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RMR Ratio as a Surrogate Marker for Low Energy Availability

  • Sports Nutrition (L Cialdella Kam, Section Editor)
  • Published:
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Abstract

Purpose of Review

Low energy availability (EA) poses severe consequences to athlete performance and overall health. Suppressed resting metabolic rate (RMR) has been observed during periods of low EA. Thus, it has been suggested that the ratio of RMR measured via indirect calorimetry to predictive RMR using a standard predictive equation (RMR ratio) may be a useful assessment of EA in athletes. This review evaluated the use of RMR ratio as a surrogate marker for low EA in athletes and compared methodologies for measuring RMR ratio.

Recent Findings

Decreased RMR ratio in recent studies often correlates with signs of low EA; however, athletes with less severe cases of energy deficiency may not present with a low RMR ratio. Additionally, the methodology for RMR ratio measurements lacks standardization and varies in recent studies.

Summary

Use of RMR ratio has promise as a complementary EA measurement when used in combination with other assessment tools.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. •• Mountjoy M, Sundgot-Borgen JK, Burke LM, et al. IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update. Br J Sports Med. 2018;52(11):687–97. https://doi.org/10.1136/bjsports-2018-099193. The health effects of low energy availability are described in the updated IOC consensus statement on RED-S.

    Article  PubMed  Google Scholar 

  2. Mountjoy M, Sundgot-Borgen J, Burke L, et al. The IOC consensus statement: beyond the Female Athlete Triad-Relative Energy Deficiency in Sport (RED-S). Br J Sports Med. 2014;48(7):491–7. https://doi.org/10.1136/bjsports-2014-093502.

    Article  PubMed  Google Scholar 

  3. Areta JL, Taylor HL, Koehler K. Low energy availability: history, definition and evidence of its endocrine, metabolic and physiological effects in prospective studies in females and males. Eur J Appl Physiol. 2021;121(1):1–21. https://doi.org/10.1007/s00421-020-04516-0.

    Article  PubMed  Google Scholar 

  4. Cialdella-Kam L, Guebels CP, Maddalozzo GF, Manore MM. Dietary intervention restored menses in female athletes with exercise-associated menstrual dysfunction with limited impact on bone and muscle health. Nutrients. 2014;6(8):3018–39. https://doi.org/10.3390/nu6083018.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. De Souza MJ, Koltun KJ, Strock NC, Williams NI. Rethinking the concept of an energy availability threshold and its role in the Female Athlete Triad. Curr Opin Physiol. 2019;10:35–42. https://doi.org/10.1016/j.cophys.2019.04.001.

    Article  Google Scholar 

  6. Loucks AB, Heath EM. Induction of low-T3 syndrome in exercising women occurs at a threshold of energy availability. Am J Physiol - Regul Integr Comp Physiol. 1994;266(3 Pt 2):R817–23. https://doi.org/10.1152/ajpregu.1994.266.3.r817.

    Article  CAS  Google Scholar 

  7. 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(1):297–311. https://doi.org/10.1210/jc.2002-020369.

    Article  CAS  PubMed  Google Scholar 

  8. Nattiv A, De Souza MJ, Koltun KJ, et al. 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. 2021;31(4):335–48. https://doi.org/10.1097/JSM.0000000000000946.

    Article  PubMed  Google Scholar 

  9. 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(4):350–63. https://doi.org/10.1123/ijsnem.2018-0142.

    Article  PubMed  Google Scholar 

  10. Guebels CP, Kam LC, Maddalozzo GF, Manore MM. Active women before/after an intervention designed to restore menstrual function: resting metabolic rate and comparison of four methods to quantify energy expenditure and energy availability. Int J Sport Nutr Exerc Metab. 2014;24(1):37–46. https://doi.org/10.1123/ijsnem.2012-0165.

    Article  PubMed  Google Scholar 

  11. 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(4):403–11. https://doi.org/10.1123/ijsnem.2017-0313.

    Article  CAS  PubMed  Google Scholar 

  12. Sim A, Burns SF. Review: questionnaires as measures for low energy availability (LEA) and relative energy deficiency in sport (RED-S) in athletes. J Eat Disord. 2021;9(1):41. https://doi.org/10.1186/s40337-021-00396-7.

