Skeletal Muscle Lipid Content and Oxidative Activity in Relation to Muscle Fiber Type in Aging and Metabolic Syndrome
Abstract
One of the most noticeable effects of aging is the reduction in skeletal muscle mass and strength (sarcopenia). The metabolic syndrome (MS) is also prevalent in old subjects, but its relevance to skeletal muscle characteristics has poorly been investigated. Immunohistochemical studies were performed with muscle biopsies from young (22 years) and old (73 years) men with and without MS to reveal age-dependent and MS-associated modifications of fiber-type characteristics. Atrophy of type II fibers and altered fiber shape characterized muscle aging in lean healthy men. In contrast, increased cross-sectional area of the most abundant type I and type IIA fibers, and reduced cytochrome c oxidase content in all fiber types, characterized MS. Aging and particularly MS were associated with accumulation of intramyocellular lipid droplets. Although lipids mostly accumulated in type I fibers, matrix-assisted laser desorption/ionization-mass spectrometry imaging of intramyocellular lipids did not distinguish fiber types, but clearly separated young, old, and MS subjects. In conclusion, our study suggests that MS in the elderly persons is associated with alterations in skeletal muscle at a fiber-type specific level. Overall, these fiber type-specific modifications may be important both for the age-related loss of muscle mass and strength and for the increased prevalence of MS in elderly subjects.
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Aging and disuse, even in the absence of insulin resistance, are associated with increased intramyocellular lipids.
“However, aging and disuse, even in the absence of insulin resistance are associated with increased IMCLs [57, 60–63].”
From Targeting Intramyocellular Lipids to Improve Aging Muscle Function (2025) · cites this paper as [63]
Compared with healthy older adults, frail, mobility-impaired and high fall-risk older adults with reduced muscle performance have greater intramyocellular lipids.
“Compared to healthy older adults, studies report greater IMCLs in frail, mobility-impaired and high fall-risk older adults with reduced muscle performance, who are at increased risk of death and disability ([63, 70, 71].”
From Targeting Intramyocellular Lipids to Improve Aging Muscle Function (2025) · cites this paper as [63]
Cites
Alberti, K. G. M. M., Eckel, R. H., Grundy, S. M., Zimmet, P. Z., Cleeman, J. I., Donato, K. A., Fruchart, J.-C., James, W. P. T., Loria, C. M., & Smith, S. C. (2009) · Circulation · doi:10.1161/circulationaha.109.192644 · Cited by 14,860 · see citing works
Cardiovascular Morbidity and Mortality Associated With the Metabolic Syndrome
Isomaa, B., Almgren, P., Tuomi, T., Forsén, B., