Bone mineral density, energy availability, and dietary restraint in collegiate cross-country runners and non-running controls

  • William P. McCormackEmail author
  • Todd C. Shoepe
  • Joseph LaBrie
  • Hawley C. Almstedt
Original Article



Weight-bearing activities such as running have been shown to be osteogenic. However, investigations have also shown that running may lead to site-specific deficiencies in bone mineral density (BMD) as well as overall low BMD. The purpose of this investigation was to evaluate and compare the BMD of female and male collegiate cross-country runners with non-running controls. In addition, energy availability and disordered eating attitudes and behaviors were assessed.


BMD of 60 collegiate cross-country runners and 47 BMI and age-matched non-running controls were measured via DXA scans. Participants completed a Block 2014 Food Frequency Questionnaire and Eating Disorder Examination Questionnaire.


Controlling for fat-free mass (FFM), male runners showed greater BMD at the femoral neck (0.934 ± 0.029 vs. 0.866 ± 0.028 g cm2, p < 0.05), total hip (1.119 ± 0.023 vs. 1.038 ± 0.021 g cm2, p < 0.05), and whole body (1.119 ± 0.023 vs. 1.038 ± 0.021 g cm2, p < 0.05) than male controls. The female runners had greater whole-body BMD than female controls (1.143 ± 0.018 vs. 1.087 ± 0.022 g cm2, p < 0.05). Runners scored significantly higher than controls in dietary restraint (1.134 ± 1.24 vs. 0.451 ± 0.75, p < 0.05), male runners were significantly higher than male controls in eating concern (1.344 ± 1.08 vs. 0.113 ± 0.27, p < 0.05) and female runners were significantly higher than male runners in shape concern (1.056 ± 1.27 vs. 0.242 ± 0.31, p < 0.05). Forty-two percent of the male runners and 29% of female runners had an energy availability of less than 30 kcals kg−1FFM.


It appears that distance running has beneficial effects on whole-body BMD and site-specific areas. Further research is warranted to further clarify the health effects of eating behaviors and EA of distance runners.


Eating disorder examination questionnaire Endurance athletes Weight-bearing exercise 



Analysis of covariance




Bone mineral density


Body mass index


Dual-energy X-ray absorptiometry


Energy availability


Eating Disorder Examination Questionnaire


Exercise energy expenditure


Energy intake


Fat-free mass


Food Frequency Questionnaire


Metabolic equivalent


Relative energy deficiency in sport


Resting metabolic rate



We are very grateful to the research participants, Scott Guerrero, Caitlin Jennings, and Liam Shorrock for their role in the success of this research project. We also acknowledge contributions from student research assistants involved with the data collection and data management including Lily Bramble, Makenzie Cook, and Rowena Feng.

