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Bone Geometry According to Menstrual Function in Female Endurance Athletes

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Abstract

Athletes have higher bone mineral density (BMD) relative to nonathletes. In amenorrheic athletes BMD may be compromised by estrogen deficiency, but it is unknown whether this is accompanied by structural differences. We compared femoral neck bone geometry and density of a-/oligomenorrheic athletes (AAs), eumenorrheic athletes (EAs), and eumenorrheic controls (ECs). We recruited 156 women: (68 endurance athletes and 88 controls). Femoral neck BMD, section modulus (Z), and width were measured using dual-energy X-ray absorptiometry. Menstrual function was assessed by questionnaire and classified as EA (≥10 periods/year) or AA (≤9 periods/year): 24 athletes were AA and 44 EA. Femoral neck BMD was significantly higher in EA than AA (8 %, difference) and EC (11 % difference): mean [SE] 1.118 [0.015], 1.023 [0.020] and 0.999 [0.014] g cm−2, respectively; p < 0.001. Z was significantly higher in EA than EC (11 % difference): EA 667 [19], AA 625 [21], and EC 592 [10] cm3; p < 0.001. Femoral neck width did not differ between groups. All differences persisted after adjustment for height, age, and body mass. The higher femoral neck Z and BMD in athletes, despite similar width, may indicate that exercise-related bone gains are endosteal rather than periosteal. Athletes with amenorrhea had smaller increments in bone mass rather than structural adaptation. The maintained femoral neck width in controls may be an adaptive mechanism to conserve bone strength in bending despite inactivity-related bone decrement.

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References

  1. Drinkwater BL (1994) 1994 C.H. McCloy Research lecture. Does physical activity play a role in preventing osteoporosis? Res Q Exerc Sport 65:197–206

    Article  PubMed  Google Scholar 

  2. Drinkwater BL, Nilson K, Chesnut CH, Bremner WJ, Shainholtz S, Southworth MB (1984) Bone mineral content of amenorrheic and eumenorrheic athletes. N Engl J Med 311:277–281

    Article  PubMed  CAS  Google Scholar 

  3. Myburgh KH, Bachrach LK, Lewis B, Kent K, Marcus R (1993) Low bone mineral density at axial and appendicular sites in amenorrheic athletes. Med Sci Sport Exerc 25:1197–1202

    CAS  Google Scholar 

  4. Micklesfield LK, Hugo J, Johnson C, Noakes TD, Lambert EV (2007) Factors associated with menstrual dysfunction and self-reported bone stress injuries in female runners in the ultra- and half-marathons of the two oceans. Br J Sports Med 41:679–683

    Article  PubMed  CAS  Google Scholar 

  5. Grimston SK (1990) Menstrual, calcuim, and training history: relationship to bone health and female runners. Clin Sports Med 2:119–128

    Google Scholar 

  6. Rencken ML, Chesnut CH, Drinkwater BL (1996) Bone density at multiple skeletal sites in amenorrheic athletes. J Am Med Ass 276:238–240

    Article  CAS  Google Scholar 

  7. 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 341:72–75

    Article  PubMed  CAS  Google Scholar 

  8. Hui SL, Slemenda CW, Johnston CC (1988) Age and bone mass as predictors of fracture in a prospective study. J Clin Invest 81:1804–1809

    Article  PubMed  CAS  Google Scholar 

  9. Bonnick SL (2007) HSA: beyond BMD with DXA. Bone 41:S9–S12

    PubMed  Google Scholar 

  10. Jarvinen TLN, Kannus P, Pajamaki I, Vuohelainen T, Tuukkanen J, Jarvinen A, Sievanen H (2003) Estrogen deposits extra mineral into bones of female rats in puberty, but simultaneously seems to suppress the responsiveness of female skeleton to mechanical loading. Bone 32:642–651

    Article  PubMed  CAS  Google Scholar 

  11. Bass SL (2003) The structural adaptations of cortical bone to loading during different stages of maturation. J Musculoskelet Neuronal Interact 3:345–347

