Skip to main content
Top
Published in: Osteoporosis International 8/2013

01-08-2013 | Original Article

Abdominal body composition measured by quantitative computed tomography and risk of non-spine fractures: the Osteoporotic Fractures in Men (MrOS) study

Authors: Y. Sheu, L. M. Marshall, K. F. Holton, P. Caserotti, R. M. Boudreau, E. S. Strotmeyer, P. M. Cawthon, J. A. Cauley

Published in: Osteoporosis International | Issue 8/2013

Login to get access

Abstract

Summary

The effect of abdominal adiposity and muscle on fracture is unclear in older men; therefore, we examined the association among 749 men aged 65+. Among various adipose tissues and muscle groups, lower psoas muscle volume and higher fatty infiltration of abdominal muscle contribute to higher fracture risk independent of BMD.

Introduction

The association of abdominal adiposity and muscle composition with incident fracture is unclear, especially in older men. Therefore, we examined the relationship of subcutaneous adipose tissue (SAT), visceral adipose tissue (VAT), abdominal intermuscular adipose tissue (IMAT), and muscle volume with incident non-spine fractures among 749 men aged 65 and older.

Methods

A case–cohort study design was used with a total of 252 fracture cases and 497 non-cases. We measured volumes (in centimeters) of adipose and muscle tissues obtained from quantitative computed tomography scan at the L4–5 intervertebral space. Three groups of muscle and IMAT were evaluated: total abdominal, psoas, and paraspinal. Cox proportional hazards regression with a robust variance estimator was used to estimate the hazard ratio (HR) of non-spine fractures per standard deviation (SD) increase in the abdominal body composition measures. The mean age among men in the random subcohort was 74.2 ± 6.1 years, and the average follow-up time was 5.2 ± 1.1 years.

Results

After adjusting for age, race, clinic site, percent body fat, and femoral neck bone mineral density (BMD), no significant relationship was found between incident fractures and SAT or VAT. One SD increase in muscle volume at the psoas, but not paraspinal, was associated with 28 % lower fracture risk (95 % CI = 0.55–0.95). When IMAT models were further adjusted for corresponding muscle volumes, only abdominal IMAT was significantly associated with fracture risk (HR = 1.30 (95 % CI = 1.04–1.63)).

