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Associations between nutrition, energy expenditure and energy availability with bone mass acquisition in dance students: a 3-year longitudinal study

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Abstract

Summary

Three years of study showed that female and male vocational dancers displayed lower bone mass compared to controls, at forearm, lumbar spine and femoral neck. Energy intake was found to positively predict bone mass accruals only in female dancers at femoral neck. Vocational dancers can be a risk population to develop osteoporosis.

Purpose

To determine whether risk factors normally associated with low bone mass in athletic populations (i.e. nutrition intake, energy expenditure and energy availability) are significant predictors of bone mass changes in vocational dance students.

Methods

The total of 101 vocational dancers (63 females, 12.8 ± 2.2 years; 38 males, 12.7 ± 2.2 years) and 115 age-matched controls (68 females, 13.0 ± 2.1 years; 47 males, 13.0 ± 1.8 years) were monitored for 3 consecutive years. Bone mass parameters were measured annually at impact sites (femoral neck, FN; lumber spine, LS) and non-impact site (forearm) using DXA. Nutrition (3-day record), energy expenditure (accelerometer), energy availability and IGF-1 serum concentration (immunoradiometric assays) were also assessed.

Results

Female and male vocational dancers had consistently reduced bone mass at all anatomical sites (p < 0.001) than controls. IGF-1 did not differ between male vocational dancers and controls, but female dancers showed it higher than controls. At baseline, calcium intake was significantly greater in female vocational dancers than controls (p < 0.05). Male vocational dancers’ fat and carbohydrate intakes were significantly lower than matched controls (p < 0.001 and p < 0.05, respectively). Energy availability of both female and male vocational dancers was within the normal range. A significant group effect was found at the FN regarding energy intake (p < 0.05) in female dancers. No significant predictors were found to explain bone mass differences in males.

Conclusion

Our 3-year study revealed that both female and male vocational dancers displayed lower bone mass compared to controls, at both impact and non-impact sites. The aetiology of these findings may be grounded on factors different than those usually considered in athletic populations.

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References

  1. Feng X, McDonald JM (2011) Disorders of bone remodeling. Annu Rev Pathol 6:121–145. https://doi.org/10.1146/annurev-pathol-011110-130203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Cummings SR, Black DM, Nevitt MC, Browner W, Cauley J, Ensrud K, Genant HK, Palermo L, Scott J, Vogt TM (1993) Bone density at various sites for prediction of hip fractures. Lancet 341(8837):72–75. https://doi.org/10.1016/0140-6736(93)92555-8

    Article  CAS  Google Scholar 

  3. Melton LJ, Atkinson EJ, O’Fallon WM, Wahner HW, Riggs BL (1993) Long-term fracture prediction by bone mineral assessed at different skeletal sites. J Bone Miner Res 8(10):1227–1233. https://doi.org/10.1002/jbmr.5650081010

    Article  PubMed  Google Scholar 

  4. Holroyd C, Cooper C, Dennison E (2008) Epidemiology of osteoporosis. Best Pract Res Clin Endocrinol Metab 22(5):671–685. https://doi.org/10.1016/j.beem.2008.06.001

    Article  PubMed  Google Scholar 

  5. Myszkewycz L, Koutedakis Y (1998) Injuries, amenorrhea, and osteoporosis in active females: an overview. J Dance Med Sci 2:88–94

    Google Scholar 

  6. Robson B, Chertoff A (2010) Bone health and female dancers:physical and nutritional guidelines. Int Assoc Dance Med Sci: 1–4. Available from: https://fusionartsphysicaltherapy.com/bone-health-and-female-dancers-physical-nutritional-guidelines/

  7. Doyle-Lucas AF, Akers JD, Davy BM (2010) Energetic efficiency, menstrual irregularity, and bone mineral density in elite professional female ballet dancers. J Dance Med Sci 14(4):146–154

    PubMed  Google Scholar 

  8. Burckhardt P, Wynn E, Krieg MA, Bagutti C, Faouzi M (2011) The effects of nutrition, puberty and dancing on bone density in adolescent ballet dancers. J Dance Med Sci 15(2):51–60