    PubMed  CAS  Google Scholar 

  12. Saxon LK, Turner CH (2006) Low-dose estrogen treatment suppresses periosteal bone formation in response to mechanical loading. Bone 39:1261–1267

    Article  PubMed  CAS  Google Scholar 

  13. Bennell KL, Malcolm SA, Thomas SA, Reid SJ, Brukner PD, Ebeling PR, Wark D (1996) Risk factors for stress fractures in track and field athletes—a twelve-month prospective study. Am J Sports Med 24:810–818

    Article  PubMed  CAS  Google Scholar 

  14. Snow-Harter CM, Marcus R (1992) Exercise, bone mineral density and osteoporosis. Exerc Sport Sci Rev 7:1291–1296

    CAS  Google Scholar 

  15. Frost HM (1999) On the estrogen–bone relationship and postmenopausal bone loss: a new model. J Bone Miner Res 14:1473–1477

    Article  PubMed  CAS  Google Scholar 

  16. Bailey CA, Brooke-Wavell K (2010) Optimum frequency of exercise for bone health: randomised controlled trial of a high-impact unilateral intervention. Bone 46:1043–1049

    Article  PubMed  Google Scholar 

  17. Faulkner KG, Wacker WK, Barden HS, Simonelli C, Burke PK, Ragi S, Del Rio L (2006) Femur strength index predicts hip fracture independent of bone density and hip axis length. Osteoporos Int 17:593–599

    Article  PubMed  CAS  Google Scholar 

  18. Yoshikawa T, Turner C, Peacock M, Selemenda C, Weaver C, Teegarden D, Markwardt P, Burr D (1994) Geometric structure of the femoral neck measured using dual energy X-ray absorptiometry. J Bone Miner Res 9:1053–1064

    Article  PubMed  CAS  Google Scholar 

  19. Rickenlund A, Carlström K, Ekblom B, Brismar T, von Schoultz B, Hirschberg A (2004) Diurnal profiles of testosterone and pituitary hormones suggest different mechanisms for menstrual disturbances in endurance athletes. J Clin Endocrinol Metab 89:702–707

    Article  PubMed  CAS  Google Scholar 

  20. Rickenlund A, Carlström K, Ekblom B, Brismar T, von Schoultz B, Hirschberg A (2003) Hyperandrogenicity is an alternative mechanism underlying oligomenorrhea or amenorrhea in female athletes and may improve physical performance. Fertil Steril 79:947–955

    Article  PubMed  Google Scholar 

  21. Broekmans F, Visser J, Laven J, Broer S, Themmen A, Frauser B (2008) Anti-mullerian hormone and ovarian dysfunction. Trends Endocrinol Metab 19:340–347

    Article  PubMed  CAS  Google Scholar 

  22. Grimston S, Sanborn C, Miller P (1990) The application of historical data for evaluation of osteopenia in female runners: the menstrual index. Clin Sports Med 1990:108–118

    Google Scholar 

  23. Bennell KL, Malcolm SA, Wark JD, Brukner PD (1997) Skeletal effects of menstrual disturbances in athletes. Scand J Med Sci Sports 7:261–273

    Article  PubMed  CAS  Google Scholar 

  24. Ducher G, Eser P, Hill B, Bass S (2009) History of amenorrhoea compromises some of the exercise-induced benefits in cortical and trabecular bone in the peripheral and axial skeleton: a study in retired elite gymnasts. Bone 45:760–767

    Article  PubMed  CAS  Google Scholar 

  25. Warren MP, Brooks-Gunn J, Fox RP, Holderness CC, Hyle EP, Hamilton WG (2002) Osteopenia in exercise-associated amenorrhea using ballet dancers as a model: a longitudinal study. J Clin Endocrinol Metab 87:3162–3168

    Article  PubMed  CAS  Google Scholar 

  26. Torstveit MK, Sundgot-Borgen J (2005) Low bone mineral density is two to three times more prevalent in non-athletic premenopausal women than in elite athletes: a comprehensive controlled study. Brit J Sport Med 39:282–287

