Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Body composition, energy expenditure and physical activity

Weight-loss-associated changes in bone mineral density and bone turnover after partial weight regain with or without aerobic exercise in obese women

European Journal of Clinical Nutrition volume 66, pages 606–612 (2012)Cite this article

Abstract

BACKGROUND/OBJECTIVES:

Moderate, long-term weight loss results in the loss of bone mass in overweight or obese premenopausal women. However, whether these changes persist during weight maintenance or regain remains to be determined.

SUBJECTS/METHODS:

Overweight or obese (body mass index: 25.8–42.5 kg/m2) women (n=40) with at least two risk factors for the metabolic syndrome participated in this 12-month study that examined the effects of prescribed weight loss and regain, with or without exercise, on bone turnover and on bone mineral density (BMD) in a subset of participants (n=24). During the first 6 month, participants lost ∼10% of their initial body weight via energy restriction and supervised aerobic exercise. Following weight loss, participants were randomly assigned to either an exercise or a no exercise treatment for the regain (+50% of weight lost) phase. A one-way (time) repeated measures one-factor analysis of variance (RMANOVA) tested the effects of weight loss on BMD and bone turnover, and a two-way RMANOVA (time, exercise) was used to examine the effects of exercise during weight regain.

RESULTS:

Hip (P=0.007) and lumbar spine (P=0.05) BMD decreased with weight loss, and remained reduced after weight regain with or without exercise. Likewise, the weight-loss-associated increases in osteocalcin (P<0.001) and C-terminal peptide of type I collagen (P<0.001) persisted following weight regain, independent of exercise.

CONCLUSIONS:

The results of the present study, which is the first to examine changes in bone mass and turnover during carefully controlled weight regain, suggest that weight-loss-induced perturbations in bone mass and turnover persist after partial weight regain, regardless of whether regular weight-bearing aerobic exercise was continued.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2

Similar content being viewed by others

References

  1. Fernandez ML . The metabolic syndrome. Nutr Rev 2007; 65, S30–S34.

    Article  Google Scholar 

  2. Villareal DT, Fontana L, Weiss EP, Racette B, Steger-May K, Schechtman KB et al. Bone mineral density response to caloric restriction-induced weight loss or exercise-induced weight loss: a randomized controlled trial. Arch Intern Med 2006; 166, 2502–2510.

    Article  Google Scholar 

  3. Villareal DT, Shah K, Banks MR, Sinacore DR, Klein S . Effect of weight loss and exercise therapy on bone metabolism and mass in obese older adults: a one-year randomized controlled trial. J Clin Endocrinol Metab 2008; 93, 2181–2187.

    Article  CAS  Google Scholar 

  4. Avenell A, Richmond PR, Lean ME, Reid DM . Bone loss associated with a high fibre weight reduction diet in postmenopausal women. Eur J Clin Nutr 1994; 48, 561–566.

    CAS  PubMed  Google Scholar 

  5. Fogelholm GM, Sievanen HT, Kukkonen-Harjula TK, Pasanen ME . Bone mineral density during reduction, maintenance and regain of body weight in premenopausal, obese women. Osteoporos Int 2001; 12, 199–206.

    Article  CAS  Google Scholar 

  6. Riedt CS, Cifuentes M, Stahl T, Chowdhury HA, Schlussel Y, Shapses SA . Overweight postmenopausal women lose bone with moderate weight reduction and 1 g/day calcium intake. J Bone Miner Res 2005; 20, 455–463.

    Article  CAS  Google Scholar 

  7. Ricci TA, Chowdhury HA, Heymsfield SB, Stahl T, Pierson Jr RN, Shapses SA . Calcium supplementation suppresses bone turnover during weight reduction in postmenopausal women. J Bone Miner Res 1998; 13, 1045–1050.

    Article  CAS  Google Scholar 

  8. Ricci TA, Heymsfield SB, Pierson Jr RN, Stahl T, Chowdhury HA, Shapses SA . Moderate energy restriction increases bone resorption in obese postmenopausal women. Am J Clin Nutr 2001; 73, 347–352.

    Article  CAS  Google Scholar 

  9. Jensen LB, Kollerup G, Quaade F, Sorensen OH . Bone minerals changes in obese women during a moderate weight loss with and without calcium supplementation. J Bone Miner Res 2001; 16, 141–147.

    Article  CAS  Google Scholar 

  10. Pritchard JE, Nowson CA, JD . Bone loss accompanying diet-induced or exercise-induced weight loss: a randomised controlled study. Int J Obes Relat Metab Disord 1996; 20, 513–520.

