Skip to main content
SpringerLink
Log in

Changes in thigh muscle volume predict bone mineral density response to lifestyle therapy in frail, obese older adults

  • Original Article
  • Published:
Osteoporosis International Aims and scope Submit manuscript

Abstract

Summary

We studied the relationships among strength, muscle mass, and bone mineral density (BMD) with lifestyle change. Lifestyle therapy consisted of exercise, diet, and diet plus exercise. Diet was by caloric restriction to induce and maintain a weight loss of 10 % from baseline body weight. Exercise attenuated weight loss-induced muscle and bone losses. Exercise improved strength despite muscle loss in patients on diet and exercise. Changes in strength did not correlate with changes in BMD. However, changes in thigh muscle volume correlated with, and predicted changes in hip BMD.

Introduction

Losses of hip BMD and lean body mass are major complications of lifestyle therapy in frail, obese older adults; however, the contribution of mechanical strain loss from muscle loss is poorly defined. We determined the effect of changes in thigh muscle volume and muscle strength on BMD in frail, obese older adults undergoing lifestyle therapy aimed at intentional weight loss with or without exercise.

Methods

One hundred seven obese older adults were randomized to control, diet, exercise, and diet–exercise groups for 1 year. Thigh muscle volume was measured by magnetic resonance imaging, BMD by DXA, knee strength by dynamometry, total strength by one-repetition maximum (1-RM), and bone markers by immunoassay.

Results

Thigh muscle volume decreased in the diet group (−6.2 ± 4.8 %) and increased in the exercise group (2.7 ± 3.1 %), while it was not significantly different from the control in the diet–exercise group. Changes in hip BMD followed similar pattern as those in thigh muscle volume. Knee extension and flexion increased in the exercise group (23 ± 20 %; 25 ± 19 %) and diet–exercise group (20 ± 19 %; 20.6 ± 27 %) but were unchanged in the control and diet groups. Changes in thigh muscle volume correlated with changes in hip BMD (r = 0.55, P = <0.001) and were an independent predictor of changes in hip BMD (β = 0.12, P = 0.03) in the multiple regression analyses after accounting for demographic factors and changes in weight and physical activity. There were no correlations between BMD changes and knee strength, 1-RM, and sclerostin changes.

Conclusions

Changes in thigh muscle volume predict hip BMD changes in obese older patients undergoing lifestyle therapy. The effect of exercise in attenuating thigh muscle loss when added to diet may in part account for the reduction in weight loss-induced bone loss in the diet–exercise group.

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
Fig. 3

Similar content being viewed by others

Reference

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  2. Shah K, Armamento-Villareal R, Parimi N, Chode S, Sinacore DR, Hilton TN et al (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 Central  PubMed  Google Scholar 

  3. Armamento-Villareal R, Sadler C, Napoli N, Shah K, Chode S, Sinacore DR et al (2012) Weight loss in obese older adults increases serum sclerostin and impairs hip geometry but both are prevented by exercise training. J Bone Miner Res 27:1215–1221

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  4. Hoshikawa Y, Iida T, Muramatsu M, Ii N, Nakajima Y, Chumank K et al. (2013) Thigh muscularity and strength in teenage soccer players. Int J Sports Med 34(5):415–23.

    Google Scholar 

  5. Villareal DT, Holloszy JO (2006) DHEA enhances effects of weight training on muscle mass and strength in elderly women and men. Am J Physiol Endocrinol Metab 291:E1003–E1008

    Article  CAS  PubMed  Google Scholar 

  6. Weiss EP, Racette SB, Villareal DT, Fontana L, Steger-May K, Schechtman KB et al (2007) Lower extremity muscle size and strength and aerobic capacity decrease with caloric restriction but not with exercise-induced weight loss. J Appl Physiol 102:634–640

    Article  PubMed  Google Scholar 

  7. Napoli N, Villareal DT, Mumm S, Halstead L, Sheikh S, Cagaanan M et al (2005) Effect of CYP1A1 gene polymorphisms on estrogen metabolism and bone density. J Bone Miner Res 20:232–239

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  9. Youm T, Koval KJ, Kummer FJ, Zuckerman JD (1999) Do all hip fractures result from a fall? Am J Orthop (Belle Mead NJ) 28:190–194

    CAS  Google Scholar 

  10. Tinetti ME, Speechley M, Ginter SF (1988) Risk factors for falls among elderly persons living in the community. N Engl J Med 319:1701–1707

