Abstract
The objective of this study was to estimate the associations between muscular fat infiltration, tibia bone mineral quantity and distribution, and physical function in healthy older women. Thirty-five women (aged 60–75 years, mean 70 years) were recruited from the community. Percent intramuscular fat (%IntraMF) within the right leg tibialis anterior, soleus, and gastrocnemius muscles and total intermuscular fat (IMF) were segmented from magnetic resonance imaging scans at the mid-calf. Intramyocellular lipid (IMCL) content in the right tibialis anterior was measured with proton magnetic resonance spectroscopy. Right tibia bone content, area, and strength were measured at the 4, 14, and 66 % sites using peripheral quantitative computed tomography. Physical function was assessed by gait speed on the 20 m walking test. After adjusting for age, body size, and activity level, %IntraMF had a negative association with bone content and area at all tibia sites (r = −0.31 to −0.03). Conversely, greater IMF was associated with increased bone content and area (r = 0.04–0.32). Correlation coefficients for the association between IMCL and bone were negative (r = −0.44 to −0.03). All measures of fat infiltration had a negative association with observed physical function (r = −0.42 to −0.04). Our findings suggest that muscular fat infiltration in the leg of healthy postmenopausal women has a compartment-specific relationship with bone status and physical function. Minimizing fat accumulation within and between muscle compartments may prevent bone fragility and functional decline in women.
Similar content being viewed by others
References
Rubenstein LZ (2006) Falls in older people: epidemiology, risk factors and strategies for prevention. Age Ageing 35(2):37–41. doi:10.1093/ageing/afl084
Kanis JA, Borgstrom F, De Laet C, Johansson H, Johnell O, Jonsson B, Oden A, Zethraeus N, Pfleger B, Khaltaev N (2005) Assessment of fracture risk. Osteoporos Int 16:581–589. doi:10.1007/s00198-004-1780-5
Lauretani F, Russo CR, Bandinelli S, Bartali B, Cavazzini C, Di Iorio A, Corsi AM, Rantanen T, Guralnik JM, Ferrucci L (2003) Age-associated changes in skeletal muscles and their effect on mobility: An operational diagnosis of sarcopenia. J Appl Physiol 95:1851–1860. doi:10.1152/japplphysiol.00246.2003
Szulc P, Beck TJ, Marchand F, Delmas PD (2005) Low skeletal muscle mass is associated with poor structural parameters of bone and impaired balance in elderly men–the MINOS study. J Bone Min Res 20:721–729
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 50:897–904
Schwenzer NF, Martirosian P, Machann J, Schraml C, Steidle G, Claussen CD, Schick F (2009) Aging effects on human calf muscle properties assessed by MRI at 3 Tesla. J Magn Reson Imaging 29:1346–1354. doi:10.1002/jmri.21789
Boettcher M, Machann J, Stefan N, Thamer C, Haring HU, Claussen CD, Fritsche A, Schick F (2009) Intermuscular adipose tissue (IMAT): association with other adipose tissue compartments and insulin sensitivity. J Magn Reson Imaging 29:1340–1345. doi:10.1002/jmri.21754
Buford TW, Lott DJ, Marzetti E, Wohlgemuth SE, Vandenborne K, Pahor M, Leeuwenburgh C, Manini TM (2012) Age-related differences in lower extremity tissue compartments and associations with physical function in older adults. Exp Gerontol 47:38–44. doi:10.1016/j.exger.2011.10.001
Lott DJ, Forbes SC, Mathur S, Germain SA, Senesac CR, Lee Sweeney H, Walter GA, Vandenborne K (2014) Assessment of intramuscular lipid and metabolites of the lower leg using magnetic resonance spectroscopy in boys with Duchenne muscular dystrophy. Neuromuscul Disord 24:574–582. doi:10.1016/j.nmd.2014.03.013
Tuttle LJ, Sinacore DR, Mueller MJ (2012) Intermuscular adipose tissue is muscle specific and associated with poor functional performance. J Aging Res 2012:172957. doi:10.1155/2012/172957
Frank AW, Farthing JP, Chilibeck PD, Arnold CM, Olszynski WP, Kontulainen SA (2015) Community-dwelling female fallers have lower muscle density in their lower legs than non-fallers: evidence from the Saskatoon Canadian Multicentre Osteoporosis study (CaMos) cohort. J Nutr Health Aging 19:113–120. doi:10.1007/s12603-014-0476-6
Wong AK, Beattie KA, Min KK, Gordon C, Pickard L, Papaioannou A, Adachi JD, Canadian Multicentre Osteoporosis Study (CaMos) Research Group (2014) Peripheral quantitative computed tomography-derived muscle density and peripheral magnetic resonance imaging-derived muscle adiposity: precision and associations with fragility fractures in women. J Musculoskelet Neuronal Interact 14:401–410