Author contributions

WPM developed the original research inquiry, recruited participants, collected data, analyzed data, and collaborated in writing of manuscript. TCS assisted in data analysis and writing of the manuscript. JWL assisted in recruiting control participants and provided guidance on the composition of the paper. HCA collected data, analyzed data, and collaborated in writing of manuscript. The control group for this investigation was funded by a National Institute on Alcohol Abuse and Alcoholism Grant 5R21AA022942-02.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Ainsworth BE, Haskell WL, Herrmann SD, Meckes N, Bassett DR Jr, Tudor-Locke C, Leon AS (2011) 2011 compendium of physical activities: a second update of codes and MET values. Med Sci Sports Exerc 43(8):1575–1581. CrossRefGoogle Scholar
  2. Anderson DA, Lundgren JD, Shapiro JR, Paulosky CA (2004) Assessment of eating disorders: review and recommendations for clinical use. Behav Modif 28(6):763–782. CrossRefGoogle Scholar
  3. Barrack MT, Rauh MJ, Barkai HS, Nichols JF (2008) Dietary restraint and low bone mass in female adolescent endurance runners. Am J Clin Nutr 87(1):36–43CrossRefGoogle Scholar
  4. Barrack MT, Gibbs JC, De Souza MJ, Williams NI, Nichols JF, Rauh MJ, Nattiv A (2014) Higher incidence of bone stress injuries with increasing female athlete triad-related risk factors: a prospective multisite study of exercising girls and women. Am J Sports Med 42(4):949–958. CrossRefGoogle Scholar
  5. Barrack MT, Fredericson M, Tenforde AS, Nattiv A (2017) Evidence of a cumulative effect for risk factors predicting low bone mass among male adolescent athletes. Br J Sports Med 51(3):200–205. CrossRefGoogle Scholar
  6. Baxter-Jones AD, Mirwald RL, McKay HA, Bailey DA (2003) A longitudinal analysis of sex differences in bone mineral accrual in healthy 8–19-year-old boys and girls. Ann Hum Biol 30(2):160–175CrossRefGoogle Scholar
  7. Baxter-Jones AD, Faulkner RA, Forwood MR, Mirwald RL, Bailey DA (2011) Bone mineral accrual from 8 to 30 years of age: an estimation of peak bone mass. J Bone Miner Res 26(8):1729–1739. CrossRefGoogle Scholar
  8. Black AE (2000) Critical evaluation of energy intake using the Goldberg cut-off for energy intake: basal metabolic rate. A practical guide to its calculation, use and limitations. Int J Obes Relat Metab Disord 24(9):1119–1130CrossRefGoogle Scholar
  9. Block G, Woods M, Potosky A, Clifford C (1990) Validation of a self-administered diet history questionnaire using multiple diet records. J Clin Epidemiol 43(12):1327–1335CrossRefGoogle Scholar
  10. Block G, Thompson FE, Hartman AM, Larkin FA, Guire KE (1992) Comparison of two dietary questionnaires validated against multiple dietary records collected during a 1-year period. J Am Diet Assoc 92(6):686–693Google Scholar
  11. Buckinx F, Landi F, Cesari M et al (2018) Pitfalls in the measurement of muscle mass: a need for a reference standard. J Cachexia Sarcopenia Muscle 9(2):269–278CrossRefGoogle Scholar
  12. Burke LM, Close GL, Lundy B, Mooses M, Morton JP, Tenforde AS (2018a) Relative energy deficiency in sport in male athletes: a commentary on its presentation among selected groups of male athletes. Int J Sport Nutr Exerc Metab 28(4):364–374. CrossRefGoogle Scholar
  13. Burke LM, Lundy B, Fahrenholtz IL, Melin AK (2018b) Pitfalls of conducting and interpreting estimates of energy availability in free-living athletes. Int J Sport Nutr Exerc Metab 28(4):350–363. CrossRefGoogle Scholar
  14. Cunningham JJ (1991) Body composition as a determinant of energy expenditure: a synthetic review and a proposed general prediction equation. Am J Clin Nutr 54(6):963–969. CrossRefGoogle Scholar