    Article  CAS  PubMed  Google Scholar 

  11. Nevitt MC, Cummings SR, Kidd S, Black D (1989) Risk factors for recurrent nonsyncopal falls. A prospective study. JAMA 261:2663–2668

    Article  CAS  PubMed  Google Scholar 

  12. Lord SR, Ward JA, Williams P, Anstey KJ (1994) Physiological factors associated with falls in older community-dwelling women. J Am Geriatr Soc 42:1110–1117

    CAS  PubMed  Google Scholar 

  13. Cummings SR, Nevitt MC, Browner WS, Stone K, Fox KM, Ensrud KE et al (1995) Risk factors for hip fracture in white women. Study of Osteoporotic Fractures Research Group. N Engl J Med 332:767–773

    Article  CAS  PubMed  Google Scholar 

  14. Marsh AP, Rejeski WJ, Espeland MA, Miller ME, Church TS, Fielding RA et al (2011) Muscle strength and BMI as predictors of major mobility disability in the Lifestyle Interventions and Independence for Elders pilot (LIFE-P). J Gerontol A Biol Sci Med Sci 66:1376–1383

    Article  PubMed  Google Scholar 

  15. Fiatarone MA, Marks EC, Ryan ND, Meredith CN, Lipsitz LA, Evans WJ (1990) High-intensity strength training in nonagenarians. Effects on skeletal muscle. JAMA 263:3029–3034

    Article  CAS  PubMed  Google Scholar 

  16. Korpelainen R, Keinanen-Kiukaanniemi S, Heikkinen J, Vaananen K, Korpelainen J (2006) Effect of exercise on extraskeletal risk factors for hip fractures in elderly women with low BMD: a population-based randomized controlled trial. J Bone Miner Res 21:772–779

    Article  PubMed  Google Scholar 

  17. Villareal DT, Banks M, Siener C, Sinacore DR, Klein S (2004) Physical frailty and body composition in obese elderly men and women. Obes Res 12:913–920

    Article  PubMed  Google Scholar 

  18. Roubenoff R (2004) Sarcopenic obesity: the confluence of two epidemics. Obes Res 12:887–888

    Article  PubMed  Google Scholar 

  19. 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 

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

    CAS  PubMed  Google Scholar 

  21. Lebrasseur NK, Achenbach SJ, Melton LJ III, Amin S, Khosla S (2012) Skeletal muscle mass is associated with bone geometry and microstructure and serum insulin-like growth factor binding protein-2 levels in adult women and men. J Bone Miner Res 27:2159–2169

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Wu CH, Yang KC, Chang HH, Yen JF, Tsai KS, Huang KC (2013) Sarcopenia is Related to Increased Risk for Low Bone Mineral Density. J Clin Densitom 16(1):98–103.

    Google Scholar 

  23. Verschueren S, Gielen E, O'Neill TW, Pye SR, Adams JE, Ward KA et al (2013) Sarcopenia and its relationship with bone mineral density in middle-aged and elderly European men. Osteoporos Int 24(1):87–98.

    Google Scholar 

  24. Capozza RF, Cure-Cure C, Cointry GR, Meta M, Cure P, Rittweger J et al (2008) Association between low lean body mass and osteoporotic fractures after menopause. Menopause 15:905–913

    Article  PubMed  Google Scholar 

  25. Richards RR, McKee MD, Paitich CB, Anderson GI, Bertoia JT (1991) A comparison of the effects of skin coverage and muscle flap coverage on the early strength of union at the site of osteotomy after devascularization of a segment of canine tibia. J Bone Joint Surg Am 73:1323–1330

    CAS  PubMed  Google Scholar 

  26. Stein H, Perren SM, Cordey J, Kenwright J, Mosheiff R, Francis MJ (2002) The muscle bed—a crucial factor for fracture healing: a physiological concept. Orthopedics 25:1379–1383

    PubMed  Google Scholar 

  27. Hamrick MW (2011) A role for myokines in muscle-bone interactions. Exerc Sport Sci Rev 39:43–47

    Article  PubMed Central  PubMed  Google Scholar 

  28. Tanaka K, Matsumoto E, Higashimaki Y, Katagiri T, Sugimoto T, Seino S et al (2012) Role of osteoglycin in the linkage between muscle and bone. J Biol Chem 287:11616–11628

    Article  CAS  PubMed  Google Scholar 

  29. Lambert CP, Wright NR, Finck BN, Villareal DT (2008) Exercise but not diet-induced weight loss decreases skeletal muscle inflammatory gene expression in frail obese elderly persons. J Appl Physiol 105:473–478

    Article  CAS  PubMed  Google Scholar 

  30. Mo C, Romero-Suarez S, Bonewald L, Johnson M, Brotto M (2012) Prostaglandin E2: from clinical applications to its potential role in bone-muscle crosstalk and myogenic differentiation. Recent Pat Biotechnol 6(3):223–229.

