Additional Files

Lane, A. R., Hackney, A. C., Smith-Ryan, A. E., Kucera, K., Register-Mikalik, J. K., & Ondrak, K. (2021). Energy Availability and RED-S Risk Factors in Competitive, Non-elite Male Endurance Athletes. Translational Medicine and Exercise Prescription, 1(1), 25–32. https://doi.org/10.53941/tmep.v1i1.29

Energy Availability and RED-S Risk Factors in Competitive, Non-elite Male Endurance Athletes

Amy R Lane1, Anthony C Hackney()1, Abbie E Smith-Ryan1, Kristen Kucera1, Johna K Register-Mihalik1 and Kristin Ondrak1 

1Department of Exercise & Sport Science, University of North Carolina, Chapel Hill, NC 27599, USA

© The Authors


 

Abstract

Relative Energy Deficiency in Sport (RED-S) is predicated on the assumption that low energy availability (EA) induces deficiencies-dysfunction in multiple physiologic systems. However, research on RED-S and EA in male athletes is limited in comparison to women. The aim of this study is to investigate EA and the risk factors for RED-S, and their potential associations in non-elite male endurance athletes. Laboratory assessments for resting metabolic rate (RMR), bone mineral density (BMD), blood hormonal biomarkers and maximal aerobic capacity were conducted on 60 competitive, recreationally trained male endurance athletes (age=43.4±11.6 years [mean±SD], training=10.9±2.7 h/wk, 7.1±8.8 years). Participants provided 7-days of training logs and 4-days of diet records. Diet and training records were used to calculate EA. Correlations were used to examine associations between EA and RMR, BMD, stress fractures and reproductive, metabolic and bone biomarkers. Mean EA was 28.7±13.4 kcal/kg fat free mass (FFM), which categorized our sample as low EA (based upon published criterion, < 30 kcal/kg FFM) and at a high risk for RED-S. Hormonal and bone biomarkers were in normal clinical ranges, even though EA was low. The only interesting significant association was EA being negatively associated with total body BMD (r=–0.360, P=0.005), opposite of expectations. On average our subjects displayed a state of low EA based upon the criterion which has been primarily developed from female-based research. Nonetheless, our participants displayed no major hormonal or bone health disturbances found in athletes diagnosed with RED-S. A value of < 30 kcal/kg FFM to diagnose low EA may not be appropriate for non-elite endurance trained men. 

