Abstract
Muscle mass is particularly relevant to follow during aging, owing to its link with physical performance and autonomy. The objectives of this work were to assess muscle volume (MV) and intramuscular fat (IMF) for all the muscles of the thigh in a large population of young and elderly healthy individuals using magnetic resonance imaging (MRI) to test the effect of gender and age on MV and IMF and to determine the best representative slice for the estimation of MV and IMF. The study enrolled 105 healthy young (range 20–30 years) and older (range 70–80 years) subjects. MRI scans were acquired along the femur length using a three-dimension three-point Dixon proton density-weighted gradient echo sequence. MV and IMF were estimated from all the slices. The effects of age and gender on MV and IMF were assessed. Predictive equations for MV and IMF were established using a single slice at various femur levels for each muscle in order to reduce the analysis process. MV was decreased with aging in both genders, particularly in the quadriceps femoris. IMF was largely increased with aging in men and, to a lesser extent, in women. Percentages of MV decrease and IMF increase with aging varied according to the muscle. Predictive equations to predict MV and IMF from single slices are provided and were validated. This study is the first one to provide muscle volume and intramuscular fat infiltration in all the muscles of the thigh in a large population of young and elderly healthy subjects.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdul-Rahman HS, Gdeisat MA, Burton DR, Lalor MJ, Lilley F, Moore CJ (2007) Fast and robust three-dimensional best path phase unwrapping algorithm. Appl Opt 46:6623–6635
Argiles JM, Busquets S, Felipe A, Lopez-Soriano FJ (2006) Muscle wasting in cancer and ageing: cachexia versus sarcopenia. Adv Gerontol 18:39–54
Azzabou N, Loureiro de Sousa P, Caldas E, Carlier PG (2015) Validation of a generic approach to muscle water T2 determination at 3T in fat-infiltrated skeletal muscle. J Magn Reson Imaging 41:645–653
Cotofana S, Hudelmaier M, Wirth W, Himmer M, Ring-Dimitriou S, Sanger AM, Eckstein F (2010) Correlation between single-slice muscle anatomical cross-sectional area and muscle volume in thigh extensors, flexors and adductors of perimenopausal women. Eur J Appl Physiol 110:91–97
D’Antona G, Lanfranconi F, Pellegrino MA, Brocca L, Adami R, Rossi R, Moro G, Miotti D, Canepari M, Bottinelli R (2006) Skeletal muscle hypertrophy and structure and function of skeletal muscle fibres in male body builders. J Physiol Lond 570:611–627
Delmonico MJ, Harris TB, Visser M, Park SW, Conroy MB, Velasquez-Mieyer P, Boudreau R, Manini TM, Nevitt M, Newman AB, Goodpaster BH, A Health Body (2009) Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr 90:1579–1585
Forsberg AM, Nilsson E, Werneman J, Bergstrom J, Hultman E (1991) Muscle composition in relation to age and sex. Clin Sci (Lond) 81:249–256
Frantzell A, Ingelmark BE (1951) Occurrence and distribution of fat in human muscles at various age levels; a morphologic and roentgenologic investigation. Acta Soc Med Ups 56:59–87
Glover GH, Schneider E (1991) Three-point Dixon technique for true water/fat decomposition with B0 inhomogeneity correction. Magn Reson Med 18:371–383
Hasson CJ, Kent-Braun JA, Caldwell GE (2011) Contractile and non-contractile tissue volume and distribution in ankle muscles of young and older adults. J Biomech 44:2299–2306
Hernando D, Haldar JP, Sutton BP, Ma J, Kellman P, Liang ZP (2008) Joint estimation of water/fat images and field inhomogeneity map. Magn Reson Med 59:571–580
Hernando D, Kellman P, Haldar JP, Liang ZP (2010) Robust water/fat separation in the presence of large field inhomogeneities using a graph cut algorithm. Magn Reson Med 63:79–90
Hines CD, Yu H, Shimakawa A, McKenzie CA, Brittain JH, Reeder SB (2009) T1 independent, T2* corrected MRI with accurate spectral modeling for quantification of fat: validation in a fat-water-SPIO phantom. J Magn Reson Imaging 30:1215–1222
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
Kawakami Y, Muraoka Y, Kubo K, Suzuki Y, Fukunaga T (2000) Changes in muscle size and architecture following 20 days of bed rest. J Gravity Physiol 7:53–59
Kent-Braun JA, Ng AV, Young K (2000) Skeletal muscle contractile and noncontractile components in young and older women and men. J Appl Physiol 88:662–668
Kouzaki M, Masani K, Akima H, Shirasawa H, Fukuoka H, Kanehisa H, Fukunaga T (2007) Effects of 20-day bed rest with and without strength training on postural sway during quiet standing. Acta Physiol (Oxf) 189:279–292
