Skip to main content

Unique effects of energy versus estrogen deficiency on multiple components of bone strength in exercising women

Osteoporosis International volume 28, pages 1365–1376 (2017)Cite this article

Abstract

Summary

Many female athletes are energy and/or estrogen deficient, but the independent effects on bone health have not been isolated. Energy deficiency was detrimental at the tibia while estrogen deficiency was detrimental at the radius. Nutrition must be considered alongside menstrual recovery when addressing compromised bone health in female athletes.

Introduction

The purpose of this study was to describe volumetric bone mineral density (vBMD), bone geometry, and estimated bone strength in exercising women (n = 60) grouped according to energy status (energy replete (EnR: n = 30) vs. energy deficient (EnD: n = 30)) and estrogen status (estrogen replete (E2R: n = 33) vs. estrogen deficient (E2D: n = 27)), resulting in four distinct groups: EnR + E2R (n = 17), EnR + E2D (n = 13), EnD + E2R (n = 16), EnD + E2D (n = 14).

Methods

Energy status was determined using the ratio of measured to predicted resting energy expenditure (mREE/pREE). Estrogen status was based on self-reported menstrual status confirmed by daily evaluation of urinary estrone-1-glucoronide (E1G), pregnanediol glucuronide (PdG), and luteinizing hormone (LH). Eumenorrheic women were considered E2R, amenorrheic women were E2D, and oligomenorrheic women were categorized based on history of menses in the past year. Bone was assessed using peripheral quantitative computed tomography (pQCT).

Results

EnD women exhibited lower total vBMD, trabecular vBMD, cortical area, and BSI at the distal tibia and lower total vBMD, smaller cortical area and cortical thickness, and larger endosteal circumference at the proximal tibia compared to EnR women (p < 0.042). E2D women had lower total and cortical vBMD, larger total and trabecular area, and lower BSI at the distal radius and lower cortical vBMD at the proximal radius compared to E2R women (p < 0.023). Energy and estrogen interacted to affect total and trabecular area at the distal tibia (p < 0.021).

Conclusions

Efforts to correct energy deficiency, which in turn may promote reproductive health, are warranted in order to address the unique contributions of energy status versus estrogen status to bone health.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2

References

  1. De Souza MJ, West SL, Jamal SA, Hawker GA, Gundberg CM, Williams NI (2008) The presence of both an energy deficiency and estrogen deficiency exacerbate alterations of bone metabolism in exercising women. Bone 43:140–148

    CAS  PubMed  Article  Google Scholar 

  2. Wade GN, Schneider JE (1992) Metabolic fuels and reproduction in female mammals. Neurosci Biobehav Rev 16:235–272

    CAS  PubMed  Article  Google Scholar 

  3. Grinspoon S, Miller K, Coyle C, Krempin J, Armstrong C, Pitts S, Herzog D, Klibanski A (1999) Severity of osteopenia in estrogen-deficient women with anorexia nervosa and hypothalamic amenorrhea. J Clin Endocrinol Metab 84:2049–2055

    CAS  PubMed  Google Scholar 

  4. Hotta M, Fukuda I, Sato K, Hizuka N, Shibasaki T, Takano K (2000) The relationship between bone turnover and body weight, serum insulin-like growth factor (IGF) I, and serum IGF-binding protein levels in patients with anorexia nervosa. J Clin Endocrinol Metab 85:200–206

    CAS  PubMed  Google Scholar 

  5. Ihle R, Loucks AB (2004) Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res 19:1231–1240

    PubMed  Article  Google Scholar 

  6. Loucks AB, Verdun M, Heath EM (1998) Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. J Appl Physiol (1985) 84:37–46

    CAS  Google Scholar 

  7. Weitzmann MN, Pacifici R (2006) Estrogen deficiency and bone loss: an inflammatory tale. J Clin Invest 116:1186–1194

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  8. De Souza MJ, Toombs RJ, Scheid JL, O’Donnell E, West SL, Williams NI (2010) High prevalence of subtle and severe menstrual disturbances in exercising women: confirmation using daily hormone measures. Hum Reprod 25:491–503

    CAS  PubMed  Article  Google Scholar 

  9. Ackerman KE, Nazem T, Chapko D, Russell M, Mendes N, Taylor AP, Bouxsein ML, Misra M (2011) Bone microarchitecture is impaired in adolescent amenorrheic athletes compared with eumenorrheic athletes and nonathletic controls. J Clin Endocrinol Metab 96:3123–3133

