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

in International Journal of Sport Nutrition and Exercise Metabolism

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Sarah Staal University of Copenhagen
The Royal Danish Ballet

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Anders Sjödin University of Copenhagen
The Royal Danish Ballet

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Ida Fahrenholtz University of Copenhagen
The Royal Danish Ballet

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Karen Bonnesen University of Copenhagen
The Royal Danish Ballet

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Anna Katarina Melin University of Copenhagen
The Royal Danish Ballet

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DOI:
https://doi.org/10.1123/ijsnem.2017-0327
Keywords:
bone mineral density; energy availability; relative energy deficiency; resting metabolic rate
In Print:
Volume 28: Issue 4
Page Range:
412–418
Restricted access

Ballet dancers are reported to have an increased risk for energy deficiency with or without disordered eating behavior. A low ratio between measured (m) and predicted (p) resting metabolic rate (RMRratio < 0.90) is a recognized surrogate marker for energy deficiency. We aimed to evaluate the prevalence of suppressed RMR using different methods to calculate pRMR and to explore associations with additional markers of energy deficiency. Female (n = 20) and male (n = 20) professional ballet dancers, 19–35 years of age, were enrolled. mRMR was assessed by respiratory calorimetry (ventilated open hood). pRMR was determined using the Cunningham and Harris–Benedict equations, and different tissue compartments derived from whole-body dual-energy X-ray absorptiometry assessment. The protocol further included assessment of body composition and bone mineral density, blood pressure, disordered eating (Eating Disorder Inventory-3), and for females, the Low Energy Availability in Females Questionnaire. The prevalence of suppressed RMR was generally high but also clearly dependent on the method used to calculate pRMR, ranging from 25% to 80% in males and 35% to 100% in females. Five percent had low bone mineral density, whereas 10% had disordered eating and 25% had hypotension. Forty percent of females had elevated Low Energy Availability in Females Questionnaire score and 50% were underweight. Suppressed RMR was associated with elevated Low Energy Availability in Females Questionnaire score in females and with higher training volume in males. In conclusion, professional ballet dancers are at risk for energy deficiency. The number of identified dancers at risk varies greatly depending on the method used to predict RMR when using RMRratio as a marker for energy deficiency.

Staal, Sjödin, Fahrenholtz, and Melin are with the Dept. of Nutrition, Exercise and Sports, University of Copenhagen, Frederiksberg, Denmark. Bonnesen is with The Royal Danish Ballet, Copenhagen, Denmark.

Address author correspondence to Anna Katarina Melin at aot@nexs.ku.dk.
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  • Ackerman, K.E., & Misra, M. (2011). Bone health and the female athlete triad in adolescent athletes. The Physician and Sportsmedicine, 39, 131–141. PubMed ID: 21378496 doi:10.3810/psm.2011.02.1871

    • Search Google Scholar
    • Export Citation

  • Amorim, T., Wyon, M., Maia, J., Machado, J., Marques, F., Metsios, G., … Koutedakis, Y. (2015). Prevalence of low bone mineral density in female dancers. Sports Medicine, 45, 257–268. PubMed ID: 25281333 doi:10.1007/s10862-010-9207-4

    • Search Google Scholar
    • Export Citation

  • Carlsohn, A., Scharhag-Rosenberger, F., Cassel, M., & Mayer, F. (2011). Resting metabolic rate in elite rowers and canoeists: Difference between indirect calorimetry and prediction. Annals of Nutrition & Metabolism, 58, 239–244. PubMed ID: 21811063 doi:10.1159/000330119

    • Search Google Scholar
    • Export Citation

  • Casiero, D., & Frishman, W.H. (2006). Cardiovascular complications of eating disorders. Cardiology in Review, 14, 227–231. PubMed ID: 16924163 doi:10.1097/01.crd.0000216745.96062.7c