    CAS  Google Scholar 

  11. Van Loan MD, Johnson HL, Barbieri TF . Effect of weight loss on bone mineral content and bone mineral density in obese women. Am J Clin Nutr 1998; 67, 734–738.

    Article  CAS  Google Scholar 

  12. Rector RS, Loethen J, Ruebel M, Thomas TR, Hinton PS . Serum markers of bone turnover are increased by modest weight loss with or without weight-bearing exercise in overweight premenopausal women. Appl Physiol Nutr Metab 2009; 34, 933–941.

    Article  CAS  Google Scholar 

  13. Villareal DT, Banks M, Sinacore DR, Siener C, Klein S . Effect of weight loss and exercise on frailty in obese older adults. Arch Intern Med 2006; 166, 860–866.

    Article  Google Scholar 

  14. Holecki M, Zahorska-Markiewicz B, Janowska J, Nieszporek T, Wojaczyñska-Stanek K, Zak-Gołab A et al. The influence of weight loss on serum osteoprotegerin concentration in obese perimenopausal women. Obesity 2007; 15, 1925–1929.

    Article  CAS  Google Scholar 

  15. Salamone LM, Cauley JA, Black DM, Simkin-Silverman L, Lang W, Gregg E et al. Effect of a lifestyle intervention on bone mineral density in premenopausal women: a randomized trial. Am J Clin Nutr 1999; 70, 97–103.

    Article  CAS  Google Scholar 

  16. Hinton PS, LeCheminant JD, Smith BK, Rector RS, Donnelly JE . Weight loss-induced alterations in serum markers of bone turnover persist during weight maintenance in obese men and women. J Am Coll Nutr 2009; 28, 565–573.

    Article  CAS  Google Scholar 

  17. Shapses SA, Riedt CS . Bone, body weight, and weight reduction: what are the concerns? J Nutr 2006; 136, 1453–1456.

    Article  CAS  Google Scholar 

  18. Bosy-Westphal A, Later W, Schautz B, Lagerpusch M, Goele K, Heller M et al. Impact of intra- and extra-osseous soft tissue composition on changes in bone mineral density with weight loss and regain. Obesity 2011; 19, 1503–1510.

    Article  Google Scholar 

  19. Riedt CS, Schlussel Y, von Thun N, Ambia-Sobhan H, Stahl T, Field MP et al. Premenopausal overweight women do not lose bone during moderate weight loss with adequate or higher calcium intake. Am J Clin Nutr 2007; 85, 972–980.

    Article  CAS  Google Scholar 

  20. Shapses SA, Von Thun NL, Heymsfield SB, Ricci TA, Ospina M, Pierson Jr RN et al. Bone turnover and density in obese premenopausal women during moderate weight loss and calcium supplementation. J Bone Miner Res 2001; 16, 1329–1336.

    Article  CAS  Google Scholar 

  21. Sukumar D, Ambia-Sobhan H, Zurfluh R, Schlussel Y, Stahl TJ, Gordon CL et al. Areal and volumetric bone mineral density and geometry at two levels of protein intake during caloric restriction: a randomized, controlled trial. J Bone Miner Res 2011; 26, 1339–1348.

    Article  CAS  Google Scholar 

  22. Bowen J, Noakes M, Clifton PM . A high dairy protein, high-calcium diet minimizes bone turnover in overweight adults during weight loss. J Nutr 2004; 134, 568–573.

    Article  CAS  Google Scholar 

  23. Thorpe MP, Jacobson EH, Layman DK, He X, Kris-Etherton PM, Evans EM . A diet high in protein, dairy, and calcium attenuates bone loss over twelve months of weight loss and maintenance relative to a conventional high-carbohydrate diet in adults. J Nutr 2008; 138, 1096–1100.

    Article  CAS  Google Scholar 

  24. Langlois JA, Visser M, Davidovic LS, Maggi S, Li G, Harris TB . Hip fracture risk in older white men is associated with change in body weight from age 50 years to old age. Arch Intern Med 1998; 158, 990–996.

    Article  CAS  Google Scholar 

  25. Langlois JA, Mussolino ME, Visser M, Looker AC, Harris T, Madans J . Weight loss from maximum body weight among middle-aged and older white women and the risk of hip fracture: the NHANES I epidemiologic follow-up study. Osteoporos Int 2001; 12, 763–768.

    Article  CAS  Google Scholar 

  26. Bacon L, Stern JS, Keim NL, Van Loan MD . Low bone mass in premenopausal chronic dieting obese women. Eur J Clin Nutr 2004; 58, 966–971.

    Article  CAS  Google Scholar 

  27. Meyer HE, Tverdal A, Selmer R . Weight variability, weight change and the incidence of hip fracture: a prospective study of 39 000 middle-aged Norwegians. Osteoporos Int 1998; 8, 373–378.

    Article  CAS  Google Scholar 

  28. Bish CL, Blanck HM, Serdula MK, Marcus M, Kohl 3rd HW, Khan LK . Diet and physical activity behaviors among Americans trying to lose weight: 2000 Behavioral Risk Factor Surveillance System. Obes Res 2005; 13, 596–607.

    Article  Google Scholar 

  29. Franz MJ, VanWormer JJ, Crain AL, Boucher JL, Histon T, Caplan W et al. Weight-loss outcomes: a systematic review and meta-analysis of weight-loss clinical trials with a minimum 1-year follow-up. J Am Diet Assoc 2007; 107, 1755–1767.

    Article  Google Scholar 

  30. Vainionpaa A, Korpelainen R, Leppaluoto J, Jamsa T . Effects of high-impact exercise on bone mineral density: a randomized controlled trial in premenopausal women. Osteoporos Int 2005; 16, 191–197.

    Article  Google Scholar 

  31. Nelson ME, Fisher EC, Dilmanian FA, Dallal GE, Evans WJ . A 1-y walking program and increased dietary calcium in postmenopausal women: effects on bone. Am J Clin Nutr 1991; 53, 1304–1311.

    Article  CAS  Google Scholar 

  32. Robling AG, Castillo AB, Turner CH . Biomechanical and molecular regulation of bone remodeling. Annu Rev Biomed Eng 2006; 8, 455–498.

    Article  CAS  Google Scholar 

  33. Borer KT . Physical activity in the prevention and amelioration of osteoporosis in women: interaction of mechanical, hormonal and dietary factors. Sports Med 2005; 35, 779–830.

    Article  Google Scholar 

  34. ACSM. ACSM's Guidelines for Exercise Testing and Prescription. 8th edn. Lippincott, Williams, and Wilkins: Philadelphia, PA, 2009.

  35. Thomas TR, Warner SO, Dellsperger KC, Hinton PS, Whaley-Connell AT, Rector RS et al. Exercise and the metabolic syndrome with weight regain. J Appl Physiol 2010; 109, 3–10.

    Article  CAS  Google Scholar 

  36. Jackson AS . Practical assessment of body composition. Phys Sport Med 1985; 13, 76–90.

    Article  CAS  Google Scholar 

  37. Seibel MJ . Biochemical markers of bone turnover: part I: biochemistry and variability. Clin Biochem Rev 2005; 26, 97–122.

    PubMed  PubMed Central  Google Scholar 

  38. Aubin JE, Liu F, Malaval L, Gupta AK . Osteoblast chondroblast differ. Bone 1995; 17, 77S–83S.

    Article  CAS  Google Scholar 

  39. Christgau S, Bitsch-Jensen O, Hanover Bjarnason N, Gamwell Henriksen E, Qvist P, Alexandersen P et al. Serum CrossLaps for monitoring the response in individuals undergoing antiresorptive therapy. Bone 2000; 26, 505–511.

    Article  CAS  Google Scholar 

  40. Food and Nutrition Board IoM. DRI Dietary Reference Intakes for Calcium, Magnesium, Vitamin D, and Fluoride. National Academy Press: Washington, DC, 1997.

  41. Garnero P, Delmas PD . Contribution of bone mineral density and bone turnover markers to the estimation of risk of osteoporotic fracture in postmenopausal women. J Musculoskelet Neuronal Interact 2004; 4, 50–63.

    CAS  PubMed  Google Scholar 

  42. Bassey EJ, Ramsdale SJ . Increase in femoral bone density in young women following high-impact exercise. Osteoporos Int 1994; 4, 72–75.

    Article  CAS  Google Scholar 

  43. Eickhoff JA, Molczyk L, Gallagher JC, De Jong S . Influence of isotonic, isometric and isokinetic muscle strength on bone mineral density of the spine and femur in young women. Bone Miner 1993; 20, 201–209.

    Article  CAS  Google Scholar 

  44. Andersen RE, Wadden TA, Herzog RJ . Changes in bone mineral content in obese dieting women. Metabolism 1997; 46, 857–861.

    Article  CAS  Google Scholar 

  45. Nakata Y, Ohkawara K, Lee DJ, Okura T, Tanaka K . Effects of additional resistance training during diet-induced weight loss on bone mineral density in overweight premenopausal women. J Bone Miner Metab 2008; 26, 172–177.

    Article  Google Scholar 

  46. Frost HM . On our age-related bone loss: insights from a new paradigm. J Bone Miner Res 1997; 12, 1539–1546.

    Article  CAS  Google Scholar 

  47. Nilsson J, Thorstensson A . Ground reaction forces at different speeds of human walking and running. Acta Physiol Scand 1989; 136, 217–227.