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  10. Duckham RL, Peirce N, Bailey CA, Summers G, Cameron N, Brooke-Wavell K (2013) Bone geometry according to menstrual function in female endurance athletes. Calcif Tissue Int 92:444–450

    CAS  PubMed  Article  Google Scholar 

  11. Mallinson RJ, Williams NI, Hill BR, De Souza MJ (2013) Body composition and reproductive function exert unique influences on indices of bone health in exercising women. Bone 56:91–100

    PubMed  Article  Google Scholar 

  12. Ackerman KE, Pierce L, Guereca G, Slattery M, Lee H, Goldstein M, Misra M (2013) Hip structural analysis in adolescent and young adult oligoamenorrheic and eumenorrheic athletes and nonathletes. J Clin Endocrinol Metab 98:1742–1749

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  13. Milos G, Spindler A, Ruegsegger P, Seifert B, Muhlebach S, Uebelhart D, Hauselmann HJ (2005) Cortical and trabecular bone density and structure in anorexia nervosa. Osteoporos Int 16:783–790

    PubMed  Article  Google Scholar 

  14. 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

    CAS  PubMed  Article  Google Scholar 

  15. Ackerman KE, Putman M, Guereca G, Taylor AP, Pierce L, Herzog DB, Klibanski A, Bouxsein M, Misra M (2012) Cortical microstructure and estimated bone strength in young amenorrheic athletes, eumenorrheic athletes and non-athletes. Bone 51:680–687

    PubMed  PubMed Central  Article  Google Scholar 

  16. Bredella MA, Misra M, Miller KK, Madisch I, Sarwar A, Cheung A, Klibanski A, Gupta R (2008) Distal radius in adolescent girls with anorexia nervosa: trabecular structure analysis with high-resolution flat-panel volume CT. Radiology 249:938–946

    PubMed  PubMed Central  Article  Google Scholar 

  17. Warren MP, Brooks-Gunn J, Fox RP, Holderness CC, Hyle EP, Hamilton WG, Hamilton L (2003) Persistent osteopenia in ballet dancers with amenorrhea and delayed menarche despite hormone therapy: a longitudinal study. Fertil Steril 80:398–404

    PubMed  Article  Google Scholar 

  18. Miller KK, Lee EE, Lawson EA, Misra M, Minihan J, Grinspoon SK, Gleysteen S, Mickley D, Herzog D, Klibanski A (2006) Determinants of skeletal loss and recovery in anorexia nervosa. J Clin Endocrinol Metab 91:2931–2937

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  19. Kosmiski L, Schmiege SJ, Mascolo M, Gaudiani J, Mehler PS (2014) Chronic starvation secondary to anorexia nervosa is associated with an adaptive suppression of resting energy expenditure. J Clin Endocrinol Metab 99:908–914

    CAS  PubMed  Article  Google Scholar 

  20. Koehler K, Williams NI, Mallinson RJ, Southmayd EA, Allaway HC, De Souza MJ. 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 physiology. Endocrinology and metabolism: ajpendo 00110 2016

  21. Hayes M, Chustek M, Wang Z, Gallagher D, Heshka S, Spungen A, Bauman W, Heymsfield SBDXA (2002) Potential for creating a metabolic map of organ-tissue resting energy expenditure components. Obes Res 10:969–977

    CAS  PubMed  Article  Google Scholar 

  22. De Souza MJ, Miller BE, Loucks AB, Luciano AA, Pescatello LS, Campbell CG, Lasley BL (1998) High frequency of luteal phase deficiency and anovulation in recreational women runners: blunted elevation in follicle-stimulating hormone observed during luteal-follicular transition. J Clin Endocrinol Metab 83:4220–4232

    CAS  PubMed  Google Scholar 

  23. Kesner JS, Wright DM, Schrader SM, Chin NW, Krieg EF Jr (1992) Methods of monitoring menstrual function in field studies: efficacy of methods. Reprod Toxicol 6:385–400

    CAS  PubMed  Article  Google Scholar 

  24. Santoro N, Crawford SL, Allsworth JE, Gold EB, Greendale GA, Korenman S, Lasley BL, McConnell D, McGaffigan P, Midgely R, Schocken M, Sowers M, Weiss G (2003) Assessing menstrual cycles with urinary hormone assays. Am J Physiol Endocrinol Metab 284:E521–E530

    CAS  PubMed  Article  Google Scholar 

  25. Munro CJ, Stabenfeldt GH, Cragun JR, Addiego LA, Overstreet JW, Lasley BL (1991) Relationship of serum estradiol and progesterone concentrations to the excretion profiles of their major urinary metabolites as measured by enzyme immunoassay and radioimmunoassay. Clin Chem 37:838–844