    • Search Google Scholar
    • Export Citation

  • Clausen, L., Rosenvinge, J.H., & Friborg, O. (2011). Validating the Eating Disorder Inventory-3 (EDI-3): A comparison between 561 female eating disorders patients and 878 females from the general population. Journal of Psychopathology and Behavioral Assessment, 33, 101–110. PubMed ID: 21472023 doi:10.1007/s10862-010-9207-4

    • 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, 2372–2374. PubMed ID: 7435418 doi:10.1093/ajcn/33.11.2372

    • Search Google Scholar
    • Export Citation

  • De Souza, M.J., Hontscharuk, R., Olmsted, M., Kerr, G., & Williams, N.I. (2007). Drive for thinness score is a proxy indicator of energy deficiency in exercising women. Appetite, 48, 359–367. PubMed ID: 17184880 doi:10.1016/j.appet.2006.10.009

    • 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, 140–148. PubMed ID: 18486582 doi:10.1016/j.bone.2008.03.013

    • Search Google Scholar
    • Export Citation

  • Diffey, B., Piers, L.S., Soares, M.J., & O’dea, K. (2007). The effect of oral contraceptive agents on the basal metabolic rate of young women. British Journal of Nutrition, 77, 853. PubMed ID: 9227183 doi:10.1079/BJN19970084

    • Search Google Scholar
    • Export Citation

  • Doyle-Lucas, A.F., Akers, J.D., & Davy, B.M. (2010). Energetic efficiency, menstrual irregularity, and bone mineral density in elite professional female ballet dancers. Journal of Dance Medicine & Science, 14, 146–155. PubMed ID: 21703085

    • Search Google Scholar
    • Export Citation

  • Elia, M., & Livesey, G. (1992). Energy expenditure and fuel selection in biological systems: The theory and practice of calculations based on indirect calorimetry and tracer methods. World Review of Nutrition and Dietetics, 70, 68–131. PubMed ID: 1292242 doi:10.1159/000421672

    • Search Google Scholar
    • Export Citation

  • Folscher, L., Grant, C.C., Fletcher, L., & Janse van Rensberg, D.C. (2015). Ultra-marathon athletes at risk for the female athlete triad. Sports Medicine—Open, 1, 29. PubMed ID: 26380807 doi:10.1186/s40798-015-0027-7

    • Search Google Scholar
    • Export Citation

  • Garner, D. (2004). Eating Disorder Inventory-3: Professional manual. Professional Manual. Lutz, FL: Psychological Assessment Resources, Inc.

    • Search Google Scholar
    • Export Citation

  • Gibbs, J.C., Williams, N.I., Scheid, J.L., Toombs, R.J., & De Souza, M.J. (2011). The association of a high drive for thinness with energy deficiency and severe menstrual disturbances: Confirmation in a large population of exercising women. International Journal of Sport Nutrition and Exercise Metabolism, 21, 280–290. PubMed ID: 21813911 doi:10.1123/ijsnem.21.4.280

    • Search Google Scholar
    • Export Citation

  • Harris, J., & Benedict, F. (1919). A biometric study of basal metabolism in man. Washington, DC: Carnegie Institution of Washington.

  • Hoch, A.Z., Papanek, P., Szabo, A., Widlansky, M.E., Schimke, J.E., & Gutterman, D.D. (2011). Association between the female athlete triad and endothelial dysfunction in dancers. Clinical Journal of Sport Medicine, 21, 119–125. PubMed ID: 21358502 doi:10.1097/JSM.0b013e3182042a9a

    • Search Google Scholar
    • Export Citation

  • Kaufman, B.A., Warren, M.P., Dominguez, J.E., Wang, J., Heymsfield, S.B., & Pierson, R.N. (2002). Bone density and amenorrhea in ballet dancers are related to a decreased resting metabolic rate and lower leptin levels. The Journal of Clinical Endocrinology and Metabolism, 87, 2777–2783. PubMed ID: 12050250 doi:10.1210/jcem.87.6.8565

