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Associations between exercise, bone mineral density, and body composition in adolescents with anorexia nervosa

  • Jason M. Nagata
  • Jennifer L. Carlson
  • Neville H. Golden
  • Stuart B. Murray
  • Jin Long
  • Mary B. Leonard
  • Rebecka Peebles
Brief Report

Abstract

Objective

To identify the effect of duration of weight-bearing exercise and team sports participation on bone mineral density (BMD) and body composition among adolescents with anorexia nervosa (AN).

Method

We retrospectively reviewed electronic medical records of all patients 9–20 years old with a DSM-5 diagnosis of AN evaluated by the Stanford Eating Disorders Program (1997–2011) who underwent dual-energy X-ray absorptiometry.

Results

A total of 188 adolescents with AN were included (178 females and 10 males). Using multivariate linear regression, duration of weight-bearing exercise (B = 0.15, p = 0.005) and participation in team sports (B = 0.53, p = 0.001) were associated with higher BMD at the hip and team sports (B = 0.39, p = 0.006) were associated with higher whole body BMC, controlling for covariates. Participation in team sports (B = − 1.06, p = 0.007) was associated with greater deficits in FMI Z-score. LBMI Z-score was positively associated with duration of weight-bearing exercise (B = 0.10, p = 0.018) and may explain the relationship between exercise and bone outcomes.

Conclusion

Duration of weight-bearing exercise and team sports participation may be protective of BMD at the hip and whole body BMC, while participation in team sports was associated with greater FMI deficits among adolescents with AN.

Level of evidence

Level V, descriptive retrospective study.

Keywords

Eating disorders Dual-energy X-ray absorptiometry DXA Bone density Bone health Body composition Exercise Sports 

Notes

Acknowledgements

The authors thank Laura Bachrach for advice in study design; Audrey Chang, Alaina Critchlow, and Jessica Kao for help with data collection; and Nicole Capdarest-Arest for help with the literature searches.

Funding

Supported by the National Institutes of Health (K23DK100558 to RP, K23 MH115184 to SM, and 5R01HD08216602 to NG); the Pediatric Scientist Development Program (K12 HD000850) supported by the American Academy of Pediatrics and American Pediatric Society to JN; and the Hilda and Preston Davis Foundation to RP.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Ethical approval

All procedures performed in this study were in accordance with the ethical standards of the university’s Institutional Review Board and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed Consent

Because data were retrospectively collected and anonymized, a waiver of informed consent was approved by the Stanford University Committee on Human Research (IRB).

Supplementary material

40519_2018_521_MOESM1_ESM.tif (32 kb)
Flow diagram of included study participants (TIF 31 KB)
40519_2018_521_MOESM2_ESM.docx (16 kb)
Supplementary material 2 (DOCX 16 KB)
40519_2018_521_MOESM3_ESM.docx (15 kb)
Supplementary material 3 (DOCX 15 KB)
40519_2018_521_MOESM4_ESM.docx (15 kb)
Supplementary material 4 (DOCX 14 KB)
40519_2018_521_MOESM5_ESM.xlsx (42 kb)
Supplementary material 5 (XLSX 41 KB)