Conclusion

Our findings suggest that lower total psoas muscle volume and higher IMAT of the total abdominal muscle contribute to higher fracture risk in older men independent of BMD.
Literature
1.
go back to reference Jacobsen SJ, Goldberg J, Miles TP, Brody JA, Stiers W, Rimm AA (1992) Race and sex differences in mortality following fracture of the hip. Am J Public Health 82(8):1147–1150PubMedCrossRef Jacobsen SJ, Goldberg J, Miles TP, Brody JA, Stiers W, Rimm AA (1992) Race and sex differences in mortality following fracture of the hip. Am J Public Health 82(8):1147–1150PubMedCrossRef
2.
go back to reference Gullberg B, Johnell O, Kanis JA (1997) World-wide projections for hip fracture. Osteoporos Int 7(5):407–413PubMedCrossRef Gullberg B, Johnell O, Kanis JA (1997) World-wide projections for hip fracture. Osteoporos Int 7(5):407–413PubMedCrossRef
3.
go back to reference Kuk JL, Saunders TJ, Davidson LE, Ross R (2009) Age-related changes in total and regional fat distribution. Ageing Res Rev 8(4):339–348PubMedCrossRef Kuk JL, Saunders TJ, Davidson LE, Ross R (2009) Age-related changes in total and regional fat distribution. Ageing Res Rev 8(4):339–348PubMedCrossRef
4.
go back to reference Kuk JL, Katzmarzyk PT, Nichaman MZ, Church TS, Blair SN, Ross R (2006) Visceral fat is an independent predictor of all-cause mortality in men. Obesity (Silver Spring, MD 14(2):336–341CrossRef Kuk JL, Katzmarzyk PT, Nichaman MZ, Church TS, Blair SN, Ross R (2006) Visceral fat is an independent predictor of all-cause mortality in men. Obesity (Silver Spring, MD 14(2):336–341CrossRef
5.
go back to reference Lewis GF, Carpentier A, Adeli K, Giacca A (2002) Disordered fat storage and mobilization in the pathogenesis of insulin resistance and type 2 diabetes. Endocr Rev 23(2):201–229PubMedCrossRef Lewis GF, Carpentier A, Adeli K, Giacca A (2002) Disordered fat storage and mobilization in the pathogenesis of insulin resistance and type 2 diabetes. Endocr Rev 23(2):201–229PubMedCrossRef
6.
go back to reference Cawthon PM, Ewing SK, McCulloch CE, Ensrud KE, Cauley JA, Cummings SR, Orwoll ES (2009) Loss of hip BMD in older men: the Osteoporotic Fractures in Men (MrOS) study. J Bone Miner Res 24(10):1728–1735PubMedCrossRef Cawthon PM, Ewing SK, McCulloch CE, Ensrud KE, Cauley JA, Cummings SR, Orwoll ES (2009) Loss of hip BMD in older men: the Osteoporotic Fractures in Men (MrOS) study. J Bone Miner Res 24(10):1728–1735PubMedCrossRef
7.
go back to reference Imamura K, Ashida H, Ishikawa T, Fujii M (1983) Human major psoas muscle and sacrospinalis muscle in relation to age: a study by computed tomography. J Gerontol 38(6):678–681PubMedCrossRef Imamura K, Ashida H, Ishikawa T, Fujii M (1983) Human major psoas muscle and sacrospinalis muscle in relation to age: a study by computed tomography. J Gerontol 38(6):678–681PubMedCrossRef
8.
go back to reference Bemben MG, Massey BH, Bemben DA, Boileau RA, Misner JE (1995) Age-related patterns in body composition for men aged 20–79 yr. Med Sci Sports Exerc 27(2):264–269PubMed Bemben MG, Massey BH, Bemben DA, Boileau RA, Misner JE (1995) Age-related patterns in body composition for men aged 20–79 yr. Med Sci Sports Exerc 27(2):264–269PubMed
9.
go back to reference Hughes VA, Frontera WR, Roubenoff R, Evans WJ, Singh MA (2002) Longitudinal changes in body composition in older men and women: role of body weight change and physical activity. Am J Clin Nutr 76(2):473–481PubMed Hughes VA, Frontera WR, Roubenoff R, Evans WJ, Singh MA (2002) Longitudinal changes in body composition in older men and women: role of body weight change and physical activity. Am J Clin Nutr 76(2):473–481PubMed
10.
go back to reference Goodpaster BH, Carlson CL, Visser M, Kelley DE, Scherzinger A, Harris TB, Stamm E, Newman AB (2001) Attenuation of skeletal muscle and strength in the elderly: the Health ABC Study. J Appl Physiol 90(6):2157–2165PubMed Goodpaster BH, Carlson CL, Visser M, Kelley DE, Scherzinger A, Harris TB, Stamm E, Newman AB (2001) Attenuation of skeletal muscle and strength in the elderly: the Health ABC Study. J Appl Physiol 90(6):2157–2165PubMed
12.
go back to reference Borkan GA, Hults DE, Gerzof SG, Robbins AH, Silbert CK (1983) Age changes in body composition revealed by computed tomography. J Gerontol 38(6):673–677PubMedCrossRef Borkan GA, Hults DE, Gerzof SG, Robbins AH, Silbert CK (1983) Age changes in body composition revealed by computed tomography. J Gerontol 38(6):673–677PubMedCrossRef
13.
go back to reference Couillard C, Gagnon J, Bergeron J, Leon AS, Rao DC, Skinner JS, Wilmore JH, Despres JP, Bouchard C (2000) Contribution of body fatness and adipose tissue distribution to the age variation in plasma steroid hormone concentrations in men: the HERITAGE Family Study. J Clin Endocrinol Metab 85(3):1026–1031PubMedCrossRef Couillard C, Gagnon J, Bergeron J, Leon AS, Rao DC, Skinner JS, Wilmore JH, Despres JP, Bouchard C (2000) Contribution of body fatness and adipose tissue distribution to the age variation in plasma steroid hormone concentrations in men: the HERITAGE Family Study. J Clin Endocrinol Metab 85(3):1026–1031PubMedCrossRef
14.
go back to reference Despres JP, Nadeau A, Tremblay A, Ferland M, Moorjani S, Lupien PJ, Theriault G, Pinault S, Bouchard C (1989) Role of deep abdominal fat in the association between regional adipose tissue distribution and glucose tolerance in obese women. Diabetes 38(3):304–309PubMedCrossRef Despres JP, Nadeau A, Tremblay A, Ferland M, Moorjani S, Lupien PJ, Theriault G, Pinault S, Bouchard C (1989) Role of deep abdominal fat in the association between regional adipose tissue distribution and glucose tolerance in obese women. Diabetes 38(3):304–309PubMedCrossRef
15.
go back to reference Goodpaster BH, Krishnaswami S, Resnick H, Kelley DE, Haggerty C, Harris TB, Schwartz AV, Kritchevsky S, Newman AB (2003) Association between regional adipose tissue distribution and both type 2 diabetes and impaired glucose tolerance in elderly men and women. Diabetes Care 26(2):372–379PubMedCrossRef Goodpaster BH, Krishnaswami S, Resnick H, Kelley DE, Haggerty C, Harris TB, Schwartz AV, Kritchevsky S, Newman AB (2003) Association between regional adipose tissue distribution and both type 2 diabetes and impaired glucose tolerance in elderly men and women. Diabetes Care 26(2):372–379PubMedCrossRef
16.
go back to reference Nguyen ND, Pongchaiyakul C, Center JR, Eisman JA, Nguyen TV (2005) Abdominal fat and hip fracture risk in the elderly: the Dubbo Osteoporosis Epidemiology Study. BMC Musculoskelet Disord 6:11PubMedCrossRef Nguyen ND, Pongchaiyakul C, Center JR, Eisman JA, Nguyen TV (2005) Abdominal fat and hip fracture risk in the elderly: the Dubbo Osteoporosis Epidemiology Study. BMC Musculoskelet Disord 6:11PubMedCrossRef
17.
go back to reference Sjostrom L (1991) A computer-tomography based multicompartment body composition technique and anthropometric predictions of lean body mass, total and subcutaneous adipose tissue. Int J Obes 15(Suppl 2):19–30PubMed Sjostrom L (1991) A computer-tomography based multicompartment body composition technique and anthropometric predictions of lean body mass, total and subcutaneous adipose tissue. Int J Obes 15(Suppl 2):19–30PubMed
18.
go back to reference Goodpaster BH, Kelley DE, Thaete FL, He J, Ross R (2000) Skeletal muscle attenuation determined by computed tomography is associated with skeletal muscle lipid content. J Appl Physiol 89(1):104–110PubMed Goodpaster BH, Kelley DE, Thaete FL, He J, Ross R (2000) Skeletal muscle attenuation determined by computed tomography is associated with skeletal muscle lipid content. J Appl Physiol 89(1):104–110PubMed
19.
go back to reference Choi HS, Kim KJ, Kim KM, Hur NW, Rhee Y, Han DS, Lee EJ, Lim SK (2010) Relationship between visceral adiposity and bone mineral density in Korean adults. Calcif Tissue Int 87(3):218–225PubMedCrossRef Choi HS, Kim KJ, Kim KM, Hur NW, Rhee Y, Han DS, Lee EJ, Lim SK (2010) Relationship between visceral adiposity and bone mineral density in Korean adults. Calcif Tissue Int 87(3):218–225PubMedCrossRef
20.
go back to reference Yamaguchi T, Kanazawa I, Yamamoto M, Kurioka S, Yamauchi M, Yano S, Sugimoto T (2009) Associations between components of the metabolic syndrome versus bone mineral density and vertebral fractures in patients with type 2 diabetes. Bone 45(2):174–179PubMedCrossRef Yamaguchi T, Kanazawa I, Yamamoto M, Kurioka S, Yamauchi M, Yano S, Sugimoto T (2009) Associations between components of the metabolic syndrome versus bone mineral density and vertebral fractures in patients with type 2 diabetes. Bone 45(2):174–179PubMedCrossRef
21.
go back to reference Russell M, Mendes N, Miller KK, Rosen CJ, Lee H, Klibanski A, Misra M (2010) Visceral fat is a negative predictor of bone density measures in obese adolescent girls. J Clin Endocrinol Metab 95(3):1247–1255PubMedCrossRef Russell M, Mendes N, Miller KK, Rosen CJ, Lee H, Klibanski A, Misra M (2010) Visceral fat is a negative predictor of bone density measures in obese adolescent girls. J Clin Endocrinol Metab 95(3):1247–1255PubMedCrossRef
22.
go back to reference Lang T, Cauley JA, Tylavsky F, Bauer D, Cummings S, Harris TB (2010) Computed tomographic measurements of thigh muscle cross-sectional area and attenuation coefficient predict hip fracture: the health, aging, and body composition study. J Bone Miner Res 25(3):513–519PubMedCrossRef Lang T, Cauley JA, Tylavsky F, Bauer D, Cummings S, Harris TB (2010) Computed tomographic measurements of thigh muscle cross-sectional area and attenuation coefficient predict hip fracture: the health, aging, and body composition study. J Bone Miner Res 25(3):513–519PubMedCrossRef
23.
go back to reference Lang T, Koyama A, Li C, Li J, Lu Y, Saeed I, Gazze E, Keyak J, Harris T, Cheng X (2008) Pelvic body composition measurements by quantitative computed tomography: association with recent hip fracture. Bone 42(4):798–805PubMedCrossRef Lang T, Koyama A, Li C, Li J, Lu Y, Saeed I, Gazze E, Keyak J, Harris T, Cheng X (2008) Pelvic body composition measurements by quantitative computed tomography: association with recent hip fracture. Bone 42(4):798–805PubMedCrossRef
24.
go back to reference Blank JB, Cawthon PM, Carrion-Petersen ML, Harper L, Johnson JP, Mitson E, Delay RR (2005) Overview of recruitment for the osteoporotic fractures in men study (MrOS). Contemp Clin Trials 26(5):557–568PubMedCrossRef Blank JB, Cawthon PM, Carrion-Petersen ML, Harper L, Johnson JP, Mitson E, Delay RR (2005) Overview of recruitment for the osteoporotic fractures in men study (MrOS). Contemp Clin Trials 26(5):557–568PubMedCrossRef
25.
go back to reference Orwoll E, Blank JB, Barrett-Connor E, Cauley J, Cummings S, Ensrud K, Lewis C, Cawthon PM, Marcus R, Marshall LM, McGowan J, Phipps K, Sherman S, Stefanick ML, Stone K (2005) Design and baseline characteristics of the osteoporotic fractures in men (MrOS) study–a large observational study of the determinants of fracture in older men. Contemp Clin Trials 26(5):569–585PubMedCrossRef Orwoll E, Blank JB, Barrett-Connor E, Cauley J, Cummings S, Ensrud K, Lewis C, Cawthon PM, Marcus R, Marshall LM, McGowan J, Phipps K, Sherman S, Stefanick ML, Stone K (2005) Design and baseline characteristics of the osteoporotic fractures in men (MrOS) study–a large observational study of the determinants of fracture in older men. Contemp Clin Trials 26(5):569–585PubMedCrossRef
26.
go back to reference Marshall LM, Lang TF, Lambert LC, Zmuda JM, Ensrud KE, Orwoll ES (2006) Dimensions and volumetric BMD of the proximal femur and their relation to age among older U.S. men. J Bone Miner Res 21(8):1197–1206PubMedCrossRef Marshall LM, Lang TF, Lambert LC, Zmuda JM, Ensrud KE, Orwoll ES (2006) Dimensions and volumetric BMD of the proximal femur and their relation to age among older U.S. men. J Bone Miner Res 21(8):1197–1206PubMedCrossRef
27.
go back to reference Kvist H, Chowdhury B, Sjostrom L, Tylen U, Cederblad A (1988) Adipose tissue volume determination in males by computed tomography and 40 K. Int J Obes 12(3):249–266PubMed Kvist H, Chowdhury B, Sjostrom L, Tylen U, Cederblad A (1988) Adipose tissue volume determination in males by computed tomography and 40 K. Int J Obes 12(3):249–266PubMed
28.
go back to reference Rossner S, Bo WJ, Hiltbrandt E, Hinson W, Karstaedt N, Santago P, Sobol WT, Crouse JR (1990) Adipose tissue determinations in cadavers—a comparison between cross-sectional planimetry and computed tomography. Int J Obes 14(10):893–902PubMed Rossner S, Bo WJ, Hiltbrandt E, Hinson W, Karstaedt N, Santago P, Sobol WT, Crouse JR (1990) Adipose tissue determinations in cadavers—a comparison between cross-sectional planimetry and computed tomography. Int J Obes 14(10):893–902PubMed
29.
go back to reference Barlow WE, Ichikawa L, Rosner D, Izumi S (1999) Analysis of case–cohort designs. J Clin Epidemiol 52(12):1165–1172PubMedCrossRef Barlow WE, Ichikawa L, Rosner D, Izumi S (1999) Analysis of case–cohort designs. J Clin Epidemiol 52(12):1165–1172PubMedCrossRef
30.
go back to reference Visser M, Goodpaster BH, Kritchevsky SB, Newman AB, Nevitt M, Rubin SM, Simonsick EM, Harris TB (2005) Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons. J Gerontol 60(3):324–333CrossRef Visser M, Goodpaster BH, Kritchevsky SB, Newman AB, Nevitt M, Rubin SM, Simonsick EM, Harris TB (2005) Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons. J Gerontol 60(3):324–333CrossRef
31.
go back to reference Visser M, Kritchevsky SB, Goodpaster BH, Newman AB, Nevitt M, Stamm E, Harris TB (2002) Leg muscle mass and composition in relation to lower extremity performance in men and women aged 70 to 79: the health, aging and body composition study. J Am Geriatr Soc 50(5):897–904PubMedCrossRef Visser M, Kritchevsky SB, Goodpaster BH, Newman AB, Nevitt M, Stamm E, Harris TB (2002) Leg muscle mass and composition in relation to lower extremity performance in men and women aged 70 to 79: the health, aging and body composition study. J Am Geriatr Soc 50(5):897–904PubMedCrossRef
32.
go back to reference Nielson CM, Marshall LM, Adams AL, LeBlanc ES, Cawthon PM, Ensrud K, Stefanick ML, Barrett-Connor E, Orwoll ES (2011) BMI and fracture risk in older men: the osteoporotic fractures in men study (MrOS). J Bone Miner Res 26(3):496–502. doi:10.1002/jbmr.235 PubMedCrossRef Nielson CM, Marshall LM, Adams AL, LeBlanc ES, Cawthon PM, Ensrud K, Stefanick ML, Barrett-Connor E, Orwoll ES (2011) BMI and fracture risk in older men: the osteoporotic fractures in men study (MrOS). J Bone Miner Res 26(3):496–502. doi:10.​1002/​jbmr.​235 PubMedCrossRef
33.
