Skip to main content

Advertisement

SpringerLink
Log in

Does exercise affect bone mineral density and content when added to a calorie-restricted diet? A systematic review and meta-analysis of controlled clinical trials

  • Review
  • Published:
Osteoporosis International Aims and scope Submit manuscript

Abstract

The effects of exercise in conjunction with weight-loss diets on bone health are mixed. Our objective was to systematically review and meta-analyze controlled clinical trials in adults investigating the addition of exercise to a weight-loss diet compared with a calorie-matched weight-loss diet without exercise on bone measures. Online databases including PubMed/MEDLINE, EMBASE, ISI (Web of Science), Scopus, and Google Scholar were searched up to April 2021 with no restriction. A random effects model was used to calculate the overall estimates. Quality of evidence was assessed using the Grading of Recommendations Assessment, Development and Evaluation (GRADE) methodology. Fourteen eligible controlled clinical trials were included in the systematic review. The meta-analysis revealed that, compared to weight-loss diets alone, the addition of exercise did not improve total body bone mineral density (BMD) [weighted mean difference (WMD) = 0.002 g/cm2, P = 0.62, n = 8], lumbar BMD (WMD = 0.007 g/cm2, P = 0.44, n = 9), total hip BMD (WMD = 0.015 g/cm2, P = 0.14, n = 4) and total bone mineral content (BMC) (WMD =  − 11.97 g, P = 0.29, n = 7). Subgroup analysis revealed that resistance exercise in conjunction with hypocaloric diets positively affects total BMD compared to an energy restrictive diet alone (WMD = 0.01 g/cm2, P = 0.003, n = 3). Overall, it appears that only resistance exercise beneficially affects total BMD during a calorie-restricted diet in adults. Further well-controlled and long-term clinical trials are still needed to confirm these results. PROSPERO registration number: CRD42020173434.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

All generated or analyzed data are included in this article, its supplementary file, and protocol [22].

Abbreviations

BMD:

Bone mineral density

BMC:

Bone mineral content

PRISMA:

Preferred Reporting Items for Systematic Reviews and Meta-Analyses

PROSPERO:

Prospective Register of Systematic Reviews

MeSH:

Medical Subject Headings

WHO:

World Health Organization

BMI:

Body mass index

SD:

Standard deviation

GRADE:

Grading of Recommendations Assessment, Development and Evaluation

SE:

Standard error

WMD:

Weighted mean difference

CIs:

Confidence intervals

I2 :

I-squared

References

  1. Bray G, Kim K, Wilding J, Federation WO (2017) Obesity: a chronic relapsing progressive disease process. A position statement of the World Obesity Federation. Obes Rev 18:715–723

    Article  CAS  PubMed  Google Scholar 

  2. Bosy-Westphal A, Kossel E, Goele K, Later W, Hitze B, Settler U, Heller M, Glüer C-C, Heymsfield SB, Müller MJ (2009) Contribution of individual organ mass loss to weight loss–associated decline in resting energy expenditure. Am J Clin Nutr 90:993–1001

    Article  CAS  PubMed  Google Scholar 

  3. Compston J, Laskey M, Croucher P, Coxon A, Kreitzman S (1992) Effect of diet-induced weight loss on total body bone mass. Clin Sci 82:429–432

    Article  CAS  Google Scholar 

  4. Villareal DT, Apovian CM, Kushner RF, Klein S (2005) Obesity in older adults: technical review and position statement of the American Society for Nutrition and NAASO, The Obesity Society. Am J Clin Nutr 82:923–934

    Article  CAS  PubMed  Google Scholar 

  5. Shah K, Armamento-Villareal R, Parimi N, Chode S, Sinacore DR, Hilton TN, Napoli N, Qualls C, Villareal DT (2011) Exercise training in obese older adults prevents increase in bone turnover and attenuates decrease in hip bone mineral density induced by weight loss despite decline in bone-active hormones. J Bone Miner Res 26:2851–2859