sex steroids endocrine hormones hypogonadism testosterone

References

  1. Otis CL, Drinkwater B, Johnson M, Loucks A, Wilmore J. ACSM position stand: The Female Athlete Triad. Med Sci Sports Exerc 1997, 29(5): i-ix. https://doi.org/10.1097/00005768-199705000-00037
  2. Loucks AB, Verdun M, Heath EM. Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. J Appl Physiol 1998, 84(1): 37-46. https://doi.org/10.1152/jappl.1998.84.1.37
  3. De Souza MJ, Nattiv A, Joy E, Misra M, Williams NI, Mallinson RJ, Gibbs JC, Olmsted M, Goolsby M, Matheson G. Female athlete triad coalition consensus statement on treatment and return to play of the female athlete triad. Br J Sports Med 2014, 48(4): 289. https://doi.org/10.1136/bjsports-2013-093218
  4. Mountjoy M, Sundgot-Borgen J, Burke L, Carter S, Constantini N, Lebrun C, Meyer N, Sherman R, Steffen K, Budgett R, Ljungqvist A. The IOC consensus statement: beyond the Female Athlete Triad – Relative Energy Deficiency in Sport (RED-S). Br J Sports Med 2014, 48: 491-97. https://doi.org/10.1136/bjsports-2014-093502
  5. 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
  6. Ainsworth BE, Haskell WL, Herrmann SD, Meckes N, Bassett DR Jr, Tudor Locke C, Greer JL, Vezina J, Whitt-Glover MC, Leon AS. Compendium of Physical Activities: a second update of codes and MET values. Med Sci Sports Exerc 2011, 43(8): 1575-81. https://doi.org/10.1249/MSS.0b013e31821ece12
  7. Whaley MH, Brubaker PH, Otto RM. ACSM's Guidelines for Exercise Testing and Prescription. 7th ed. Lippincott Williams &Wilkins: Philadelphia, PA, USA. 2006 Schaal K, Van Loan MD, Casazza GA. Reduced catecholamine response to exercise in amenorrheic athletes. Med Sci Sports Exerc 2011, 43(1): 34-43. https://doi.org/10.1249/MSS.0b013e3181e91ece
  8. Schaal K, Van Loan MD, Casazza GA. Reduced catecholamine response to exercise in amenorrheic athletes. Med Sci Sports Exerc 2011, 43(1): 34-43. https://doi.org/10.1249/MSS.0b013e3181e91ece
  9. De Souza MJ, West SI, 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: 140-48. https://doi.org/10.1016/j.bone.2008.03.013
  10. Melin A, Tornberg AB, Skouby S, Moller SS, Sundgot-Borgen J, Faber J, Sjodin A. Energy availability and the female athlete triad in elite endurance athletes. Scand J Med Sci Sports 2015, 25(5): 610-22. https://doi.org/10.1111/sms.12261
  11. Myerson M, Gutin B, Warren MP, May MT, Contento I, Lee M, Pisunyer FX, Pierson Jr. RN, Brooks-Gunn J. Resting metabolic rate and energy balance in amenorrheic and eumenorrheic runners. Med Sci Sports Exerc 1991, 23: 15-22. https://doi.org/10.1249/00005768-199101000-00004
  12. Staal S, Sjodin A, Fahrenholtz I, Bonneson K, Melin A. Low RMRratio as a surrogate marker for energy deficiency, the choice of predictive equation vital for correctly identifying male and female ballet dancers at risk. Int J Sport Nutr Exerc Metab 2018, 28(4): 412-18. https://doi.org/10.1123/ijsnem.2017-0327
  13. Heikura IA, Uusitalo AL, Stellingwerff T, Bergland D, Antti AM, 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(4): 403-11. https://doi.org/10.1123/ijsnem.2017-0313
  14. Buysee DJ, Reynolds CF, Monk TH, Berman SR, Kupfer DJ. The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiat Res 1989, 28(2): 193-213. https://doi.org/10.1016/0165-1781(89)90047-4
  15. Kellman M. Preventing overtraining in athletes in high-intensity sports and stress/recovery monitoring. Scand J Med Sci Sports 2010, 20 suppl 2: 95-102. https://doi.org/10.1111/j.1600-0838.2010.01192.x
  16. Kellmann M, Kallus KW. Recovery-stress Questionnaire for Athletes. Human Kinetics: Champaign, IL, USA. 2001 Vermeulen A, Verdouck L, Kaufman JM. A critical evaluation of simple methods for the estimation of free testosterone in serum. J Clin Endocrinol Metab 1999, 84(10): 3666-72. https://doi.org/10.1210/jcem.84.10.6079
  17. Vermeulen A, Verdouck L, Kaufman JM. A critical evaluation of simple methods for the estimation of free testosterone in serum. J Clin Endocrinol Metab 1999, 84(10): 3666-72. https://doi.org/10.1210/jcem.84.10.6079
  18. Hackney AC, Viru A. Research methodology: endocrinologic measurements in exercise science and sports medicine. J Athl Train 2008, 43(6): 631-39. https://doi.org/10.4085/1062-6050-43.6.631