go back to reference Schaffler A, Herfarth H, Paul G, Ehling A, Muller-Ladner U, Scholmerich J, Zietz B (2004) Identification of influencing variables on adiponectin serum levels in diabetes mellitus type 1 and type 2. Exp Clin Endocrinol Diabetes 112(7):383–389PubMedCrossRef Schaffler A, Herfarth H, Paul G, Ehling A, Muller-Ladner U, Scholmerich J, Zietz B (2004) Identification of influencing variables on adiponectin serum levels in diabetes mellitus type 1 and type 2. Exp Clin Endocrinol Diabetes 112(7):383–389PubMedCrossRef
34.
go back to reference Strotmeyer ES, Cauley JA (2007) Diabetes mellitus, bone mineral density, and fracture risk. Curr Opin Endocrinol Diabetes Obes 14(6):429–435PubMedCrossRef Strotmeyer ES, Cauley JA (2007) Diabetes mellitus, bone mineral density, and fracture risk. Curr Opin Endocrinol Diabetes Obes 14(6):429–435PubMedCrossRef
36.
go back to reference Schafer AL, Vittinghoff E, Lang TF, Sellmeyer DE, Harris TB, Kanaya AM, Strotmeyer ES, Cawthon PM, Cummings SR, Tylavsky FA, Scherzinger AL, Schwartz AV (2010) Fat infiltration of muscle, diabetes, and clinical fracture risk in older adults. J Clin Endocrinol Metab 95(11):E368–E372. doi:10.1210/jc.2010-0780 PubMedCrossRef Schafer AL, Vittinghoff E, Lang TF, Sellmeyer DE, Harris TB, Kanaya AM, Strotmeyer ES, Cawthon PM, Cummings SR, Tylavsky FA, Scherzinger AL, Schwartz AV (2010) Fat infiltration of muscle, diabetes, and clinical fracture risk in older adults. J Clin Endocrinol Metab 95(11):E368–E372. doi:10.​1210/​jc.​2010-0780 PubMedCrossRef
37.
go back to reference Hicks GE, Simonsick EM, Harris TB, Newman AB, Weiner DK, Nevitt MA, Tylavsky FA (2005) Cross-sectional associations between trunk muscle composition, back pain, and physical function in the health, aging and body composition study. J Gerontol 60(7):882–887CrossRef Hicks GE, Simonsick EM, Harris TB, Newman AB, Weiner DK, Nevitt MA, Tylavsky FA (2005) Cross-sectional associations between trunk muscle composition, back pain, and physical function in the health, aging and body composition study. J Gerontol 60(7):882–887CrossRef
38.
go back to reference Mengiardi B, Schmid MR, Boos N, Pfirrmann CW, Brunner F, Elfering A, Hodler J (2006) Fat content of lumbar paraspinal muscles in patients with chronic low back pain and in asymptomatic volunteers: quantification with MR spectroscopy. Radiology 240(3):786–792PubMedCrossRef Mengiardi B, Schmid MR, Boos N, Pfirrmann CW, Brunner F, Elfering A, Hodler J (2006) Fat content of lumbar paraspinal muscles in patients with chronic low back pain and in asymptomatic volunteers: quantification with MR spectroscopy. Radiology 240(3):786–792PubMedCrossRef
39.
go back to reference Sinaki M, Itoi E, Wahner HW, Wollan P, Gelzcer R, Mullan BP, Collins DA, Hodgson SF (2002) Stronger back muscles reduce the incidence of vertebral fractures: a prospective 10 year follow-up of postmenopausal women. Bone 30(6):836–841PubMedCrossRef Sinaki M, Itoi E, Wahner HW, Wollan P, Gelzcer R, Mullan BP, Collins DA, Hodgson SF (2002) Stronger back muscles reduce the incidence of vertebral fractures: a prospective 10 year follow-up of postmenopausal women. Bone 30(6):836–841PubMedCrossRef
41.
go back to reference Pollock NK, Bernard PJ, Wenger K, Misra S, Gower BA, Allison JD, Zhu H, Davis CL (2010) Lower bone mass in prepubertal overweight children with pre-diabetes. J Bone Miner Res 25(12):2760–2769 Pollock NK, Bernard PJ, Wenger K, Misra S, Gower BA, Allison JD, Zhu H, Davis CL (2010) Lower bone mass in prepubertal overweight children with pre-diabetes. J Bone Miner Res 25(12):2760–2769
42.