Leskinen T, Sipila S, Alen M, Cheng S, Pietilainen KH, Usenius JP, Suominen H, Kovanen V, Kainulainen H, Kaprio J, Kujala UM (2009) Leisure-time physical activity and high-risk fat: a longitudinal population-based twin study. Int J Obes 33:1211–1218
Macaluso A, Nimmo MA, Foster JE, Cockburn M, McMillan NC, De Vito G (2002) Contractile muscle volume and agonist-antagonist coactivation account for differences in torque between young and older women. Muscle Nerve 25:858–863
Maden-Wilkinson TM, Degens H, Jones DA, McPhee JS (2013) Comparison of MRI and DXA to measure muscle size and age-related atrophy in thigh muscles. J Musculoskelet Neuronal Interact 13:320–328
McPhee JS, Hogrel JY, Maier AB, Seppet E, Seynnes OR, Sipilä S, Bottinelli R, Barnouin Y, Bijlsma AY, Gapeyeva H, Maden-Wilkinson TM, Meskers CG, Pääsuke M, Sillanpää E, Stenroth L, Butler-Browne G, Narici MV, Jones DA (2013) Physiological and functional evaluation of healthy young and older men and women: design of the European MyoAge study. Biogerontology 14:325–337
Morse CI, Thom JM, Birch KM, Narici MV (2005a) Changes in triceps surae muscle architecture with sarcopenia. Acta Physiol Scand 183:291–298
Morse CI, Thom JM, Mian OS, Muirhead A, Birch KM, Narici MV (2005b) Muscle strength, volume and activation following 12-month resistance training in 70-year-old males. Eur J Appl Physiol 95:197–204
Morse CI, Degens H, Jones DA (2007) The validity of estimating quadriceps volume from single MRI cross-sections in young men. Eur J Appl Physiol 100:267–274
Narici MV, Maganaris CN, Reeves ND, Capodaglio P (2003) Effect of aging on human muscle architecture. J Appl Physiol 95:2229–2234
Nilwik R, Snijders T, Leenders M, Groen BB, van Kranenburg J, Verdijk LB, van Loon LJ (2013) The decline in skeletal muscle mass with aging is mainly attributed to a reduction in type II muscle fiber size. Exp Gerontol 48:492–498
Ogawa M, Yasuda T, Abe T (2012) Component characteristics of thigh muscle volume in young and older healthy men. Clin Physiol Funct Imaging 32:89–93
Overend TJ, Cunningham DA, Paterson DH, Lefcoe MS (1992) Thigh composition in young and elderly men determined by computed tomography. Clin Physiol 12:629–640
Piepoli MF, Kaczmarek A, Francis DP, Davies LC, Rauchhaus M, Jankowska EA, Anker SD, Capucci A, Banasiak W, Ponikowski P (2006) Reduced peripheral skeletal muscle mass and abnormal reflex physiology in chronic heart failure. Circulation 114:126–134
Reeder SB, Pineda AR, Wen Z, Shimakawa A, Yu H, Brittain JH, Gold GE, Beaulieu CH, Pelc NJ (2005) Iterative decomposition of water and fat with echo asymmetry and least-squares estimation (IDEAL): application with fast spin-echo imaging. Magn Reson Med 54:636–644
Reeder SB, Robson PM, Yu H, Shimakawa A, Hines CD, McKenzie CA, Brittain JH (2009) Quantification of hepatic steatosis with MRI: the effects of accurate fat spectral modeling. J Magn Reson Imaging 29:1332–1339
Roubenoff R (2000) Acquired immunodeficiency syndrome wasting, functional performance, and quality of life. Am J Manag Care 6:1003–1016
Sharma SD, Hu HH, Nayak KS (2012) Accelerated water-fat imaging using restricted subspace field map estimation and compressed sensing. Magn Reson Med 67:650–659
Stein TP, Wade CE (2005) Metabolic consequences of muscle disuse atrophy. J Nutr 135:1824S–1828S
Trappe TA, Lindquist DM, Carrithers JA (2001) Muscle-specific atrophy of the quadriceps femoris with aging. J Appl Physiol 90:2070–2074
Verdijk LB, Koopman R, Schaart G, Meijer K, Savelberg HH, van Loon LJ (2007) Satellite cell content is specifically reduced in type II skeletal muscle fibers in the elderly. Am J Physiol Endocrinol Metab 292:E151–E157
Vermeeren MAP, Creutzberg EC, Schols A, Postma DS, Pieters WR, Roldaan AC, Wouters EFM, Grp CS (2006) Prevalence of nutritional depletion in a large out-patient population of patients with COPD. Respir Med 100:1349–1355
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
Acknowledgments
This study was funded in part by the EU within the frame of the FP7 Project Myoage (contract n 223576) and the Association Française contre les Myopathies. The authors wish to thank the Comité Départemental de la Retraite Sportive de Paris, the Lions Club de Paris, and their members who volunteered to take part in this study. The authors wish to thank Jean-Marc Boisserie and Julien Le Louër for their skillful assistance in MRI explorations.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Table 1
(DOC 36 kb)
Supplementary Table 2
(DOC 36 kb)
About this article
Cite this article
Hogrel, JY., Barnouin, Y., Azzabou, N. et al. NMR imaging estimates of muscle volume and intramuscular fat infiltration in the thigh: variations with muscle, gender, and age. AGE 37, 60 (2015). https://doi.org/10.1007/s11357-015-9798-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11357-015-9798-5