    • Search Google Scholar
    • Export Citation

  • Keen, A., & Drinkwater, B. (1997). Irreversible bone loss in former amenorrheic athletes. Osteoporosis International, 7, 311–315. PubMed ID: 9373563 doi:10.1007/BF01623770

    • Search Google Scholar
    • Export Citation

  • Kim, J.H., Kim, M.H., Kim, G.S., Park, J.S., & Kim, E.K. (2015). Accuracy of predictive equations for resting metabolic rate in Korean athletic and non-athletic adolescents. Nutrition Research and Practice, 9(4), 370–378. PubMed ID: 26244075 doi:10.4162/nrp.2015.9.4.370

    • Search Google Scholar
    • Export Citation

  • Koehler, K., Williams, N.I., Mallinson, R.J., Southmayd, E.A., Allaway, H.C.M., & De Souza, M.J. (2016). Low resting metabolic rate in exercise-associated amenorrhea is not due to a reduced proportion of highly metabolically active tissue compartments. American Journal of Applied Physiology, Endocrinology and Metabolism, 311, 480–487. PubMed ID: 27382033 doi:10.1152/ajpendo.00110.2016

    • Search Google Scholar
    • Export Citation

  • Lagowska, K., Kapczuk, K., & Jeszka, J. (2014). Nine-month nutritional intervention improves restoration of menses in young female athletes and ballet dancers. Journal of the International Society of Sports Nutrition, 11, 1–9. PubMed ID: 25389380 doi:10.1186/1550-2783-11-1

    • Search Google Scholar
    • Export Citation

  • Melin, A., Tornberg, A.B., Skouby, S., Faber, J., Ritz, C., Sjödin, 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, 540–545. PubMed ID: 24563388 doi:10.1136/bjsports-2013-093240

    • Search Google Scholar
    • Export Citation

  • Melin, A., Tornberg, A.B., Skouby, S., Møller, S.S., Sundgot-Borgen, J., Faber, J., … Sjödin, A. (2015). Energy availability and the female athlete triad in elite endurance athletes. Scandinavian Journal of Medicine and Science in Sports, 25, 610–622. PubMed ID: 24888644 doi:10.1111/sms.12261

    • Search Google Scholar
    • Export Citation

  • Meyer, N.L., Sundgot-Borgen, J., & Lohman, T.G. (2013). Body composition for health and performance: A survey of body composition assessment practice carried out by the Ad Hoc Research Working Group on Body Composition, Health and Performance under the auspices of the IOC Medical Commission. British Journal of Sport Medicine, 47, 1044–1053. PubMed ID: 24065075 doi:10.1136/bjsports-2013-092561

    • 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 Sport Medicine, 48, 491–497. PubMed ID: 24620037 doi:10.1136/bjsports-2014-093502

    • Search Google Scholar
    • Export Citation

  • Myburgh, K., Berman, C., Novick, I., Noakes, T.D., & Lambert, E.V. (1999). Decreased resting metabolic rate in ballet dancers with menstrual irregularities. International Journal of Sport Nutrition, 9(3), 285–294. PubMed ID: 10477364 doi:10.1123/ijsn.9.3.285

    • Search Google Scholar
    • Export Citation

  • Nattiv, A., Loucks, A.B., Manore, M.M., Sanborn, C.F., Sundgot-Borgen, J., & Warren, M.P. (2007). The female athlete triad. Medicine & Science in Sports & Exercise, 39, 1867–1882. PubMed ID: 17909417 doi:10.1249/mss.0b013e318149f111

    • Search Google Scholar
    • Export Citation

  • O’Connor, P.J., Lewis, R.D., & Kirchner, E.M. (1995). Eating disorder symptoms in female college gymnasts. Medicine & Science in Sports & Exercise, 27(4), 550–555. PubMed ID: 7791586 doi:10.1249/00005768-199504000-00013

    • Search Google Scholar
    • Export Citation

  • Ribeiro, L.G., & Da Veiga, G.V. (2010). Risk behaviors for eating disorders in Brazilian dancers. International Journal of Sports Medicine, 31, 283–288. PubMed ID: 20148375 doi:10.1055/s-0030-1248241

