Abstract
Purpose
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.
Methods
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.
Results
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.
Conclusion
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.
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Abbreviations
- ANCOVA:
-
Analysis of covariance
- AP:
-
Anterior–posterior
- BMD:
-
Bone mineral density
- BMI:
-
Body mass index
- DXA:
-
Dual-energy X-ray absorptiometry
- EA:
-
Energy availability
- EDEQ:
-
Eating Disorder Examination Questionnaire
- EEE:
-
Exercise energy expenditure
- EI:
-
Energy intake
- FFM:
-
Fat-free mass
- FFQ:
-
Food Frequency Questionnaire
- MET:
-
Metabolic equivalent
- RED-S:
-
Relative energy deficiency in sport
- RMR:
-
Resting metabolic rate
References
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. https://doi.org/10.1249/MSS.0b013e31821ece12
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. https://doi.org/10.1177/0145445503259851
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):36–43
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. https://doi.org/10.1177/0363546513520295
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. https://doi.org/10.1136/bjsports-2016-096698
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):160–175
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. https://doi.org/10.1002/jbmr.412
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):1119–1130
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):1327–1335
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):686–693
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):269–278
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. https://doi.org/10.1123/ijsnem.2018-0182
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. https://doi.org/10.1123/ijsnem.2018-0142
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. https://doi.org/10.1093/ajcn/54.6.963
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. https://doi.org/10.1016/j.eatbeh.2013.04.002
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 York
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. https://doi.org/10.1136/bjsm.2006.030783 (discussion 668)
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. https://doi.org/10.1249/mss.0b013e318213fefb
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. https://doi.org/10.1123/ijsnem.2012-0165
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. https://doi.org/10.1097/JES.0b013e318236e5ee
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):305–315
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. https://doi.org/10.1123/ijsnem.2017-0313
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. https://doi.org/10.1016/j.bone.2006.03.012
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. https://doi.org/10.1007/s00421-011-2008-y
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. https://doi.org/10.1359/JBMR.040410
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. https://doi.org/10.1007/s00421-005-0060-1
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. https://doi.org/10.1139/apnm-2012-0373
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):1228–1239
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):1985–1996
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):391–398
Loucks AB (2004) Energy balance and body composition in sports and exercise. J Sports Sci 22(1):1–14. https://doi.org/10.1080/0264041031000140518
Loucks AB, Kiens B, Wright HH (2011) Energy availability in athletes. J Sports Sci 29(Suppl 1):S7–15. https://doi.org/10.1080/02640414.2011.588958
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. https://doi.org/10.1016/j.eatbeh.2006.04.003
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. https://doi.org/10.1111/sms.12261
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. https://doi.org/10.1136/bjsports-2014-093502
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. https://doi.org/10.1123/ijsnem.2018-0136
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.0b013e318149f11100005768-200710000-00026
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. https://doi.org/10.1016/j.bone.2017.08.019
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):S1–205
Quick VM, Byrd-Bredbenner C (2013) Eating Disorders Examination Questionnaire (EDE-Q): norms for US college students. Eat Weight Disord 18(1):29–35. https://doi.org/10.1007/s40519-013-0015-1
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. https://doi.org/10.1249/MSS.0b013e3181a7a5a2
Stewart AD, Hannan J (2000) Total and regional bone density in male runners, cyclists, and controls. Med Sci Sports Exerc 32(8):1373–1377
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. https://doi.org/10.1080/02640414.2017.1313998
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. https://doi.org/10.1016/j.pmrj.2011.05.019
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. https://doi.org/10.1177/0363546515572142
Tenforde AS, Kraus E, Fredericson M (2016) Bone stress injuries in runners. Phys Med Rehabil Clin N Am 27(1):139–149. https://doi.org/10.1016/j.pmr.2015.08.008
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. https://doi.org/10.1177/0363546516676262
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. https://doi.org/10.1177/0363546517730584
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. https://doi.org/10.1123/ijsnem.2015-0073
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. https://doi.org/10.1007/s004210000293
Acknowledgements
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.
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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.
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Communicated by Olivier Seynnes.
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McCormack, W.P., Shoepe, T.C., LaBrie, J. et al. Bone mineral density, energy availability, and dietary restraint in collegiate cross-country runners and non-running controls. Eur J Appl Physiol 119, 1747–1756 (2019). https://doi.org/10.1007/s00421-019-04164-z
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DOI: https://doi.org/10.1007/s00421-019-04164-z