    PubMed  Google Scholar 

  9. Valentino R, Savastano S, Tommaselli AP, D’Amore G, Dorato M, Lombardi G (2001) The influence of intense ballet training on trabecular bone mass, hormone status, and gonadotropin structure in young women. J Clin Endocrinol Metab 86(10):4674–4678. https://doi.org/10.1210/jcem.86.10.7908

    Article  CAS  PubMed  Google Scholar 

  10. Keay N, Fogelman I, Blake G (1997) Bone mineral density in professional female dancers. Br J Sports Med 31(2):143–147. https://doi.org/10.1136/bjsm.31.2.143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP (2007) American College of Sports Medicine position stand: the female athlete triad. Med Sci Sports Exerc 39(10):1867–1882. https://doi.org/10.1249/mss.0b013e318149f111

    Article  PubMed  Google Scholar 

  12. 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). Br J Sports Med 48(7):491–497. https://doi.org/10.1136/bjsports-2014-093502

    Article  PubMed  Google Scholar 

  13. Koutedakis Y, Jamurtas A (2004) The dancer as a performing athlete: physiological considerations. Sports Med 34(10):651–661. https://doi.org/10.2165/00007256-200434100-00003

    Article  PubMed  Google Scholar 

  14. Locatelli V, Bianchi VE (2014) Effect of GH/IGF-1 on bone metabolism and osteoporsosis. Int J Endocrinol 2014:1–25. https://doi.org/10.1155/2014/235060

    Article  CAS  Google Scholar 

  15. Amorim T, Wyon M, Maia J, Machado JC, Marques F, Metsios GS, Flouris AD, Koutedakis Y (2015) Prevalence of low bone mineral density in female dancers. Sports Med 45(2):257–268. https://doi.org/10.1007/s40279-014-0268-5

    Article  PubMed  Google Scholar 

  16. Amorim T, Metsios GS, Flouris AD, Nevill A, Gomes TN, Wyon M, Marques F, Nogueira L, Adubeiro N, Jamurtas AZ, Maia J, Koutedakis Y (2019) Endocrine parameters in association with bone mineral accrual in young female vocational ballet dancers. Arch Osteoporos 14(46):1–9. https://doi.org/10.1007/s11657-019-0596-z

    Article  Google Scholar 

  17. Mirwald RL, Baxter-Jones AD, Bailey DA, Beunen GP (2002) An assessment of maturity from anthropometric measurements. Med Sci Sports Exerc 34(4):689–694. https://doi.org/10.1097/00005768-200204000-00020

    Article  Google Scholar 

  18. Crawford PB, Obarzanek E, Morrison J, Sabry ZI (1994) Comparative advantage of 3-day food records over 24-hour recall and 5-day food frequency validated by observation of 9- and 10-year-old girls. J Am Diet Assoc 94(6):626–630. https://doi.org/10.1016/0002-8223(94)90158-9

    Article  CAS  PubMed  Google Scholar 

  19. Brazeau AS, Beaudoin N, Bélisle V, Messier V, Karelis AD, Rabasa-Lhoret R (2016) Validation and reliability of two activity monitors for energy expenditure assessment. J Sci Med Sport 19(1):46–50. https://doi.org/10.1016/j.jsams.2014.11.001

    Article  PubMed  Google Scholar 

  20. Weeks BK, Beck BR (2008) The BPAQ: a bone-specific physical activity assessment instrument. Osteoporos Int 19(11):1567–1577. https://doi.org/10.1007/s00198-008-0606-2

    Article  CAS  PubMed  Google Scholar 

  21. Cardadeiro G, Baptista F, Rosati N, Zymbal V, Janz KF, Sardinha LB (2014) Influence of physical activity and skeleton geometry on bone mass at the proximal femur in 10- to 12-year-old children: a longitudinal study. Osteoporos Int 25(8):2035–2045. https://doi.org/10.1007/s00198-014-2729-y

    Article  CAS  PubMed  Google Scholar 

  22. Farr JN, Lee VR, Blew RM, Lohman TG, Going SB (2011) Quantifying bone-relevant activity and its relation to bone strength in girls. Med Sci Sports Exerc 43(3):476–483. https://doi.org/10.1249/MSS.0b013e3181eeb2f2