Cawthon PM, Fox KM, Gandra SR, Delmonico MJ, Chiou CF, Anthony MS, Sewall A, Goodpaster B, Satterfield S, Cummings SR, Harris TB, Aging and Body Composition Study (2009) Do muscle mass, muscle density, strength, and physical function similarly influence risk of hospitalization in older adults? J Am Geriatr Soc 57:1411–1419. doi:10.1111/j.1532-5415.2009.02366.x
Douchi T, Kosha S, Uto H, Oki T, Nakae M, Yoshimitsu N, Nagata Y (2003) Precedence of bone loss over changes in body composition and body fat distribution within a few years after menopause. Maturitas 46:133–138
Murtagh KN, Hubert HB (2004) Gender differences in physical disability among an elderly cohort. Am J Public Health 94:1406–1411
Lang T, Cauley JA, Tylavsky F, Bauer D, Cummings S, Harris TB, Health ABC Study (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 25:513–519. doi:10.1359/jbmr.090807
Delmonico MJ, Harris TB, Visser M, Park SW, Conroy MB, Velasquez-Mieyer P, Boudreau R, Manini TM, Nevitt M, Newman AB, Goodpaster BH, Health, Aging and Body Composition Study (2009) Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr 90:1579–1585. doi:10.3945/ajcn.2009.28047
Marcus RL, Addison O, Dibble LE, Foreman KB, Morrell G, Lastayo P (2012) Intramuscular adipose tissue, sarcopenia, and mobility function in older individuals. J Aging Res 2012:629637. doi:10.1155/2012/629637
Karampinos DC, Baum T, Nardo L, Alizai H, Yu H, Carballido-Gamio J, Yap SP, Shimakawa A, Link TM, Majumdar S (2012) Characterization of the regional distribution of skeletal muscle adipose tissue in type 2 diabetes using chemical shift-based water/fat separation. J Magn Reson Imaging 35:899–907. doi:10.1002/jmri.23512
Nakagawa Y, Hattori M, Harada K, Shirase R, Bando M, Okano G (2007) Age-related changes in intramyocellular lipid in humans by in vivo H-MR spectroscopy. Gerontology 53:218–223. doi:10.1159/000100869
Sinha R, Dufour S, Petersen KF, LeBon V, Enoksson S, Ma YZ, Savoye M, Rothman DL, Shulman GI, Caprio S (2002) Assessment of skeletal muscle triglyceride content by (1)H nuclear magnetic resonance spectroscopy in lean and obese adolescents: relationships to insulin sensitivity, total body fat, and central adiposity. Diabetes 51:1022–1027
Watts NB, GLOW investigators (2014) Insights from the Global Longitudinal Study of Osteoporosis in Women (GLOW). Nat Rev Endocrinol 10:412–422. doi:10.1038/nrendo.2014.55
Schwartz AV, Sellmeyer DE, Ensrud KE, Cauley JA, Tabor HK, Schreiner PJ, Jamal SA, Black DM, Cummings SR, Study of Osteoporotic Features Research Group (2001) Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab 86:32–38. doi:10.1210/jcem.86.1.7139
Bermeo S, Gunaratnam K, Duque G (2014) Fat and bone interactions. Curr Osteoporos Rep 12:235–242. doi:10.1007/s11914-014-0199-y
Papaioannou A, Morin S, Cheung AM, Atkinson S, Brown JP, Feldman S, Hanley DA, Hodsman A, Jamal SA, Kaiser SM, Kvern B, Siminoski K, Leslie WD, Scientific Advisory Council of Osteoporosis Canada (2010) 2010 Clinical practice guidelines for the diagnosis and management of osteoporosis in Canada: summary. CMAJ 182:1864–1873. doi:10.1503/cmaj.100771
Kanis JA, Oden A, Johnell O, Jonsson B, de Laet C, Dawson A (2001) The burden of osteoporotic fractures: a method for setting intervention thresholds. Osteoporos Int 12:417–427. doi:10.1007/s001980170112
Elzibak AH, Noseworthy MD (2013) Assessment of diffusion tensor imaging indices in calf muscles following postural change from standing to supine position. Magn Reson Mater Phys. doi:10.1007/s10334-013-0424-1
Lorbergs AL, Noseworthy MD, MacIntyre NJ (2014) Age-related differences in the response of leg muscle cross-sectional area and water diffusivity measures to a period of supine rest. Magn Reson Mater Phys. doi:10.1007/s10334-014-0464-1
Lund H, Christensen L, Savnik A, Boesen J, Danneskiold-Samsoe B, Bliddal H (2002) Volume estimation of extensor muscles of the lower leg based on MR imaging. Eur Radiol 12:2982–2987. doi:10.1007/s00330-002-1334-1
Provencher SW (1993) Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med 30:672–679. doi:10.1002/mrm.1910300604
Kontulainen SA, Johnston JD, Liu D, Leung C, Oxland TR, McKay HA (2008) Strength indices from pQCT imaging predict up to 85% of variance in bone failure properties at tibial epiphysis and diaphysis. J Musculoskelet Neuronal Interact 8:401–409
Lyritis G (ed) (1999) Biomechanical examinations for validation of the bone strength strain index SSI, calculated by peripheral quantitative computed tomography, vol 2. Holonome editions, Athens