    Article  CAS  PubMed  Google Scholar 

  6. Villareal DT, Chode S, Parimi N, Sinacore DR, Hilton T, Armamento-Villareal R, Napoli N, Qualls C, Shah K (2011) Weight loss, exercise, or both and physical function in obese older adults. N Engl J Med 364:1218–1229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Bolam KA, van Uffelen JG, Taaffe DR (2013) The effect of physical exercise on bone density in middle-aged and older men: a systematic review. Osteoporos Int 24:2749–2762

    Article  CAS  PubMed  Google Scholar 

  8. Martyn-St James M, Carroll S (2006) High-intensity resistance training and postmenopausal bone loss: a meta-analysis. Osteoporos Int 17:1225–1240

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  10. Hosny IA, Elghawabi HS, Younan WBF, Sabbour AA, Gobrial MAM (2012) Beneficial impact of aerobic exercises on bone mineral density in obese premenopausal women under caloric restriction. Skeletal Radiol 41:423–427

    Article  PubMed  Google Scholar 

  11. Serra M, Blumenthal J, Ryan A (2013) Impact of weight loss and aerobic exercise on nutrition and bone mineral density in African American and Caucasian postmenopausal women. J Aging Res Clin Pract 2:11–16

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Beavers DP, Beavers KM, Loeser RF, Walton NR, Lyles MF, Nicklas BJ, Shapses SA, Newman JJ, Messier SP (2014) The independent and combined effects of intensive weight loss and exercise training on bone mineral density in overweight and obese older adults with osteoarthritis. Osteoarthritis Cartilage 22:726–733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Yarizadeh H, Asadi S, Baharlooi H, Setayesh L, Kakavandi NR, Hambly C, Djafarian K, Mirzaei K (2020) Beneficial impact of exercise on bone mass in individuals under calorie restriction: a systematic review and meta-analysis of randomized clinical trials. Crit Rev Food Sci Nutr 61:553–565

  14. Weiss EP, Jordan RC, Frese EM, Albert SG, Villareal DT (2017) Effects of weight loss on lean mass, strength, bone, and aerobic capacity. Med Sci Sports Exerc 49:206–217

    Article  PubMed  PubMed Central  Google Scholar 

  15. Redman LM, Rood J, Anton SD, Champagne C, Smith SR, Ravussin E (2008) Calorie restriction and bone health in young, overweight individuals. Arch Intern Med 168:1859–1866

    Article  PubMed  PubMed Central  Google Scholar 

  16. de Sousa MV, Fukui R, Krustrup P, Pereira R, Silva P, Rodrigues A, de Andrade J, Hernandez A, da Silva MR (2014) Positive effects of football on fitness, lipid profile, and insulin resistance in B razilian patients with type 2 diabetes. Scand J Med Sci Sports 24:57–65

    Article  PubMed  Google Scholar 

  17. Miller T, Mull S, Aragon AA, Krieger J, Schoenfeld BJ (2018) Resistance training combined with diet decreases body fat while preserving lean mass independent of resting metabolic rate: a randomized trial. Int J Sport Nutr Exerc Metab 28:46–54

    Article  CAS  PubMed  Google Scholar 

  18. Nakata Y, Tanaka K, Shigematsu R, Amagai H, Suzuki T (2002) Effects of change in body mass and body composition during body mass reduction on bone mass in obese middle-aged women. Jpn J Phys Fitness Sports Med 51:129–137

    Article  Google Scholar 

  19. Nam S-s, Sunoo S, Park H-y, Moon H-w (2016) The effects of long-term whole-body vibration and aerobic exercise on body composition and bone mineral density in obese middle-aged women. J Exerc Nutr Biochem 20:19–27

    Article  Google Scholar 

  20. St-Onge M, Rabasa-Lhoret R, Strychar I, Faraj M, Doucet É, Lavoie J-M (2013) Impact of energy restriction with or without resistance training on energy metabolism in overweight and obese postmenopausal women: a Montreal Ottawa New Emerging Team group study. Menopause 20:194–201

    Article  PubMed  Google Scholar 

  21. Thompson JL, Gylfadottir UK, Moynihan S, Jensen CD, Butterfield GE (1997) Effects of diet and exercise on energy expenditure in postmenopausal women. Am J Clin Nutr 66:867–873

    Article  CAS  PubMed  Google Scholar 

  22. Beigrezaei S, Yazdanpanah Z, Soltani S, Rajaie SH, Mohseni-Takalloo S, Zohrabi T, Kaviani M, Forbes SC, Baker JS, Salehi-Abargouei A (2021) The effects of exercise and low-calorie diets compared with low-calorie diets alone on health: a protocol for systematic reviews and meta-analyses of controlled clinical trials. Syst Rev 10:1–6

    Article  Google Scholar 

  23. Sterne JA, Hernán MA, Reeves BC, Savović J, Berkman ND, Viswanathan M, Henry D, Altman DG, Ansari MT, Boutron I (2016) ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions. BMJ 355:1–7

  24. Guyatt G, Oxman AD, Akl EA, Kunz R, Vist G, Brozek J, Norris S, Falck-Ytter Y, Glasziou P, DeBeer H (2011) GRADE guidelines: 1. Introduction—GRADE evidence profiles and summary of findings tables. J Clin Epidemiol 64:383–394

    Article  PubMed  Google Scholar 

  25. MUNDY GR, (1999) Bone remodeling. In: Favus MJ (ed) Primer on the metabolic bone diseases and disorders of mineral metabolism. Lippincott Williams & Wilkins, Philadelphia, pp 30–38

    Google Scholar 

  26. Andersen RE, Wadden TA, Herzog RJ (1997) Changes in bone mineral content in obese dieting women. Met Clin and Exp 46:857–861

    Article  CAS  Google Scholar 

  27. Ryan AS, Nicklas BJ, Dennis KE (1998) Aerobic exercise maintains regional bone mineral density during weight loss in postmenopausal women. J Appl Physiol 84:1305–1310

    Article  CAS  PubMed  Google Scholar 

  28. Silverman NE, Nicklas BJ, Ryan AS (2009) Addition of aerobic exercise to a weight loss program increases BMD, with an associated reduction in inflammation in overweight postmenopausal women. Calcif Tissue Int 84:257–265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Beavers KM, Walkup MP, Weaver AA, Lenchik L, Kritchevsky SB, Nicklas BJ, Ambrosius WT, Stitzel JD, Register TC, Shapses SA (2018) Effect of exercise modality during weight loss on bone health in older adults with obesity and cardiovascular disease or metabolic syndrome: a randomized controlled trial. J Bone Miner Res 33:2140–2149

    Article  PubMed  Google Scholar 

  30. Zibellini J, Seimon RV, Lee CM, Gibson AA, Hsu MS, Shapses SA, Nguyen TV, Sainsbury A (2015) Does diet-induced weight loss lead to bone loss in overweight or obese adults? A systematic review and meta-analysis of clinical trials. J Bone Miner Res 30:2168–2178

    Article  CAS  PubMed  Google Scholar 

  31. Soltani S, Hunter G, Kazemi A, Shab-Bidar S (2016) The effects of weight loss approaches on bone mineral density in adults: a systematic review and meta-analysis of randomized controlled trials. Osteoporos Int 27:2655–2671

    Article  CAS  PubMed  Google Scholar 

  32. Kemmler W, Shojaa M, Kohl M, von Stengel S (2020) Effects of different types of exercise on bone mineral density in postmenopausal women: a systematic review and meta-analysis. Calcif Tissue Int 107:409–439

  33. Mason C, Xiao L, Imayama I, Duggan CR, Bain C, Foster-Schubert KE, Kong A, Campbell KL, Wang C-Y, Neuhouser ML (2011) Effects of weight loss on serum vitamin D in postmenopausal women. Am J Clin Nutr 94:95–103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Fukushima N, Hanada R, Teranishi H, Fukue Y, Tachibana T, Ishikawa H, Takeda S, Takeuchi Y, Fukumoto S, Kangawa K (2005) Ghrelin directly regulates bone formation. J Bone Miner Res 20:790–798

