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Published in: Osteoporosis International 2/2014

01-02-2014 | Original Article

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

Authors: R. Armamento-Villareal, L. Aguirre, N. Napoli, K. Shah, T. Hilton, D. R. Sinacore, C. Qualls, D. T. Villareal

Published in: Osteoporosis International | Issue 2/2014

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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.
Literature
1.
go back to reference 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 364:1218–1229PubMedCentralPubMedCrossRef 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 364:1218–1229PubMedCentralPubMedCrossRef
2.
go back to reference 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 26:2851–2859PubMedCentralPubMedCrossRef 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 26:2851–2859PubMedCentralPubMedCrossRef
3.
go back to reference 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 27:1215–1221PubMedCentralPubMedCrossRef 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 27:1215–1221PubMedCentralPubMedCrossRef
4.
go back to reference 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. 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.
5.
go back to reference 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–E1008PubMedCrossRef 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–E1008PubMedCrossRef
6.
go back to reference 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 102:634–640PubMedCrossRef 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 102:634–640PubMedCrossRef
7.
go back to reference 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 20:232–239PubMedCrossRef 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 20:232–239PubMedCrossRef
8.
go back to reference 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 166:860–866PubMedCrossRef 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 166:860–866PubMedCrossRef
9.
go back to reference 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 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
10.
go back to reference Tinetti ME, Speechley M, Ginter SF (1988) Risk factors for falls among elderly persons living in the community. N Engl J Med 319:1701–1707PubMedCrossRef Tinetti ME, Speechley M, Ginter SF (1988) Risk factors for falls among elderly persons living in the community. N Engl J Med 319:1701–1707PubMedCrossRef
11.
go back to reference Nevitt MC, Cummings SR, Kidd S, Black D (1989) Risk factors for recurrent nonsyncopal falls. A prospective study. JAMA 261:2663–2668PubMedCrossRef Nevitt MC, Cummings SR, Kidd S, Black D (1989) Risk factors for recurrent nonsyncopal falls. A prospective study. JAMA 261:2663–2668PubMedCrossRef
12.
go back to reference Lord SR, Ward JA, Williams P, Anstey KJ (1994) Physiological factors associated with falls in older community-dwelling women. J Am Geriatr Soc 42:1110–1117PubMed Lord SR, Ward JA, Williams P, Anstey KJ (1994) Physiological factors associated with falls in older community-dwelling women. J Am Geriatr Soc 42:1110–1117PubMed
13.
go back to reference 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 332:767–773PubMedCrossRef 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 332:767–773PubMedCrossRef
14.
go back to reference 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 66:1376–1383PubMedCrossRef 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 66:1376–1383PubMedCrossRef
15.
go back to reference Fiatarone MA, Marks EC, Ryan ND, Meredith CN, Lipsitz LA, Evans WJ (1990) High-intensity strength training in nonagenarians. Effects on skeletal muscle. JAMA 263:3029–3034PubMedCrossRef Fiatarone MA, Marks EC, Ryan ND, Meredith CN, Lipsitz LA, Evans WJ (1990) High-intensity strength training in nonagenarians. Effects on skeletal muscle. JAMA 263:3029–3034PubMedCrossRef
16.
go back to reference 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 21:772–779PubMedCrossRef 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 21:772–779PubMedCrossRef
17.
go back to reference Villareal DT, Banks M, Siener C, Sinacore DR, Klein S (2004) Physical frailty and body composition in obese elderly men and women. Obes Res 12:913–920PubMedCrossRef Villareal DT, Banks M, Siener C, Sinacore DR, Klein S (2004) Physical frailty and body composition in obese elderly men and women. Obes Res 12:913–920PubMedCrossRef
18.
19.
go back to reference Ryan AS, Nicklas BJ, Dennis KE (1998) Aerobic exercise maintains regional bone mineral density during weight loss in postmenopausal women. J Appl Physiol 84:1305–1310PubMedCrossRef Ryan AS, Nicklas BJ, Dennis KE (1998) Aerobic exercise maintains regional bone mineral density during weight loss in postmenopausal women. J Appl Physiol 84:1305–1310PubMedCrossRef
20.
go back to reference 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 70:97–103PubMed 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 70:97–103PubMed
21.
go back to reference 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 27:2159–2169PubMedCentralPubMedCrossRef 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 27:2159–2169PubMedCentralPubMedCrossRef
22.
go back to reference 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. 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.
23.
go back to reference 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. 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.
24.
go back to reference 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 15:905–913PubMedCrossRef 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 15:905–913PubMedCrossRef
25.
go back to reference 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 73:1323–1330PubMed 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 73:1323–1330PubMed
26.
go back to reference 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 25:1379–1383PubMed 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 25:1379–1383PubMed
28.
go back to reference 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 287:11616–11628PubMedCrossRef 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 287:11616–11628PubMedCrossRef
29.
go back to reference 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 105:473–478PubMedCrossRef 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 105:473–478PubMedCrossRef
30.
go back to reference 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. 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.
31.
go back to reference Christodoulides C, Lagathu C, Sethi JK, Vidal-Puig A (2009) Adipogenesis and WNT signalling. Trends Endocrinol Metab 20:16–24PubMedCrossRef Christodoulides C, Lagathu C, Sethi JK, Vidal-Puig A (2009) Adipogenesis and WNT signalling. Trends Endocrinol Metab 20:16–24PubMedCrossRef
32.
go back to reference 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 102:3324–3329PubMedCentralPubMedCrossRef 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 102:3324–3329PubMedCentralPubMedCrossRef
33.
go back to reference 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). 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.
go back to reference 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 283:5866–5875PubMedCrossRef 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 283:5866–5875PubMedCrossRef
35.
go back to reference Turner CH, Warden SJ, Bellido T, Plotkin LI, Kumar N, Jasiuk I et al (2009) Mechanobiology of the skeleton. Sci Signal 2:t3 Turner CH, Warden SJ, Bellido T, Plotkin LI, Kumar N, Jasiuk I et al (2009) Mechanobiology of the skeleton. Sci Signal 2:t3
36.
go back to reference 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 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
37.
go back to reference Goodpaster BH, Thaete FL, Kelley DE (2000) Composition of skeletal muscle evaluated with computed tomography. Ann N Y Acad Sci 904:18–24PubMedCrossRef Goodpaster BH, Thaete FL, Kelley DE (2000) Composition of skeletal muscle evaluated with computed tomography. Ann N Y Acad Sci 904:18–24PubMedCrossRef
38.
go back to reference 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 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
Metadata
Title
Changes in thigh muscle volume predict bone mineral density response to lifestyle therapy in frail, obese older adults
Authors
R. Armamento-Villareal
L. Aguirre
N. Napoli
K. Shah
T. Hilton
D. R. Sinacore
C. Qualls
D. T. Villareal
Publication date
01-02-2014
Publisher
Springer London
Published in
Osteoporosis International / Issue 2/2014
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-013-2450-2

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