  15. Darcy AM, Hardy KK, Lock J, Hill KB, Peebles R (2013) The Eating Disorder Examination Questionnaire (EDE-Q) among university men and women at different levels of athleticism. Eat Behav 14(3):378–381. CrossRefGoogle Scholar
  16. Fairburn CG, Cooper Z, O’Connor M (2008) Eating Disorder Examination. In: Fairburn CG (ed) Cognitive behavior therapy and eating disorders, 16.0th edn. Guilford Press, New YorkGoogle Scholar
  17. Fredericson M, Chew K, Ngo J, Cleek T, Kiratli J, Cobb K (2007) Regional bone mineral density in male athletes: a comparison of soccer players, runners and controls. Br J Sports Med 41(10):664–668. (discussion 668) CrossRefGoogle Scholar
  18. Garber CE, Blissmer B, Deschenes MR, Franklin BA, Lamonte MJ, Lee IM, American College of Sports M (2011) American College of Sports Medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Med Sci Sports Exerc 43(7):1334–1359. CrossRefGoogle Scholar
  19. Guebels CP, Kam LC, Maddalozzo GF, Manore MM (2014) 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 24(1):37–46. CrossRefGoogle Scholar
  20. Gunter KB, Almstedt HC, Janz KF (2012) Physical activity in childhood may be the key to optimizing lifespan skeletal health. Exerc Sport Sci Rev 40(1):13–21. CrossRefGoogle Scholar
  21. Hartman AM, Block G, Chan W, Williams J, McAdams M, Banks WL Jr, Robbins A (1996) Reproducibility of a self-administered diet history questionnaire administered three times over three different seasons. Nutr Cancer 25(3):305–315CrossRefGoogle Scholar
  22. Heikura IA, Uusitalo ALT, Stellingwerff T, Bergland D, Mero AA, Burke LM (2018) 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 28(4):403–411. CrossRefGoogle Scholar
  23. Hind K, Truscott JG, Evans JA (2006) Low lumbar spine bone mineral density in both male and female endurance runners. Bone 39(4):880–885. CrossRefGoogle Scholar
  24. Hind K, Gannon L, Whatley E, Cooke C, Truscott J (2012) Bone cross-sectional geometry in male runners, gymnasts, swimmers and non-athletic controls: a hip-structural analysis study. Eur J Appl Physiol 112(2):535–541. CrossRefGoogle Scholar
  25. Ihle R, Loucks AB (2004) Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res 19(8):1231–1240. CrossRefGoogle Scholar
  26. Kemmler W, Engelke K, Baumann H, Beeskow C, von Stengel S, Weineck J, Kalender WA (2006) Bone status in elite male runners. Eur J Appl Physiol 96(1):78–85. CrossRefGoogle Scholar
  27. Koehler K, Achtzehn S, Braun H, Mester J, Schaenzer W (2013) Comparison of self-reported energy availability and metabolic hormones to assess adequacy of dietary energy intake in young elite athletes. Appl Physiol Nutr Metab 38(7):725–733. CrossRefGoogle Scholar
  28. Kohl HW, Blair SN, Paffenbarger RS Jr, Macera CA, Kronenfeld JJ (1988) A mail survey of physical activity habits as related to measured physical fitness. Am J Epidemiol 127(6):1228–1239CrossRefGoogle Scholar
  29. Kohrt WM, Bloomfield SA, Little KD, Nelson ME, Yingling VR (2004) American College of Sports Medicine Position Stand: physical activity and bone health. Med Sci Sports Exerc 36(11):1985–1996CrossRefGoogle Scholar
  30. LaBrie JW, Boyle S, Earle A, Almstedt HC (2018) Heavy episodic drinking is associated with poorer bone health in adolescent and young adult women. J Stud Alcohol Drugs 79(3):391–398CrossRefGoogle Scholar
  31. Loucks AB (2004) Energy balance and body composition in sports and exercise. J Sports Sci 22(1):1–14. CrossRefGoogle Scholar
  32. Loucks AB, Kiens B, Wright HH (2011) Energy availability in athletes. J Sports Sci 29(Suppl 1):S7–15. CrossRefGoogle Scholar
  33. Luce KH, Engler PA, Crowther JH (2007) Eating disorders and alcohol use: group differences in consumption rates and drinking motives. Eat Behav 8(2):177–184. CrossRefGoogle Scholar