    Article  CAS  PubMed  Google Scholar 

  35. Sumithran P, Prendergast LA, Delbridge E, Purcell K, Shulkes A, Kriketos A, Proietto J (2011) Long-term persistence of hormonal adaptations to weight loss. N Engl J Med 365:1597–1604

    Article  CAS  PubMed  Google Scholar 

  36. Oshima K, Nampei A, Matsuda M, Iwaki M, Fukuhara A, Hashimoto J, Yoshikawa H, Shimomura I (2005) Adiponectin increases bone mass by suppressing osteoclast and activating osteoblast. Biochem Biophys Res Commun 331:520–526

    Article  CAS  PubMed  Google Scholar 

  37. Shapses SA, Sukumar D (2012) Bone metabolism in obesity and weight loss. Annu Rev Nutr 32:287–309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. O’dea JP, Wieland RG, Hallberg MC, Llerena LA, Zorn EM, Genuth SM (1979) Effect of dietary weight loss on sex steroid binding, sex steroids, and gonadotropins in obese postmenopausal women. J Lab Clin Med 93:1004–1008

    CAS  PubMed  Google Scholar 

  39. Eriksen EF, Colvard DS, Berg NJ, Graham ML, Mann KG, Spelsberg TC, Riggs BL (1988) Evidence of estrogen receptors in normal human osteoblast-like cells. Science 241:84–86

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  42. Kerr D, Morton A, Dick I, Prince R (1996) Exercise effects on bone mass in postmenopausal women are site-specific and load-dependent. J Bone Miner Res 11:218–225

    Article  CAS  PubMed  Google Scholar 

  43. Maddalozzo G, Snow C (2000) High intensity resistance training: effects on bone in older men and women. Calcif Tissue Int 66:399–404

    Article  CAS  PubMed  Google Scholar 

  44. Wallace B, Cumming R (2000) Systematic review of randomized trials of the effect of exercise on bone mass in pre-and postmenopausal women. Calcif Tissue Int 67:10–18

    Article  CAS  PubMed  Google Scholar 

  45. Williams NI, Leidy HJ, Hill BR, Lieberman JL, Legro RS, Souza MJD (2015) Magnitude of daily energy deficit predicts frequency but not severity of menstrual disturbances associated with exercise and caloric restriction. Am J Physiol Endocrinol Metab 308:E29–E39

    Article  CAS  PubMed  Google Scholar 

  46. Anderson JW, Konz EC, Frederich RC, Wood CL (2001) Long-term weight-loss maintenance: a meta-analysis of US studies. Am J Clin Nutr 74:579–584

    Article  CAS  PubMed  Google Scholar 

  47. Daly RM, Dunstan DW, Owen N, Jolley D, Shaw JE, Zimmet PZ (2005) Does high-intensity resistance training maintain bone mass during moderate weight loss in older overweight adults with type 2 diabetes? Osteoporos Int 16:1703–1712

    Article  PubMed  Google Scholar 

  48. Svendsen OL, Hassager C, Christiansen C (1993) Effect of an energy-restrictive diet, with or without exercise, on lean tissue mass, resting metabolic rate, cardiovascular risk factors, and bone in overweight postmenopausal women. Am J Med 95:131–140

    Article  CAS  PubMed  Google Scholar 

  49. Kanis JA (2002) Diagnosis of osteoporosis and assessment of fracture risk. Lancet (London, England) 359:1929–1936

    Article  Google Scholar 

  50. Brownbill RA, Ilich JZ (2005) Measuring body composition in overweight individuals by dual energy x-ray absorptiometry. BMC Med Imaging 5:1–7

    Article  PubMed  PubMed Central  Google Scholar 

  51. Pisani P, Renna MD, Conversano F, Casciaro E, Muratore M, Quarta E, Di Paola M, Casciaro S (2013) Screening and early diagnosis of osteoporosis through X-ray and ultrasound based techniques. World J Radiol 5:398

    Article  PubMed  PubMed Central  Google Scholar 

  52. Mckee H, Beattie K, Lau A, Wong A, Adachi R (2017) Novel imaging modalities in the diagnosis and risk stratification of osteoporosis. J Orthop Ther 2017:1–9

    Google Scholar 

  53. Burian E, Syväri J, Dieckmeyer M, Holzapfel C, Drabsch T, Sollmann N, Kirschke JS, Rummeny EJ, Zimmer C, Hauner H (2020) Age-and BMI-related variations of fat distribution in sacral and lumbar bone marrow and their association with local muscle fat content. Sci Rep 10:1–8

    Article  Google Scholar 

  54. Wehrli FW, Hopkins JA, Hwang SN, Song HK, Snyder PJ, Haddad JG (2000) Cross-sectional study of osteopenia with quantitative MR imaging and bone densitometry. Radiology 217:527–538

    Article  CAS  PubMed  Google Scholar 

  55. Rantalainen T, Nikander R, Heinonen A, Cervinka T, Sievänen H, Daly RM (2013) Differential effects of exercise on tibial shaft marrow density in young female athletes. J Clin Endocrinol Metab 98:2037–2044

    Article  CAS  PubMed  Google Scholar 

  56. Chandran M, Hough F, Lee K (2010) Is BMD measurement still useful with the advent of the FRAX fracture risk assessment tool. Medicographia 32:49–58

    Google Scholar 

  57. Pappou IP, Girardi FP, Sandhu HS, Parvataneni HK, Cammisa FP Jr, Schneider R, Frelinghuysen P, Lane JM (2006) Discordantly high spinal bone mineral density values in patients with adult lumbar scoliosis. Spine 31:1614–1620

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the research council of Nutrition and Food Security Research Center, Shahid Sadoughi University of Medical Sciences for scientific support of the present study.

Funding

The present systematic review was financially supported by Nutrition and Food Security research center, Shahid Sadoughi University of Medical Sciences, Yazd, Iran.

Author information

Authors and Affiliations

  1. Department of Nutrition, Faculty of Health, School of Public Health, Shahid Sadoughi University of Medical Sciences, PO Code 8915173160 , Yazd, Iran

    Zeinab Yazdanpanah, Sara Beigrezaei, Sahar Mohseni-Takalloo, Seyede Hamide Rajaie, Tayebeh Zohrabi & Amin Salehi-Abargouei

  2. Nutrition and Food Security Research Center, Shahid Sadoughi University of Medical Sciences, Yazd, Iran

    Zeinab Yazdanpanah, Sara Beigrezaei, Sahar Mohseni-Takalloo, Seyede Hamide Rajaie, Tayebeh Zohrabi & Amin Salehi-Abargouei

  3. Noncommunicable Diseases Research Center, Bam University of Medical Sciences, Bam, Iran

    Sahar Mohseni-Takalloo

  4. Yazd Cardiovascular Research Center, Shahid Sadoughi University of Medical Sciences, Yazd, Iran

    Sepideh Soltani

  5. School of Nutrition and Dietetics, Faculty of Pure & Applied Science, Acadia University, Wolfville, NS, Canada

    Mojtaba Kaviani

  6. Department of Physical Education Studies, Faculty of Education, Brandon University, Brandon, MB, Canada

    Scott C. Forbes

  7. Centre for Health and Exercise Science Research, Department of Sport, Physical Education and Health, Hong Kong Baptist University, Kowloon Tong, Hong Kong

    Julien S. Baker

Authors
  1. Zeinab Yazdanpanah
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sara Beigrezaei
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sahar Mohseni-Takalloo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sepideh Soltani
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Seyede Hamide Rajaie
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tayebeh Zohrabi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mojtaba Kaviani
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Scott C. Forbes
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Julien S. Baker
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Amin Salehi-Abargouei
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Amin Salehi-Abargouei.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Conflict of interest

None.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 24 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yazdanpanah, Z., Beigrezaei, S., Mohseni-Takalloo, S. et al. Does exercise affect bone mineral density and content when added to a calorie-restricted diet? A systematic review and meta-analysis of controlled clinical trials. Osteoporos Int 33, 339–354 (2022). https://doi.org/10.1007/s00198-021-06187-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-021-06187-9

Keywords

Search

Navigation