    Google Scholar 

  31. Christodoulides C, Lagathu C, Sethi JK, Vidal-Puig A (2009) Adipogenesis and WNT signalling. Trends Endocrinol Metab 20:16–24

    Article  CAS  PubMed  Google Scholar 

  32. Bennett CN, Longo KA, Wright WS, Suva LJ, Lane TF, Hankenson KD et al (2005) Regulation of osteoblastogenesis and bone mass by Wnt10b. Proc Natl Acad Sci U S A 102:3324–3329

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Romero-Suarez S, Mo C, Lara N, Jaehn K, Johnson M, Bonewald L et al (2013) The B-catenin activating factor, Wnt3a, stimulates skeletal myogenesis. J Bone Miner Res (in press).

  34. Robling AG, Niziolek PJ, Baldridge LA, Condon KW, Allen MR, Alam I et al (2008) Mechanical stimulation of bone in vivo reduces osteocyte expression of Sost/sclerostin. J Biol Chem 283:5866–5875

    Article  CAS  PubMed  Google Scholar 

  35. Turner CH, Warden SJ, Bellido T, Plotkin LI, Kumar N, Jasiuk I et al (2009) Mechanobiology of the skeleton. Sci Signal 2:t3

    Google Scholar 

  36. Cipriani C, Romagnoli E, Carnevale V, Raso I, Scarpiello A, Angelozzi M et al (2012) Muscle strength and bone in healthy women: effect of age and gonadal status. Hormones (Athens ) 11:325–332

    Google Scholar 

  37. Goodpaster BH, Thaete FL, Kelley DE (2000) Composition of skeletal muscle evaluated with computed tomography. Ann N Y Acad Sci 904:18–24

    Article  CAS  PubMed  Google Scholar 

  38. Jo E, Lee SR, Park BS, Kim JS (2012) Potential mechanisms underlying the role of chronic inflammation in Age-related Muscle Wasting. Aging Clin Exp Res 5:412–422

    Google Scholar 

  39. Meng SJ, Yu LJ (2010) Oxidative stress, molecular inflammation and sarcopenia. Int J Mol Sci 11:1509–1526

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank the participants for their cooperation and the staff of the Intensive Research Unit of the Institute of Clinical and Translational Sciences for their skilled assistance in the performance of this study. This study was supported by grants RO1-AG025501, R01-AG031176, P30-DK56341 (Clinical Nutrition Research Unit), and UL1-RR024992 (Clinical and Translational Science) and resources at the New Mexico VA Health Care System.

Conflicts of Interest

The authors have no conflicts of interests.

Author information

Authors and Affiliations

  1. New Mexico VA Health Care System, Albuquerque, NM, USA

    R. Armamento-Villareal, L. Aguirre & D. T. Villareal

  2. University of New Mexico School of Medicine, Albuquerque, NM, USA

    R. Armamento-Villareal, C. Qualls & D. T. Villareal

  3. Campus Biomedico, Rome, Italy

    N. Napoli

  4. University of Rochester School of Medicine, Rochester, NY, USA

    K. Shah

  5. Ithaca College, Rochester, NY, USA

    T. Hilton

  6. Washington University School of Medicine, St. Louis, MO, USA

    N. Napoli, D. R. Sinacore & D. T. Villareal

Authors
  1. R. Armamento-Villareal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. Aguirre
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. Napoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. Shah
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. T. Hilton
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. D. R. Sinacore
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. C. Qualls
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. D. T. Villareal
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. T. Villareal.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Armamento-Villareal, R., Aguirre, L., Napoli, N. et al. Changes in thigh muscle volume predict bone mineral density response to lifestyle therapy in frail, obese older adults. Osteoporos Int 25, 551–558 (2014). https://doi.org/10.1007/s00198-013-2450-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-013-2450-2

Keywords

Search

Navigation