    Article  CAS  Google Scholar 

  48. Wu J, Oka J, Tabata I, Higuchi M, Toda T, Fuku N et al. Effects of isoflavone and exercise on BMD and fat mass in postmenopausal Japanese women: a 1-year randomized placebo-controlled trial. J Bone Miner Res 2006; 21, 780–789.

    Article  CAS  Google Scholar 

  49. Cifuentes M, Riedt CS, Brolin RE, Field MP, Sherrell RM, Shapses SA . Weight loss and calcium intake influence calcium absorption in overweight postmenopausal women. Am J Clin Nutr 2004; 80, 123–130.

    Article  CAS  Google Scholar 

  50. Wagner G, Kindrick S, Hertzler S, DiSilvestro RA . Effects of various forms of calcium on body weight and bone turnover markers in women participating in a weight loss program. J Am Coll Nutr 2007; 26, 456–461.

    Article  CAS  Google Scholar 

  51. Hinton PS, Rector RS, Donnelly JE, Smith BK, Bailey B . Total body bone mineral content and density during weight loss and maintenance on a low- or recommended-dairy weight-maintenance diet in obese men and women. Eur J Clin Nutr 2010; 64, 392–399.

    Article  CAS  Google Scholar 

  52. Lee NK, Sowa H, Hinoi E, Ferron M, Ahn JD, Confavreux C et al. Endocrine regulation of energy metabolism by the skeleton. Cell 2007; 130, 456–469.

    Article  CAS  Google Scholar 

  53. Fernandez-Real JM, Izquierdo M, Ortega F, Gorostiaga E, Gómez-Ambrosi J, Moreno-Navarrete JM et al. The relationship of serum osteocalcin concentration to insulin secretion, sensitivity, and disposal with hypocaloric diet and resistance training. J Clin Endocrinol Metab 2009; 94, 237–245.

    Article  CAS  Google Scholar 

  54. Tothill P . Dual-energy X-ray absorptiometry measurements of total-body bone mineral during weight change. J Clin Densitom 2005; 8, 31–38.

    Article  Google Scholar 

  55. Tothill P, Laskey MA, Orphanidou CI, van Wijk M . Anomalies in dual energy X-ray absorptiometry measurements of total-body bone mineral during weight change using Lunar, Hologic and Norland instruments. Br J Radiol 1999; 72, 661–669.

    Article  CAS  Google Scholar 

  56. Truby H, Hiscutt R, Herriot AM, Stanley M, Delooy A, Fox KR et al. Commercial weight loss diets meet nutrient requirements in free living adults over 8 weeks: a randomised controlled weight loss trial. Nutr J 2008; 7, 25.

    Article  Google Scholar 

  57. Ashley JM, Herzog H, Clodfelter S, Bovee V, Schrage J, Pritsos C . Nutrient adequacy during weight loss interventions: a randomized study in women comparing the dietary intake in a meal replacement group with a traditional food group. Nutr J 2007; 6, 12.

    Article  Google Scholar 

  58. Turner CH, Robling AG . Mechanisms by which exercise improves bone strength. J Bone Miner Metab 2005; 23 (Suppl), 16–22.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the F21C Summer Research Program, the Department of Nutritional Sciences and Exercise Physiology, and NIH ROI DK67036 (TRT).

Author information

Authors and Affiliations

  1. Department of Nutrition and Exercise Physiology, Columbia, MO, USA

    P S Hinton, R S Rector, M A Linden, S O Warner, Y Liu & T R Thomas

  2. Department of,

    R S Rector, K C Dellsperger, A Chockalingam & A T Whaley-Connell

  3. Internal Medicine, Columbia, MO, USA

    R S Rector, K C Dellsperger, A Chockalingam & A T Whaley-Connell

  4. Harry S. Truman Veterans Affairs Medical Center, Columbia, MO, USA

    R S Rector, A Chockalingam & A T Whaley-Connell

  5. Department of Medical Pharmacology and Physiology, Columbia, MO, USA

    K C Dellsperger

Authors
  1. P S Hinton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R S Rector
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M A Linden
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S O Warner
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. K C Dellsperger
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A Chockalingam
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. A T Whaley-Connell
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Y Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. T R Thomas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P S Hinton.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hinton, P., Rector, R., Linden, M. et al. Weight-loss-associated changes in bone mineral density and bone turnover after partial weight regain with or without aerobic exercise in obese women. Eur J Clin Nutr 66, 606–612 (2012). https://doi.org/10.1038/ejcn.2011.212

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ejcn.2011.212

Keywords

This article is cited by

Search

Advanced search

Quick links