Jones CJ, Rikli RE, Beam WC (1999) A 30-s chair-stand test as a measure of lower body strength in community-residing older adults. Res Q Exerc Sport 70:113–119
Topolski TD, LoGerfo J, Patrick DL, Williams B, Walwick J, Patrick MB (2006) The rapid assessment of physical activity (RAPA) among older adults. Prev Chronic Dis 3:A118
Daughton DM, Fix AJ, Kass I, Bell CW, Patil KD (1982) Maximum oxygen consumption and the ADAPT quality-of-life scale. Arch Phys Med Rehabil 63:620–622
Patsch JM, Burghardt AJ, Yap SP, Baum T, Schwartz AV, Joseph GB, Link TM (2013) Increased cortical porosity in type 2 diabetic postmenopausal women with fragility fractures. J Bone Miner Res 28:313–324. doi:10.1002/jbmr.1763
Gnudi S, Sitta E, Fiumi N (2007) Relationship between body composition and bone mineral density in women with and without osteoporosis: relative contribution of lean and fat mass. J Bone Miner Metab 25:326–332. doi:10.1007/s00774-007-0758-8
Studenski S, Perera S, Patel K, Rosano C, Faulkner K, Inzitari M, Brach J, Chandler J, Cawthon P, Connor EB, Nevitt M, Visser M, Kritchevsky S, Badinelli S, Harris T, Newman AB, Cauley J, Ferrucci L, Guralnik J (2011) Gait speed and survival in older adults. JAMA 305:50–58. doi:10.1001/jama.2010.1923
Bennell K, Dobson F, Hinman R (2011) Measures of physical performance assessments: self-Paced Walk Test (SPWT), Stair Climb Test (SCT), Six-Minute Walk Test (6MWT), Chair Stand Test (CST), Timed Up & Go (TUG), Sock Test, Lift and Carry Test (LCT), and Car Task. Arthritis Care Res (Hoboken) 63(11):S350–S370. doi:10.1002/acr.20538
Volpato S, Bianchi L, Lauretani F, Lauretani F, Bandinelli S, Guralnik JM, Zuliani G, Ferrucci L (2012) Role of muscle mass and muscle quality in the association between diabetes and gait speed. Diab Care 35:1672–1679. doi:10.2337/dc11-2202
Ferrucci L, Penninx BW, Leveille SG, Corti MC, Pahor M, Wallace R, Harris TB, Havlik RJ, Guralnik JM (2000) Characteristics of nondisabled older persons who perform poorly in objective tests of lower extremity function. J Am Geriatr Soc 48:1102–1110
Guralnik JM, Simonsick EM, Ferrucci L, Glynn RJ, Berkman LF, Blazer DG, Scherr PA, Wallace RB (1994) A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission. J Gerontol 49:M85–M94
Uusi-Rasi K, Kannus P, Cheng S, Sievanen H, Pasanen M, Heinonen A, Nenonen A, Halleen J, Fuerst T, Genant H, Vuori I (2003) Effect of alendronate and exercise on bone and physical performance of postmenopausal women: a randomized controlled trial. Bone 33:132–143
Stathopoulos KD, Katsimbri P, Atsali E, Metania E, Zoubos AB, Skarantavos G (2011) Age-related differences of bone mass, geometry, and strength in treatment-naive postmenopausal women. A tibia pQCT study. J Clin Densitom 14:33–40. doi:10.1016/j.jocd.2010.11.004
Edwards MH, Gregson CL, Patel HP, Jameson KA, Harvey NC, Sayer AA, Dennison EM, Cooper C (2013) Muscle size, strength, and physical performance and their associations with bone structure in the Hertfordshire Cohort Study. J Bone Miner Res 28:2295–2304. doi:10.1002/jbmr.1972
Acknowledgments
The study was funded in part by a grant from The Arthritis Society. The authors thank Dr. Jean Wessel for her contribution to study design. The authors appreciate the assistance and guidance from Norm Konyer and the MRI technologists (Janet Burr, Cheryl Contant, Julie Lecomte). Thanks to Dr. Christopher Gordon and Lesley Beaumont for their assistance with pQCT measurements. AL held doctoral scholarships from the Ontario Women’s Health Scholar Award and the Joint Motion Program, a Canadian Institutes of Health Research Training Program in Musculoskeletal Health Research and Leadership.
Conflict of interest
Amanda L. Lorbergs, Michael D. Noseworthy, Jonathan D. Adachi, Paul W. Stratford, and Norma J. MacIntyre declare that they have no conflict of interest.
Human and animal rights and informed consent
Our institutional Research Ethics Review Board approved the study protocol, and all participants provided written informed consent prior to enrolling in the study.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lorbergs, A.L., Noseworthy, M.D., Adachi, J.D. et al. Fat Infiltration in the Leg is Associated with Bone Geometry and Physical Function in Healthy Older Women. Calcif Tissue Int 97, 353–363 (2015). https://doi.org/10.1007/s00223-015-0018-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00223-015-0018-1