    CAS  PubMed  Google Scholar 

  26. Miller RC, Brindle E, Holman DJ, Shofer J, Klein NA, Soules MR, O’Connor KA (2004) Comparison of specific gravity and creatinine for normalizing urinary reproductive hormone concentrations. Clin Chem 50:924–932

    CAS  PubMed  Article  Google Scholar 

  27. Wilcox R 2012. One-way and higher designs for independent groups. Introduction to robust estimation and hypothesis testing, 3rd edition: 291–377

  28. White HA (1980) Heteroskedasticity-consistent covariance-matrix estimator and a direct test for Heteroskedasticity. Econometrica 48:817–838

    Article  Google Scholar 

  29. Bonewald LF, Johnson ML (2008) Osteocytes, mechanosensing and Wnt signaling. Bone 42:606–615

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  30. Boyce BF, Xing L (2007) The RANKL/RANK/OPG pathway. Current osteoporosis reports 5:98–104

    PubMed  Article  Google Scholar 

  31. You L, Temiyasathit S, Lee P, Kim CH, Tummala P, Yao W, Kingery W, Malone AM, Kwon RY, Jacobs CR (2008) Osteocytes as mechanosensors in the inhibition of bone resorption due to mechanical loading. Bone 42:172–179

    CAS  PubMed  Article  Google Scholar 

  32. Holly JM, Perks CM (2012) Insulin-like growth factor physiology: what we have learned from human studies. Endocrinol Metab Clin N Am 41:249–263

    CAS  Article  Google Scholar 

  33. Guntur AR, Rosen CJ (2013) IGF-1 regulation of key signaling pathways in bone. Bonekey Rep 2:437

    PubMed  PubMed Central  Article  Google Scholar 

  34. Sienkiewicz E, Magkos F, Aronis KN, Brinkoetter M, Chamberland JP, Chou S, Arampatzi KM, Gao C, Koniaris A, Mantzoros CS (2011) Long-term metreleptin treatment increases bone mineral density and content at the lumbar spine of lean hypoleptinemic women. Metabolism 60:1211–1221

    CAS  PubMed  Article  Google Scholar 

  35. Chou SH, Chamberland JP, Liu X, Matarese G, Gao C, Stefanakis R, Brinkoetter MT, Gong H, Arampatzi K, Mantzoros CS (2011) Leptin is an effective treatment for hypothalamic amenorrhea. Proc Natl Acad Sci U S A 108:6585–6590

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  36. Combs CE, Nicholls JJ, Duncan Bassett JH, Williams GR (2011) Thyroid hormones and bone development. Minerva Endocrinol 36:71–85

    CAS  PubMed  Google Scholar 

  37. Seeman E (2003) Periosteal bone formation--a neglected determinant of bone strength. N Engl J Med 349:320–323

    PubMed  Article  Google Scholar 

  38. Schlenker RA, VonSeggen WW (1976) The distribution of cortical and trabecular bone mass along the lengths of the radius and ulna and the implications for in vivo bone mass measurements. Calcif Tissue Res 20:41–52

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgments

This study was supported by the U.S. Department of Defense, U.S. Army Medical Research and Material Command (Grant#: PR054531).

Author information

Affiliations

  1. Women’s Health and Exercise Lab, Department of Kinesiology, Pennsylvania State University, University Park, State College, PA, 16802, USA

    E. A. Southmayd, R. J. Mallinson, N. I. Williams & M. J. De Souza

  2. School of Social and Behavioral Sciences, Stockton University, 101 Vera King Farris Drive, Galloway, NJ, 08205, USA

    D. J. Mallinson

Authors
  1. E. A. Southmayd
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. J. Mallinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. I. Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. J. Mallinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. J. De Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. A. Southmayd.

Ethics declarations

Both studies were approved by the Biomedical Institutional Review Board at Penn State University. Study volunteers were informed of the purpose, procedures, and potential risks and benefits of participation, and signed consent was obtained.

Conflicts of interest

None.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Southmayd, E.A., Mallinson, R.J., Williams, N.I. et al. Unique effects of energy versus estrogen deficiency on multiple components of bone strength in exercising women. Osteoporos Int 28, 1365–1376 (2017). https://doi.org/10.1007/s00198-016-3887-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-016-3887-x

Keywords

  • Bone geometry
  • Energy deficiency
  • Estimated bone strength
  • Female athlete triad
  • pQCT
  • Volumetric bone mineral density