References

  1. 1.
    Katzman DK (2005) Medical complications in adolescents with anorexia nervosa: a review of the literature. Int J Eat Disord.  https://doi.org/10.1002/eat.20118 (37 Suppl:S52-9; discussion S87-9)Google Scholar
  2. 2.
    Sachs KV, Harnke B, Mehler PS, Krantz MJ (2016) Cardiovascular complications of anorexia nervosa: a systematic review. Int J Eat Disord 49:238–248  https://doi.org/10.1002/eat.22481 CrossRefPubMedGoogle Scholar
  3. 3.
    Misra M, Klibanski A (2014) Anorexia nervosa and bone. J Endocrinol 221:R163-76.  https://doi.org/10.1530/JOE-14-0039 CrossRefPubMedGoogle Scholar
  4. 4.
    Solmi M, Veronese N, Correll CU, Favaro A, Santonastaso P, Caregaro L, Vancampfort D, Luchini C, De Hert M, Stubbs B (2016) Bone mineral density, osteoporosis, and fractures among people with eating disorders: a systematic review and meta-analysis. Acta Psychiatr Scand 133:341–351.  https://doi.org/10.1111/acps.12556 CrossRefPubMedGoogle Scholar
  5. 5.
    Nagata JM, Golden NH, Peebles R, Long J, Leonard MB, Carlson JL (2017) Assessment of sex differences in bone deficits among adolescents with anorexia nervosa. Int J Eat Disord 50:352–358.  https://doi.org/10.1002/eat.22626 CrossRefPubMedGoogle Scholar
  6. 6.
    Vestergaard P, Emborg C, Stoving RK, Hagen C, Mosekilde L, Brixen K (2002) Fractures in patients with anorexia nervosa, bulimia nervosa, and other eating disorders–a nationwide register study. Int J Eat Disord 32:301–308.  https://doi.org/10.1002/eat.10101 CrossRefPubMedGoogle Scholar
  7. 7.
    Faje AT, Karim L, Taylor A, Lee H, Miller KK, Mendes N, Meenaghan E, Goldstein MA, Bouxsein ML, Misra M et al (2013) Adolescent girls with anorexia nervosa have impaired cortical and trabecular microarchitecture and lower estimated bone strength at the distal radius. J Clin Endocrinol Metab 98:1923–1929.  https://doi.org/10.1210/jc.2012-4153 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Nagata JM, Golden NH, Leonard MB, Copelovitch L, Denburg MR (2017) Assessment of sex differences in fracture risk among patients with anorexia nervosa: a population-based cohort study using the health improvement network. J Bone Miner Res 32:1082–1089.  https://doi.org/10.1002/jbmr.3068 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    DiVasta AD, Feldman HA, O’Donnell JM, Long J, Leonard MB, Gordon CM (2017) Effect of exercise and antidepressants on skeletal outcomes in adolescent girls with anorexia nervosa. J Adolesc Health 60:229–232CrossRefPubMedGoogle Scholar
  10. 10.
    Misra M, Katzman DK, Cord J, Manning SJ, Mickley D, Herzog DB, Miller KK, Klibanski A (2008) Percentage extremity fat, but not percentage trunk fat, is lower in adolescent boys with anorexia nervosa than in healthy adolescents. Am J Clin Nutr 88:1478–1484.  https://doi.org/10.3945/ajcn.2008.26273 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Warren MP (2011) Endocrine manifestations of eating disorders. J Clin Endocrinol Metab 96:333–343.  https://doi.org/10.1210/jc.2009-2304 CrossRefPubMedGoogle Scholar
  12. 12.
    Scofield KL, Hecht S (2012) Bone health in endurance athletes: runners, cyclists, and swimmers. Curr Sports Med Rep 11:328–334.  https://doi.org/10.1249/JSR.0b013e3182779193 CrossRefPubMedGoogle Scholar
  13. 13.
    Bielemann RM, Domingues MR, Horta BL, Gigante DP (2014) Physical activity from adolescence to young adulthood and bone mineral density in young adults from the 1982 Pelotas (Brazil) Birth Cohort. Prev Med 62:201–207.  https://doi.org/10.1016/j.ypmed.2014.02.014 CrossRefPubMedGoogle Scholar
  14. 14.
    Wetzsteon RJ, Zemel BS, Shults J, Howard KM, Kibe LW, Leonard MB (2011) Mechanical loads and cortical bone geometry in healthy children and young adults. Bone 48:1103–1108.  https://doi.org/10.1016/j.bone.2011.01.005 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Petit MA, Beck TJ, Shults J, Zemel BS, Foster BJ, Leonard MB (2005) Proximal femur bone geometry is appropriately adapted to lean mass in overweight children and adolescents. Bone 36:568–576CrossRefPubMedGoogle Scholar
  16. 16.
    Tenforde AS, Fredericson M (2011) Influence of sports participation on bone health in the young athlete: a review of the literature. PM R 3:861–867.  https://doi.org/10.1016/j.pmrj.2011.05.019 CrossRefPubMedGoogle Scholar
  17. 17.