    Article  PubMed  PubMed Central  Google Scholar 

  23. Kindler JM, Ross HL, Laing EM, Modlesky CM, Pollock NK, Baile CA, Lewis RD (2015) Load-specific physical activity scores are related to tibia bone architecture. Int J Sport Nutr Exerc Metab 25(2):136–144. https://doi.org/10.1123/ijsnem.2013-0258

    Article  PubMed  Google Scholar 

  24. Amorim T, Koutedakis Y, Nevill A, Wyon M, Maia J, Machado JC, Marques F, Metsios GS, Flouris AD, Adubeiro N, Nogueira L, Dimitriou L (2017) Bone mineral density in vocational and professional ballet dancers. Osteoporos Int 28(10):2903–2912. https://doi.org/10.1007/s00198-017-4130-0

    Article  CAS  PubMed  Google Scholar 

  25. Amorim T, Metsios GS, Wyon M, Nevill AM, Flouris AD, Maia J, Teixeira E, Machado JC, Marques F, Koutedakis Y (2017) Bone mass of female dance students prior to professional dance training: a cross-sectional study. PLoS ONE 12(7):1–11. https://doi.org/10.1371/journal.pone.0180639

    Article  CAS  Google Scholar 

  26. Warren MP, Brooks-Gunn J, Fox RP, Lancelot C, Newman D, Hamilton WG (1991) Lack of bone accretion and amenorrhea: evidence for a relative osteopenia in weight-bearing bones. J Clin Endocrinol Metab 72(4):847–853. https://doi.org/10.1210/jcem-72-4-847

    Article  CAS  PubMed  Google Scholar 

  27. Armann S, Wells C, Cheung S (1986) Bone mass, menstrual abnormalities, dietary intake, and body composition in classical ballerinas. Kinesiol Med Dance 13(1):1–15

    Google Scholar 

  28. Pearce G, Bass S, Young N, Formica C, Seeman E (1990) Does weight-bearing exercise protect against the effects of exercise-induced oligomenorrhea on bone density? Osteoporos Int 6:448–452

    Article  Google Scholar 

  29. Russell JA, Kruse DW, Koutedakis Y, McEwan IM, Wyon MA (2010) Pathoanatomy of posterior ankle impingement in ballet dancers. Clin Anat 23(6):613–621. https://doi.org/10.1002/ca.20991

    Article  PubMed  Google Scholar 

  30. Angioi M, Metsios GS, Koutedakis Y, Twitchett E, Wyon MA (2009) Physical fitness and severity of injuries in contemporary dance. Med Probl Perform Art 24(1):26–29

    Article  Google Scholar 

  31. Fortes CM, Goldberg TB, Kurokawa CS, Silva CC, Moretto MR, Biason TP, Teixeira AS, Nunes HR (2014) Relationship between chronological and bone ages and pubertal stage of breasts with bone biomarkers and bone mineral density in adolescents. J Pediatr (Rio J) 90(6):624–631. https://doi.org/10.1016/j.jped.2014.04.008

    Article  Google Scholar 

  32. Rantalainen T, Weeks BK, Nogueira RC, Beck BR (2015) Effects of bone-specific physical activity, gender and maturity on tibial cross-sectional bone material distribution: a cross-sectional pQCT comparison of children and young adults aged 5–29 years. Bone 72:101–108. https://doi.org/10.1016/j.bone.2014.11.015

    Article  PubMed  Google Scholar 

  33. Oral A, Tarakçi D, Disci R (2006) Calcaneal quantitative ultrasound measurements in young male and female professional dancers. J Strength Cond Res 20(3):572–578. https://doi.org/10.1519/r-17915.1

    Article  PubMed  Google Scholar 

  34. Cuesta A, Revilla M, Villa LF, Hernández ER, Rico H (1996) Total and regional bone mineral content in spanish professional ballet dancers. Calcif Tissue Int 58(3):150–154. https://doi.org/10.1007/bf02526880