    • Search Google Scholar
    • Export Citation

  • Scheid, J.L., Williams, N.I., West, S.L., Van Heest, J.L., & De Souza, M.J. (2009). Elevated PYY is associated with energy deficiency and indices of subclinical disordered eating in exercising women with hypothalamic amenorrhea. Appetite, 52, 184–192. PubMed ID: 18929607 doi:10.1016/j.appet.2008.09.016

    • Search Google Scholar
    • Export Citation

  • Slater, J., McLay-Cooke, R., Brown, R., & Black, K. (2016). Female recreational exercisers at risk of low energy availability. International Journal of Sports Nutrition and Exercise Metabolism, 26, 421–427. PubMed ID: 26841435 doi:10.1123/ijsnem.2015-0245

    • Search Google Scholar
    • Export Citation

  • Sterling, W.M., Golden, N.H., Jacobsen, M.S., Ornstein, R.M., & Hertz, S.M. (2009). Metabolic assessment of menstruating and nonmenstruating normal weight adolescents. International Journal of Eating Disorders, 42, 658–663. PubMed ID: 19247996 doi:10.1002/eat.20604

    • Search Google Scholar
    • Export Citation

  • Sundgot-Borgen, J. (1993). Prevalence of eating disorders in elite female athletes. International Journal of Sports Nutrition, 3, 29–40. PubMed ID: 8499936 doi:10.1123/ijsn.3.1.29

    • Search Google Scholar
    • Export Citation

  • Tenforde, A.S., & Fredericson, M. (2011). Influence of sports participation on bone health in the young athlete: A review of the literature. PM & R: The Journal of Injury, Function, and Rehabilitation, 3, 861–867. PubMed ID: 21944303 doi:10.1016/j.pmrj.2011.05.019

    • Search Google Scholar
    • Export Citation

  • Thomas, D.T., Erdman, K.A., & Burke, L.M. (2016). Position of the academy of nutrition and dietetics, dietitians of Canada, and the American college of sports medicine: Nutrition and athletic performance. Journal of the Academy of Nutrition and Dietetics, 116, 501–528. PubMed ID: 26920240 doi:10.1016/j.jand.2015.12.006

    • 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, 30–34. PubMed ID: 8537566 doi:10.1016/S0002-8223(96)00010-7

    • Search Google Scholar
    • Export Citation

  • Torstveit, M.K., Rosenvinge, J.H., & Sundgot-Borgen, J. (2008). Prevalence of eating disorders and the predictive power of risk models in female athletes: A controlled study. Scandinavian Journal of Medicine & Science in Sports, 18, 108–118. PubMed ID: 17490455 doi:10.1111/j.1600-0838.2007.00657.x

    • Search Google Scholar
    • Export Citation

  • Twitchett, E., Koutedakis, Y., & Wyon, M. (2009). Video analysis of classical ballet performance. Journal of Dance Medicine & Science, 13, 124–128. PubMed ID: 19930814

    • Search Google Scholar
    • Export Citation

  • Vescovi, J.D., Scheid, J.L., Hontscharuk, R., & De Souza, M.J. (2008). Cognitive dietary restraint: Impact on bone, menstrual and metabolic status in young women. Physiology & Behavior, 95, 48–55. PubMed ID: 18508099 doi:10.1016/j.physbeh.2008.04.003

    • Search Google Scholar
    • Export Citation

  • Warren, M.P., Brooks-Gunn, J., Fox, R.P., Holderness, C.C., Hyle, E.P., Hamilton, W.G., & Hamilton, L. (2003). Persistent osteopenia in ballet dancers with amenorrhea and delayed menarche despite hormone therapy: A longitudinal study. Fertility and Sterility, 80, 398–404. PubMed ID: 12909505 doi:10.1016/S0015-0282(03)00660-5

    • Search Google Scholar
    • Export Citation
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