    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. Br J Sports Med 39:282–287CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Nagata JM, Carlson JL, Kao JM, Golden NH, Murray SB, Peebles R (2017) Characterization and correlates of exercise among adolescents with anorexia nervosa and bulimia nervosa. Int J Eat Disord 50:1394–1403.  https://doi.org/10.1002/eat.22796 CrossRefPubMedGoogle Scholar
  19. 19.
    American Psychiatric Association (2013) Diagnostic and Statistical Manual of Mental Disorders. American Psychiatric Association, WashingtonCrossRefGoogle Scholar
  20. 20.
    American Psychiatric Association (1990) Diagnostic and statistical manual of mental disorders. American Psychiatric Association, WashingtonGoogle Scholar
  21. 21.
    Centers for Disease Control, C.D.C (2000) Growth charts. http://www.cdc.gov/growthcharts/
  22. 22.
    Society for Adolescent Health and Medicine, Golden NH, Katzman DK, Sawyer SM, Ornstein RM, Rome ES, Garber AK, Kohn M, Kreipe RE (2015) Position Paper of the Society for Adolescent Health and Medicine: medical management of restrictive eating disorders in adolescents and young adults. J Adolesc Health 56:121–125.  https://doi.org/10.1016/j.jadohealth.2014.10.259 CrossRefGoogle Scholar
  23. 23.
    Yoon V, Maalouf NM, Sakhaee K (2012) The effects of smoking on bone metabolism. Osteoporos Int 23:2081–2092.  https://doi.org/10.1007/s00198-012-1940-y CrossRefPubMedGoogle Scholar
  24. 24.
    Ak E, Bulut SD, Bulut S, Akdag HA, Oter GB, Kaya H, Kaya OB, Sengul CB, Kisa C (2015) Evaluation of the effect of selective serotonin reuptake inhibitors on bone mineral density: an observational cross-sectional study. Osteoporos Int 26:273–279.  https://doi.org/10.1007/s00198-014-2859-2 CrossRefPubMedGoogle Scholar
  25. 25.
    Rauma PH, Honkanen RJ, Williams LJ, Tuppurainen MT, Kroger HP, Koivumaa-Honkanen H (2016) Effects of antidepressants on postmenopausal bone loss—a 5-year longitudinal study from the OSTPRE cohort. Bone 89:25–31CrossRefPubMedGoogle Scholar
  26. 26.
    Zemel BS, Kalkwarf HJ, Gilsanz V, Lappe JM, Oberfield S, Shepherd JA, Frederick MM, Huang X, Lu M, Mahboubi S et al (2011) Revised reference curves for bone mineral content and areal bone mineral density according to age and sex for black and non-black children: results of the bone mineral density in childhood study. J Clin Endocrinol Metab 96:3160–3169.  https://doi.org/10.1210/jc.2011-1111 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Zemel BS, Leonard MB, Kelly A, Lappe JM, Gilsanz V, Oberfield S, Mahboubi S, Shepherd JA, Hangartner TN, Frederick MM et al (2010) Height adjustment in assessing dual energy X-ray absorptiometry measurements of bone mass and density in children. J Clin Endocrinol Metab 95:1265–1273.  https://doi.org/10.1210/jc.2009-2057 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Weber DR, Moore RH, Leonard MB, Zemel BS (2013) Fat and lean BMI reference curves in children and adolescents and their utility in identifying excess adiposity compared with BMI and percentage body fat. Am J Clin Nutr 98:49–56.  https://doi.org/10.3945/ajcn.112.053611 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Misra M, Katzman DK, Clarke H, Snelgrove D, Brigham K, Miller KK, Klibanski A (2013) Hip structural analysis in adolescent boys with anorexia nervosa and controls. J Clin Endocrinol Metab 98:2952–2958.  https://doi.org/10.1210/jc.2013-1457 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Misra M, Katzman DK, Cord J, Manning SJ, Mendes N, Herzog DB, Miller KK, Klibanski A (2008) Bone metabolism in adolescent boys with anorexia nervosa. J Clin Endocrinol Metab 93:3029–3036.  https://doi.org/10.1210/jc.2008-0170 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Mudd LM, Fornetti W, Pivarnik JM (2007) Bone mineral density in collegiate female athletes: comparisons among sports. J Athl Train 42:403–408PubMedPubMedCentralGoogle Scholar
  32. 32.
    Warden SJ, Mantila Roosa SM, Kersh ME, Hurd AL, Fleisig GS, Pandy MG, Fuchs RK (2014) Physical activity when young provides lifelong benefits to cortical bone size and strength in men. Proc Natl Acad Sci U S A 111:5337–5342.  https://doi.org/10.1073/pnas.1321605111 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Nilsson M, Sundh D, Ohlsson C, Karlsson M, Mellstrom D, Lorentzon M (2014) Exercise during growth and young adulthood is independently associated with cortical bone size and strength in old Swedish men. J Bone Miner Res 29:1795–1804.  https://doi.org/10.1002/jbmr.2212 CrossRefPubMedGoogle Scholar
  34. 34.