    Article  PubMed  PubMed Central  Google Scholar 

  13. • Staal S, Sjödin A, Fahrenholtz I, Bonnesen K, Melin AK. 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):412–8. https://doi.org/10.1123/ijsnem.2017-0327. LEAF-Q scores and RMR ratio assessed using three predictive equations in 40 professional ballet dancers (20 men, 20 women).

    Article  PubMed  Google Scholar 

  14. Martin CK, Heilbronn LK, De Jonge L, et al. Effect of calorie restriction on resting metabolic rate and spontaneous physical activity. Obesity. 2007;15(12):2964–73. https://doi.org/10.1038/oby.2007.354.

    Article  PubMed  Google Scholar 

  15. Melin A, Tornberg B, Skouby S, et al. Energy availability and the female athlete triad in elite endurance athletes. Scand J Med Sci Sport. 2015;25(5):610–22. https://doi.org/10.1111/sms.12261.

    Article  CAS  Google Scholar 

  16. De Souza MJ, Hontscharuk R, Olmsted M, Kerr G, Williams NI. Drive for thinness score is a proxy indicator of energy deficiency in exercising women. Appetite. 2007;48(3):359–67. https://doi.org/10.1016/j.appet.2006.10.009.

    Article  PubMed  Google Scholar 

  17. •• Strock NCA, Koltun KJ, Southmayd EA, Williams NI, de Souza MJ. Indices of resting metabolic rate accurately reflect energy deficiency in exercising women. Int J Sport Nutr Exerc Metab. 2020;30(1):14–24. https://doi.org/10.1123/ijsnem.2019-0199. Total triiodothyronine (T3) concentration and RMR ratio assessed in 217 female exercisers. Higher RMR ratio cutoffs proposed for two predictive equations based on sensitivity calculations.

    Article  CAS  PubMed  Google Scholar 

  18. • Stenqvist TB, Torstveit MK, Faber J, Melin AK. Impact of a 4-week intensified endurance training intervention on markers of Relative Energy Deficiency in Sport (RED-S) and performance among well-trained male cyclists. Front Endocrinol (Lausanne). 2020;11: 512365. https://doi.org/10.3389/fendo.2020.512365. RMR and energy status assessed during a 4-week exercise intervention in 20 male cyclists.

    Article  Google Scholar 

  19. Taguchi M, Moto K, Lee S, Torii S, Hongu N. Energy intake deficiency promotes bone resorption and energy metabolism suppression in Japanese male endurance runners: a pilot study. Am J Mens Health. 2020;14(1):1557988320905251. https://doi.org/10.1177/1557988320905251.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Lee S, Kuniko M, Han S, Oh T, Taguchi M. Association of low energy availability and suppressed metabolic status in Korean male collegiate soccer players: a pilot study. Am J Mens Health. 2020;14(6):1557988320982186. https://doi.org/10.1177/1557988320982186.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Moss SL, Randell RK, Burgess D, et al. Assessment of energy availability and associated risk factors in professional female soccer players. Eur J Sport Sci. 2021;21(6):861–70. https://doi.org/10.1080/17461391.2020.1788647.

    Article  PubMed  Google Scholar 

  22. • Rogers MA, Appaneal RN, Hughes D, et al. Prevalence of impaired physiological function consistent with Relative Energy Deficiency in Sport (RED-S): an Australian elite and pre-elite cohort. Br J Sports Med. 2021;55(1):38–45. https://doi.org/10.1136/bjsports-2019-101517. RMR ratio and low EA risk measured in 112 elite and pre-elite female athletes from eight sports.

    Article  PubMed  Google Scholar 

  23. • Zabriskie HA, Currier BS, Harty PS, Stecker RA, Jagim AR, Kerksick CM. Energy status and body composition across a collegiate women’s lacrosse season. Nutrients. 2019;11(2):470. https://doi.org/10.3390/nu11020470. Energy status and RMR ratio assessed over academic year in 20 female collegiate lacrosse players.

    Article  CAS  PubMed Central  Google Scholar 

  24. • Strock NCA, Koltun KJ, Mallinson RJ, Williams NI, De Souza MJ. Characterizing the resting metabolic rate ratio in ovulatory exercising women over 12 months. Scand J Med Sci Sport. 2020;30(8):1337–47. https://doi.org/10.1111/sms.13688. T3 concentration and RMR ratio assessed in 14 exericsing women over 12-month period.

