://doi.org/10.1016/S0002-8223(96)00010-7

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Torstveit, M.K., Fahrenholtz, I., Stenqvist, T.B., Sylta, O., & Melin, A. (2018). Within-day energy deficiency and metabolic perturbation in male endurance athletes. The International Journal of Sport Nutrition and Exercise Metabolism, 28(4), 419427. https://doi.org/10.1123/ijsnem.2017-0337

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Torstveit, M.K., Fahrenholtz, I.L., Lichtenstein, M.B., Stenqvist, T.B., & Melin, A.K. (2019). Exercise dependence, eating disorder symptoms and biomarkers of relative energy deficiency in sports (RED-S) among male endurance athletes. BMJ Open Sport Exercise Medicine, 5(1), e000439. https://doi.org/10.1136/bmjsem-2018-000439

    • Crossref
    • 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. The International Journal of Sport Nutrition and Exercise Metabolism, 25(6), 594602. https://doi.org/10.1123/ijsnem.2015-0073

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Weir, J.B. (1990). New methods for calculating metabolic rate with special reference to protein metabolism. 1949. Nutrition, 6(3), 213221.

    • Search Google Scholar
    • Export Citation
  • Wells, K.R., Jeacocke, N.A., Appaneal, R., Smith, H.D., Vlahovich, N., Burke, L.M., & Hughes, D. (2020). The Australian Institute of Sport (AIS) and National Eating Disorders Collaboration (NEDC) position statement on disordered eating in high performance sport. British Journal of Sports Medicine, 54(21), 12471258. https://doi.org/10.1136/bjsports-2019-101813

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Wilson, G., Martin, D., Morton, J.P., & Close, G.L. (2018). Male flat jockeys do not display deteriorations in bone density or resting metabolic rate in accordance with race riding experience: Implications for RED-S. International Journal of Sport Nutrition and Exercise Metabolism, 28(4), 434439.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Woods, A.L., Garvican-Lewis, L.A., Lundy, B., Rice, A.J., & Thompson, K.G. (2017). New approaches to determine fatigue in elite athletes during intensified training: Resting metabolic rate and pacing profile. PLoS One, 12(3), e0173807. https://doi.org/10.1371/journal.pone.0173807

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Woods, A.L., Rice, A.J., Garvican-Lewis, L.A., Wallett, A.M., Lundy, B., Rogers, M.A., Welvaert, M., Halson, S., McKune, A., & Thompson, K.G. (2018). The effects of intensified training on resting metabolic rate (RMR), body composition and performance in trained cyclists. PLoS One, 13(2), e0191644. https://doi.org/10.1371/journal.pone.0191644

    • Crossref
    • Search Google Scholar
    • Export Citation
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