  34. Melin A, Tornberg AB, Skouby S, Moller SS, Sundgot-Borgen J, Faber J, Sjodin A (2015) Energy availability and the female athlete triad in elite endurance athletes. Scand J Med Sci Sports 25(5):610–622. CrossRefGoogle Scholar
  35. 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). Br J Sports Med 48(7):491–497. CrossRefGoogle Scholar
  36. Mountjoy M, Sundgot-Borgen J, Burke L, Ackerman KE, Blauwet C, Constantini N, Budgett R (2018) International Olympic Committee (IOC) Consensus Statement on Relative Energy Deficiency in Sport (RED-S): 2018 update. Int J Sport Nutr Exerc Metab 28(4):316–331. CrossRefGoogle Scholar
  37. 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. CrossRefGoogle Scholar
  38. Papageorgiou M, Elliott-Sale KJ, Parsons A, Tang JCY, Greeves JP, Fraser WD, Sale C (2017) Effects of reduced energy availability on bone metabolism in women and men. Bone 105:191–199. CrossRefGoogle Scholar
  39. Pereira MA, FitzerGerald SJ, Gregg EW, Joswiak ML, Ryan WJ, Suminski RR, Zmuda JM (1997) A collection of Physical Activity Questionnaires for health-related research. Med Sci Sports Exerc 29(6 Suppl):S1–205Google Scholar
  40. Quick VM, Byrd-Bredbenner C (2013) Eating Disorders Examination Questionnaire (EDE-Q): norms for US college students. Eat Weight Disord 18(1):29–35. CrossRefGoogle Scholar
  41. Smock AJ, Hughes JM, Popp KL, Wetzsteon RJ, Stovitz SD, Kaufman BC, Petit MA (2009) Bone volumetric density, geometry, and strength in female and male collegiate runners. Med Sci Sports Exerc 41(11):2026–2032. CrossRefGoogle Scholar
  42. Stewart AD, Hannan J (2000) Total and regional bone density in male runners, cyclists, and controls. Med Sci Sports Exerc 32(8):1373–1377CrossRefGoogle Scholar
  43. Tam N, Santos-Concejero J, Tucker R, Lamberts RP, Micklesfield LK (2018) Bone health in elite Kenyan runners. J Sports Sci 36(4):456–461. Google Scholar
  44. Tenforde AS, Fredericson M (2011) Influence of sports participation on bone health in the young athlete: a review of the literature. PMR 3(9):861–867. CrossRefGoogle Scholar
  45. Tenforde AS, Fredericson M, Sayres LC, Cutti P, Sainani KL (2015) Identifying sex-specific risk factors for low bone mineral density in adolescent runners. Am J Sports Med 43(6):1494–1504. CrossRefGoogle Scholar
  46. Tenforde AS, Kraus E, Fredericson M (2016) Bone stress injuries in runners. Phys Med Rehabil Clin N Am 27(1):139–149. CrossRefGoogle Scholar
  47. Tenforde AS, Carlson JL, Chang A, Sainani KL, Shultz R, Kim JH, Fredericson M (2017) Association of the female athlete triad risk assessment stratification to the development of bone stress injuries in collegiate athletes. Am J Sports Med 45(2):302–310. CrossRefGoogle Scholar
  48. Tenforde AS, Parziale AL, Popp KL, Ackerman KE (2018) Low bone mineral density in male athletes is associated with bone stress injuries at anatomic sites with greater trabecular composition. Am J Sports Med 46(1):30–36. CrossRefGoogle Scholar
  49. Viner RT, Harris M, Berning JR, Meyer NL (2015) Energy availability and dietary patterns of adult male and female competitive cyclists with lower than expected bone mineral density. Int J Sport Nutr Exerc Metab 25(6):594–602. CrossRefGoogle Scholar
  50. Zanker CL, Swaine IL (2000) Responses of bone turnover markers to repeated endurance running in humans under conditions of energy balance or energy restriction. Eur J Appl Physiol 83(4–5):434–440. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • William P. McCormack
    • 1
    Email author
  • Todd C. Shoepe
    • 1
  • Joseph LaBrie
    • 2
  • Hawley C. Almstedt
    • 1
  1. 1.Department of Health and Human SciencesLoyola Marymount UniversityLos AngelesUSA
  2. 2.Department of PsychologyLoyola Marymount UniversityLos AngelesUSA

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