    Article  Google Scholar 

  25. Hooper DR, Mallard J, Wight JT, et al. Performance and health decrements associated with Relative Energy Deficiency in Sport for Division I women athletes during a collegiate cross-country season: a case series. Front Endocrinol (Lausanne). 2021;12: 524762. https://doi.org/10.3389/fendo.2021.524762.

    Article  Google Scholar 

  26. Benardot D. Energy thermodynamics revisited: energy intake strategies for optimizing athlete body composition and performance. Pensar en Mov Rev Ciencias del Ejerc y la Salud. 2013;11(2):1–13. https://doi.org/10.15517/pensarmov.v11i2.10841.

  27. • Fahrenholtz IL, Sjödin A, Benardot D, et al. Within-day energy deficiency and reproductive function in female endurance athletes. Scand J Med Sci Sport. 2018;28(3):1139–46. https://doi.org/10.1111/sms.13030. Within-day energy balance (WDEB) and RMR assessed in 24 female competitive endurance athletes. Energy balance measured in single-hour increments.

    Article  CAS  Google Scholar 

  28. • Torstveit MK, Fahrenholtz I, Stenqvist TB, Sylta O, Melin A. Within-day energy deficiency and metabolic perturbation in male endurance athletes. Int J Sport Nutr Exerc Metab. 2018;28(4):419–27. https://doi.org/10.1123/ijsnem.2017-0337. WDEB and RMR assessed in 31 male endurance athletes. Energy balance measured in single-hour increments.

    Article  CAS  PubMed  Google Scholar 

  29. Fullmer S, Benson-Davies S, Earthman CP, et al. Evidence analysis library review of best practices for performing indirect calorimetry in healthy and non-critically ill individuals. J Acad Nutr Diet. 2015;115(9):1417-1446.e2. https://doi.org/10.1016/j.jand.2015.04.003.

    Article  PubMed  Google Scholar 

  30. • Costa PB, Richmond SR, Smith CR, et al. Physiologic, metabolic, and nutritional attributes of collegiate synchronized swimmers. Int J Sports Physiol Perform. 2019;14(5):658–64. https://doi.org/10.1123/ijspp.2018-0547. Estimated EA and RMR ratio assessed using four predictive equations in 21 female collegate syncrhonized swimmers.

    Article  PubMed  Google Scholar 

  31. Spaeth AM, Dinges DF, Goel N. Resting metabolic rate varies by race and by sleep duration. Obesity. 2015;23(12):2349–56. https://doi.org/10.1002/oby.21198.

    Article  PubMed  Google Scholar 

  32. Zhu B, Shi C, Park CG, Zhao X, Reutrakul S. Effects of sleep restriction on metabolism-related parameters in healthy adults: a comprehensive review and meta-analysis of randomized controlled trials. Sleep Med Rev. 2019;45:18–30. https://doi.org/10.1016/j.smrv.2019.02.002.

    Article  CAS  PubMed  Google Scholar 

  33. Benton MJ, Hutchins AM, Dawes JJ. Effect of menstrual cycle on resting metabolism: a systematic review and meta-analysis. PLoS ONE. 2020;15(7): e0236025. https://doi.org/10.1371/journal.pone.0236025.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. • Tinsley GM, Graybeal AJ, Lane MM. Resting metabolic rate in muscular physique athletes: validity of existing methods and development of new prediction equations. Appl Physiol Nutr Metab. 2019;44(4):397–406. https://doi.org/10.1139/apnm-2018-0412. Absolute RMR values from two handheld IC devices compared to RMR measurement using a metabolic cart in 27 muscular physique athletes (17 men, 10 women).

    Article  PubMed  Google Scholar 

  35. Purcell SA, Johnson-Stoklossa C, Braga Tibaes JR, et al. Accuracy and reliability of a portable indirect calorimeter compared to whole-body indirect calorimetry for measuring resting energy expenditure. Clin Nutr ESPEN. 2020;39:67–73. https://doi.org/10.1016/j.clnesp.2020.07.017.

    Article  PubMed  Google Scholar 

  36. O’Neill JERG, Walsh CS, McNulty SJ, et al. Resting metabolic rate in female rugby players. J Strength Cond Res. 2020;Publish Ah. https://doi.org/10.1519/jsc.0000000000003634.