    Article  CAS  PubMed  Google Scholar 

  35. Bonewald LF (2011) The amazing osteocyte. J Bone Miner Res 26(2):229–238. https://doi.org/10.1002/jbmr.320

    Article  CAS  PubMed  Google Scholar 

  36. Amorim T, Durães C, Machado JC, Metsios GS, Wyon M, Maia J, Flouris AD, Marques F, Nogueira L, Adubeiro N, Koutedakis Y (2018) Genetic variation in Wnt/β-catenin and ER signalling pathways in female and male elite dancers and its associations with low bone mineral density: a cross-section and longitudinal study. Osteoporos Int 29(10):2261–2274. https://doi.org/10.1007/s00198-018-4610-x

    Article  CAS  PubMed  Google Scholar 

  37. Jepsen KJ (2009) Systems analysis of bone. WIREs Syst Biol Med 1(1):73–88. https://doi.org/10.1002/wsbm.15

    Article  CAS  Google Scholar 

  38. Xing W, Baylink D, Kesavan C, Hu Y, Kapoor S, Chadwick RB, Mohan S (2005) Global gene expression analysis in the bones reveals involvement of several novel genes and pathways in mediating an anabolic response of mechanical loading in mice. J Cell Biochem 96(5):1049–1060. https://doi.org/10.1002/jcb.20606

    Article  CAS  PubMed  Google Scholar 

  39. Suuriniemi M, Mahonen A, Kovanen V, Alén M, Lyytikainen A, Wang Q, Kroger H, Cheng S (2004) Association between exercise and pubertal BMD is modulated by estrogen receptor alpha genotype. J Bone Miner Res 19(11):1758–1765. https://doi.org/10.1359/jbmr.040918

    Article  CAS  PubMed  Google Scholar 

  40. Crabtree NJ, Arabi A, Bachrach LK, Fewtrell M, El-Hajj Fuleihan G, Kecskemethy HH, Jaworski M, Gordon CM (2014) Dual-energy X-ray absorptiometry interpretation and reporting in children and adolescents: the revised 2013 ISCD pediatric official positions. J Clin Densitom 17(2):225–242. https://doi.org/10.1016/j.jocd.2014.01.003

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors thank the Portuguese Foundation for Science and Technology for supporting this research (PhD Grant: SFRH/BD/88585/2012). Thanks are also expressed to the radiology services of the Beatriz Angelo Hospital.

Funding

The study was supported by the Portuguese Foundation for Science and Technology (PhD Grant: SFRH/BD/88585/2012).

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Authors and Affiliations

  1. The Faculty of Education, Health and Wellbeing, University of Wolverhampton, Gorway Rd, Walsall, Wolverhampton, WS1 3BE, UK

    Tânia Amorim, George S. Metsios, Matthew Wyon & Yiannis Koutedakis

  2. Centre of Research, Education, Innovation and Intervention in Sport, Faculty of Sport, University of Porto, Porto, Portugal

    Tânia Amorim, Thayse Natacha Gomes & José Maia

  3. Research Centre for Physical Activity, Health and Leisure, Faculty of Sport, University of Porto, Porto, Portugal

    Laura Freitas

  4. School of Sports and Exercise Sciences, University of Thessaly, Trikala, Greece

    George S. Metsios & Yiannis Koutedakis

  5. FAME Laboratory, Department of Exercise Science, University of Thessaly, Trikala, Greece

    Andreas D. Flouris

  6. UCIBIO/REQUIMTE, Faculty of Pharmacy, University of Porto, Porto, Portugal

    Franklim Marques

  7. School of Health Technology of Porto, Polytechnic Institute of Porto, Porto, Portugal

    Luísa Nogueira & Nuno Adubeiro

Authors
  1. Tânia Amorim
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  2. Laura Freitas
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Corresponding author

Correspondence to Tânia Amorim.

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Ethics approval

Study design protocol and consent forms involving human participants were in accordance with the Helsinki Declaration (1964) and approved by the ethics committee of the Regional Administration of Health of Lisbon, Portugal (Proc.063/CES/INV/2012).

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Informed consent was obtained from all individual participants included in the study.

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Amorim, T., Freitas, L., Metsios, G.S. et al. Associations between nutrition, energy expenditure and energy availability with bone mass acquisition in dance students: a 3-year longitudinal study. Arch Osteoporos 16, 141 (2021). https://doi.org/10.1007/s11657-021-01005-5

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