    Article  CAS  Google Scholar 

  27. Robinson TL, Snowharter C, Taaffe DR, Gillis D, Shaw J, Marcus R (1995) Gymnasts exhibit higher bone mass than runners despite similar prevalence of amenorrhea and oligomenorrhea. J Bone Miner Res 10:26–35

    Article  PubMed  CAS  Google Scholar 

  28. DiVasta AD, Beck TJ, Petit MA, Feldman HA, LeBoff MS, Gordon CM (2007) Bone cross-sectional geometry in adolescents and young women with anorexia nervosa: a hip structural analysis study. Osteoporos Int 18:797–804

    Article  PubMed  CAS  Google Scholar 

  29. Kaptoge S, Dalzell N, Jakes RW, Wareham N, Day NE, Khaw KT, Beck TJ, Loveridge N (2003) Hip section modulus, a measure of bending resistance, is more strongly related to reported physical activity than BMD. Osteoporos Int 14:941–949

    Article  PubMed  CAS  Google Scholar 

  30. Haapasalo H, Kontulainen S, Sievanen H, Kannus P, Jarvinen M, Vuori I (2000) Exercise-induced bone gain is due to enlargement in bone size without a change in volumetric bone density: a peripheral quantitative computed tomography study of the upper arms of male tennis players. Bone 27:351–357

    Article  PubMed  CAS  Google Scholar 

  31. Hamilton CJ, Swan VJD, Jamal SA (2010) The effects of exercise and physical activity participation on bone mass and geometry in postmenopausal women: a systematic review of pQCT studies. Osteoporos Int 21:11–23

    Article  PubMed  CAS  Google Scholar 

  32. Nikander R, Sievanen H, Heinonen A, Kannus P (2005) Femoral neck structure in adult female athletes subjected to different loading modalities. J Bone Miner Res 20:520–528

    Article  PubMed  Google Scholar 

  33. Ahlborg HG, Johnell O, Turner CH, Rannevik G, Karlsson MK (2003) Bone loss and bone size after menopause. N Engl J Med 349:327–334

    Article  PubMed  Google Scholar 

  34. Cobb KL, Bachrach LK, Greendale G, Marcus R, Neer RM, Nieves J, Sowers MF, Brown BW, Gopalakrishnan G, Luetters C, Tanner HK, Ward B, Kelsey JL (2003) Disordered eating, menstrual irregularity, and bone mineral density in female runners. Med Sci Sports Exerc 35:711–719

    Article  PubMed  Google Scholar 

  35. Hind K (2008) Recovery of bone mineral density and fertility in a former amenorrheic athlete. J Sport Sci Med 7:415–418

    Google Scholar 

  36. Christo K, Prabhakaran R, Lamparello B, Cord J, Miller KK, Goldstein MA, Gupta N, Herzog DB, Klibanski A, Misra M (2008) Bone metabolism in adolescent athletes with amenorrhea, athletes with eumenorrhea, and control subjects. Pediatrics 121:1127–1136

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. School of Sport, Exercise and Health Sciences, Loughborough University, Loughborough, Leicestershire, LE11 3TU, UK

    R. L. Duckham, C. A. Bailey, N. Cameron & K. Brooke-Wavell

  2. English Cricket Board, Loughborough, Leicestershire, UK

    N. Peirce

  3. Derby Hospitals NHS Foundation Trust, Derby, Derbyshire, UK

    G. Summers

  4. Nottingham University Hospitals NHS Trust, Nottingham, UK

    N. Peirce

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  1. R. L. Duckham
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  2. N. Peirce
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  3. C. A. Bailey
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  4. G. Summers
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  5. N. Cameron
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  6. K. Brooke-Wavell
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Correspondence to R. L. Duckham.

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Duckham, R.L., Peirce, N., Bailey, C.A. et al. Bone Geometry According to Menstrual Function in Female Endurance Athletes. Calcif Tissue Int 92, 444–450 (2013). https://doi.org/10.1007/s00223-013-9700-3

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  • DOI: https://doi.org/10.1007/s00223-013-9700-3

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