  37. Smith DR, King RFGJ, Duckworth LC, et al. Energy expenditure of rugby players during a 14-day in-season period, measured using doubly labelled water. Eur J Appl Physiol. 2018;118(3):647–56. https://doi.org/10.1007/s00421-018-3804-4.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Reale RJ, Roberts TJ, Lee KA, Bonsignore JL, Anderson ML. Metabolic rate in adolescent athletes: the development and validation of new equations, and comparison to previous models. Int J Sport Nutr Exerc Metab. 2020;30(4):249–57. https://doi.org/10.1123/ijsnem.2019-0323.

    Article  PubMed  Google Scholar 

  39. Jagim AR, Camic CL, Kisiolek J, et al. Accuracy of resting metabolic rate prediction equations in athletes. J Strength Cond Res. 2018;32(7):1875–81. https://doi.org/10.1519/JSC.0000000000002111.

    Article  PubMed  Google Scholar 

  40. Schofield KL, Thorpe H, Sims ST. Resting metabolic rate prediction equations and the validity to assess energy deficiency in the athlete population. Exp Physiol. 2019;104(4):469–75. https://doi.org/10.1113/EP087512.

    Article  CAS  PubMed  Google Scholar 

  41. Webb P. Energy expenditure and fat-free mass in men and women. Am J Clin Nutr. 1981;34(9):1816–26. https://doi.org/10.1093/ajcn/34.9.1816.

    Article  CAS  PubMed  Google Scholar 

  42. Ravussin E, Bogardus C. Relationship of genetics, age, and physical fitness to daily energy expenditure and fuel utilization. Am J Clin Nutr. 1989;49(5 Suppl):968–75. https://doi.org/10.1093/ajcn/49.5.968.

    Article  CAS  PubMed  Google Scholar 

  43. Mackay KJ, Schofield KL, Sims ST, McQuillan JA, Driller MW. The validity of resting metabolic rate-prediction equations and reliability of measured RMR in female athletes. Int J Exerc Sci. 2019;12(2):886–97.

    PubMed  PubMed Central  Google Scholar 

  44. Slater G, Shaw G, Kerr A. Athlete considerations for physique measurement. In: Hume PA, Kerr DA, Ackland TR, editors. Best Practice Protocols for Physique Assessment in Sport. Springer Singapore; 2018. p. 47–60. https://doi.org/10.1007/978-981-10-5418-1_5.

    Chapter  Google Scholar 

  45. Gatterer H, Schenk K, Burtscher M. Assessment of human body composition : methods and limitations. In: Lukaski HC, editor. Body Composition: Health and Performance in Exercise and Sport. Wales: CRC Press/Taylor & Francis Group; 2017.

    Google Scholar 

  46. Ackland TR, Lohman TG, Sundgot-Borgen J, et al. Current status of body composition assessment in sport: review and position statement on behalf of the Ad Hoc research working group on body composition health and performance, under the auspices of the I.O.C. medical commission. Sport Med. 2012;42(3):227–249. https://doi.org/10.2165/11597140-000000000-00000.

  47. Prado CMM, Heymsfield SB. Lean tissue imaging: a new era for nutritional assessment and intervention. JPEN J Parenter Enteral Nutr. 2014;38(8):940–53. https://doi.org/10.1177/0148607114550189.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Cunningham JJ. A reanalysis of the factors influencing basal metabolic rate in normal adults. Am J Clin Nutr. 1980;33(11):2372–4. https://doi.org/10.1093/ajcn/33.11.2372.

    Article  CAS  PubMed  Google Scholar 

  49. Volpe S. Athlete Study. 2021. Unpublished.

  50. Reneau J, Obi B, Moosreiner A, Kidambi S. Do we need race-specific resting metabolic rate prediction equations? Nutr Diabetes. 2019;9(1):21. https://doi.org/10.1038/s41387-019-0087-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to Trisha Sterringer.

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Trisha Sterringer and D. Enette Larson-Meyer declare they have no conflicts of interests.

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Sterringer, T., Larson-Meyer, D.E. RMR Ratio as a Surrogate Marker for Low Energy Availability. Curr Nutr Rep 11, 263–272 (2022). https://doi.org/10.1007/s13668-021-00385-x

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