go back to reference Szulc P, Varennes A, Delmas PD, Goudable J, Chapurlat R (2010) Men with metabolic syndrome have lower bone mineral density but lower fracture risk–the MINOS study. J Bone Miner Res 25(6):1446–1454PubMedCrossRef Szulc P, Varennes A, Delmas PD, Goudable J, Chapurlat R (2010) Men with metabolic syndrome have lower bone mineral density but lower fracture risk–the MINOS study. J Bone Miner Res 25(6):1446–1454PubMedCrossRef
43.
go back to reference Ensrud KE, Lipschutz RC, Cauley JA, Seeley D, Nevitt MC, Scott J, Orwoll ES, Genant HK, Cummings SR (1997) Body size and hip fracture risk in older women: a prospective study. Study of Osteoporotic Fractures Research Group. Am J Med 103(4):274–280PubMedCrossRef Ensrud KE, Lipschutz RC, Cauley JA, Seeley D, Nevitt MC, Scott J, Orwoll ES, Genant HK, Cummings SR (1997) Body size and hip fracture risk in older women: a prospective study. Study of Osteoporotic Fractures Research Group. Am J Med 103(4):274–280PubMedCrossRef
44.
go back to reference Sheu Y, Cauley JA (2011) The role of bone marrow and visceral fat on bone metabolism. Curr Osteoporos Rep 9(2):67–75PubMedCrossRef Sheu Y, Cauley JA (2011) The role of bone marrow and visceral fat on bone metabolism. Curr Osteoporos Rep 9(2):67–75PubMedCrossRef
46.
go back to reference Miyawaki T, Abe M, Yahata K, Kajiyama N, Katsuma H, Saito N (2004) Contribution of visceral fat accumulation to the risk factors for atherosclerosis in non-obese Japanese. Intern Med (Tokyo, Japan) 43(12):1138–1144CrossRef Miyawaki T, Abe M, Yahata K, Kajiyama N, Katsuma H, Saito N (2004) Contribution of visceral fat accumulation to the risk factors for atherosclerosis in non-obese Japanese. Intern Med (Tokyo, Japan) 43(12):1138–1144CrossRef
47.
go back to reference Miljkovic I, Cauley JA, Petit MA, Ensrud KE, Strotmeyer E, Sheu Y, Gordon CL, Goodpaster BH, Bunker CH, Patrick AL, Wheeler VW, Kuller LH, Faulkner KA, Zmuda JM (2009) Greater adipose tissue infiltration in skeletal muscle among older men of African ancestry. J Clin Endocrinol Metab 94(8):2735–2742. doi:10.1210/jc.2008-2541 PubMedCrossRef Miljkovic I, Cauley JA, Petit MA, Ensrud KE, Strotmeyer E, Sheu Y, Gordon CL, Goodpaster BH, Bunker CH, Patrick AL, Wheeler VW, Kuller LH, Faulkner KA, Zmuda JM (2009) Greater adipose tissue infiltration in skeletal muscle among older men of African ancestry. J Clin Endocrinol Metab 94(8):2735–2742. doi:10.​1210/​jc.​2008-2541 PubMedCrossRef
48.
go back to reference Zoico E, Rossi A, Di Francesco V, Sepe A, Olioso D, Pizzini F, Fantin F, Bosello O, Cominacini L, Harris TB, Zamboni M (2010) Adipose tissue infiltration in skeletal muscle of healthy elderly men: relationships with body composition, insulin resistance, and inflammation at the systemic and tissue level. J Gerontol 65(3):295–299. doi:10.1093/gerona/glp155 Zoico E, Rossi A, Di Francesco V, Sepe A, Olioso D, Pizzini F, Fantin F, Bosello O, Cominacini L, Harris TB, Zamboni M (2010) Adipose tissue infiltration in skeletal muscle of healthy elderly men: relationships with body composition, insulin resistance, and inflammation at the systemic and tissue level. J Gerontol 65(3):295–299. doi:10.​1093/​gerona/​glp155
Metadata
Title
Abdominal body composition measured by quantitative computed tomography and risk of non-spine fractures: the Osteoporotic Fractures in Men (MrOS) study
Authors
Y. Sheu
L. M. Marshall
K. F. Holton
P. Caserotti
R. M. Boudreau
E. S. Strotmeyer
P. M. Cawthon
J. A. Cauley
Publication date
01-08-2013
Publisher
Springer London
Published in
Osteoporosis International / Issue 8/2013
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-013-2322-9

Other articles of this Issue 8/2013

Osteoporosis International 8/2013 Go to the issue