  19. Wu A. Tietz Clinical Guide to Laboratory Tests. 4th ed. Saunders Publishing: New York. 2006 Black K, Slater J, Brown RC, Cooke R. Low energy availability, plasma lipids, and hormonal profiles of recreational athletes. J Strength Cond Res 2018, 32(10): 2816-24. https://doi.org/10.1519/JSC.0000000000002540
  20. Black K, Slater J, Brown RC, Cooke R. Low energy availability, plasma lipids, and hormonal profiles of recreational athletes. J Strength Cond Res 2018, 32(10): 2816-24. https://doi.org/10.1519/JSC.0000000000002540
  21. Hoch AZ, Pajewski NM, Moraski L, Carrera GF, Wilson CR, Hoffmann RG, Gutterman DD. Prevalence of the Female Athlete Triad in high school athletes and sedentary students. Clin J Sport Med 2009,19(5): 421-28. https://doi.org/10.1097/JSM.0b013e3181b8c136
  22. Hoch AZ, Papanek P, Szabo A, Widlansky ME, Schimke JE, Gutterman DD. Association between the female athlete triad and endothelial dysfunction in dancers. Clin J Sport Med 2011, 21(2): 119-25. https://doi.org/10.1097/JSM.0b013e3182042a9a
  23. Koehler K, Achtzehn S, Braun H, Mester J, Schnaezer W. Comparison of self reported energy availability and metabolic hormones to assess adequacy of dietary energy intake in young elite athletes. Appl Physiol Nutr Me 2013, 38(7): 725-33. https://doi.org/10.1139/apnm-2012-0373
  24. Melin A, Tornberg AB, Scouby S, Faber J, Ritz C, Sjodin A, Sundgot-Borgen J. The LEAF questionnaire: a screening tool for the identification of female athletes at risk for the female athlete triad. Br J Sport Med 2014, 48(7): 540-45. https://doi.org/10.1136/bjsports-2013-093240
  25. Tenforde AS, Barrack MT, Nattiv A, Fredericson M. Parallels with the female athlete triad in male athletes. Sports Med 2016, 46(2): 171-82. https://doi.org/10.1007/s40279-015-0411-y
  26. Ackerman KE, Putman M, Guereca G, Taylor AP. Corticol microstructure and estimated bone strength in young amenorrheic athletes, eumenorrheic athletes and non-athletes. Bone 2012, 51: 680-87. https://doi.org/10.1016/j.bone.2012.07.019
  27. Papageorgiou M, Dolan E, Elliott-Sale KJ, Sale C. Reduced energy availability: implications for bone health in physically active populations. Eur J Nutr 2018, 57: 847-59. https://doi.org/10.1007/s00394-017-1498-8
  28. Viner RT, Harris M, Berning JR, Meyer NL. 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 2015, 25: 594-602. https://doi.org/10.1123/ijsnem.2015-0073
  29. Allaway HCM, Southmayd EA, De Souza MJ. The physiology of functional hypothalamic amenorrhea associated with energy deficiency in exercising women and in women with anorexia nervosa. Horm Mol Biol Clin Investig 2016, 25: 91-119. https://doi.org/10.1515/hmbci-2015-0053
  30. MacConnie S, Barkan A, Lampman RM, Schork M, Beitins IZ. Decreased hypothalamic gonadotropin-releasing hormone secretion in male marathon runners. New Engl J Med 1986, 315: 411-17. https://doi.org/10.1056/NEJM198608143150702
  31. McColl EM, Wheeler GD, Gomes P, Bhambhani Y, Cumming DC. The effects of acute exercise on pulsatile LH release in high-mileage male runners. Clin Endocrinol (Oxf) 1989, 31(5): 617-21. https://doi.org/10.1111/j.1365-2265.1989.tb01286.x
  32. Clark LR, Dellogono MJ, Chenette EE, Mangano KM, Wilson TA. 12-week treadmill exercise program elicits lower energy availability without changes in serum testosterone in male rats. Sport Sci Health 2018, 14: 537-45. https://doi.org/10.1007/s11332-018-0455-0
  33. Bronson FH. Mammalian reproduction: an ecological perspective. Biol Reprod 1985, 32(1): 1-26. https://doi.org/10.1095/biolreprod32.1.1
  34. Fagerberg P. Negative consequences of low energy availability in natural male bodybuilding: a review. Int J Sport Nutr Exerc Metab 2018, 28(4): 385-402. https://doi.org/10.1123/ijsnem.2016-0332
  35. Koehler K, Hoerner NR, Gibbs JC, Zinner C, Braun H, De Souza MJ, Schaenzer W. Low energy availability in exercising men is associated with reduced leptin and insulin but not with changes in other metabolic hormones. J Sport Sci 2016, 34(20): 1921-29. https://doi.org/10.1080/02640414.2016.1142109
  36. Stubbs RJ, O'Reilly LM, Whybrow S, Fuller Z, Johnstone AM, Livingstone MB, Ritz P, Horgan GW. Measuring the difference between actual and reported food intakes in the context of energy balance under laboratory conditions. Br J Nutr 2014, 111(11): 2032-43. https://doi.org/10.1017/S0007114514000154