    Nattiv A, Loucks AB, Manore MM, Sanborn CF, Sundgot-Borgen J, Warren MP, American College of Sports Medicine (2007) American College of Sports Medicine position stand. The female athlete triad. Med Sci Sports Exerc 39:1867–1882.  https://doi.org/10.1249/mss.0b013e318149f111 CrossRefPubMedGoogle Scholar
  35. 35.
    Golden NH, Katzman DK, Sawyer SM, Ornstein RM, Rome ES, Garber AK, Kohn M, Kreipe RE (2015) Update on the medical management of eating disorders in adolescents. J Adolesc Health 56:370–375.  https://doi.org/10.1016/j.jadohealth.2014.11.020 CrossRefPubMedGoogle Scholar
  36. 36.
    Joy E, Kussman A, Nattiv A (2016) 2016 update on eating disorders in athletes: a comprehensive narrative review with a focus on clinical assessment and management. Br J Sports Med 50:154–162.  https://doi.org/10.1136/bjsports-2015-095735 CrossRefPubMedGoogle Scholar
  37. 37.
    Achamrah N, Coeffier M, Dechelotte P (2016) Physical activity in patients with anorexia nervosa. Nutr Rev 74:301–311.  https://doi.org/10.1093/nutrit/nuw001 CrossRefPubMedGoogle Scholar
  38. 38.
    Sundgot-Borgen J, Rosenvinge JH, Bahr R, Schneider LS (2002) The effect of exercise, cognitive therapy, and nutritional counseling in treating bulimia nervosa. Med Sci Sports Exerc 34:190–195CrossRefPubMedGoogle Scholar
  39. 39.
    Ng LW, Ng DP, Wong WP (2013) Is supervised exercise training safe in patients with anorexia nervosa? a meta-analysis. Physiotherapy 99:1–11.  https://doi.org/10.1016/j.physio.2012.05.006 CrossRefPubMedGoogle Scholar
  40. 40.
    Vancampfort D, Vanderlinden J, De Hert M, Soundy A, Adamkova M, Skjaerven LH, Catalan-Matamoros D, Lundvik Gyllensten A, Gomez-Conesa A, Probst M (2014) A systematic review of physical therapy interventions for patients with anorexia and bulemia nervosa. Disabil Rehabil 36:628–634.  https://doi.org/10.3109/09638288.2013.808271 CrossRefPubMedGoogle Scholar
  41. 41.
    Noetel M, Miskovic-Wheatley J, Crosby RD, Hay P, Madden S, Touyz S (2016) A clinical profile of compulsive exercise in adolescent inpatients with anorexia nervosa. J Eat Disord.  https://doi.org/10.1186/s40337-016-0090-6 PubMedPubMedCentralGoogle Scholar
  42. 42.
    Nagata JM, Golden NH, Peebles R, Long J, Murray SB, Leonard MB, Carlson JL (2017) Assessment of sex differences in body composition among adolescents with anorexia nervosa. J Adolesc Health 60:455–459.  https://doi.org/10.1016/j.jadohealth.2016.11.005 CrossRefPubMedGoogle Scholar
  43. 43.
    Misra M, Aggarwal A, Miller KK, Almazan C, Worley M, Soyka LA, Herzog DB, Klibanski A (2004) Effects of anorexia nervosa on clinical, hematologic, biochemical, and bone density parameters in community-dwelling adolescent girls. Pediatrics 114:1574–1583 pii].CrossRefPubMedGoogle Scholar
  44. 44.
    Holm-Denoma JM, Scaringi V, Gordon KH, Van Orden KA, Joiner TE (2009) Eating disorder symptoms among undergraduate varsity athletes, club athletes, independent exercisers, and nonexercisers. Int J Eat Disord 42:47–53.  https://doi.org/10.1002/eat.20560 CrossRefPubMedGoogle Scholar
  45. 45.
    Sundgot-Borgen J, Torstveit MK (2004) Prevalence of eating disorders in elite athletes is higher than in the general population. Clin J Sport Med 14:25–32CrossRefPubMedGoogle Scholar
  46. 46.
    Leonard MB, Zemel BS, Wrotniak BH, Klieger SB, Shults J, Stallings VA, Stettler N (2015) Tibia and radius bone geometry and volumetric density in obese compared to non-obese adolescents. Bone 73:69–76.  https://doi.org/10.1016/j.bone.2014.12.002 CrossRefPubMedGoogle Scholar
  47. 47.
    Callewaert F, Sinnesael M, Gielen E, Boonen S, Vanderschueren D (2010) Skeletal sexual dimorphism: relative contribution of sex steroids, GH-IGF1, and mechanical loading. J Endocrinol 207:127–134.  https://doi.org/10.1677/JOE-10-0209 CrossRefPubMedGoogle Scholar
  48. 48.
    Wren TA, Shepherd JA, Kalkwarf HJ, Zemel BS, Lappe JM, Oberfield S, Dorey FJ, Winer KK, Gilsanz V (2012) Racial disparity in fracture risk between white and nonwhite children in the United States. J Pediatr 161:1035–1040.  https://doi.org/10.1016/j.jpeds.2012.07.054 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of PediatricsStanford University School of MedicinePalo AltoUSA
  2. 2.Department of PediatricsUniversity of California, San FranciscoSan FranciscoUSA
  3. 3.Department of PsychiatryUniversity of California, San FranciscoSan FranciscoUSA
  4. 4.Department of PediatricsChildren’s Hospital of PhiladelphiaPhiladelphiaUSA

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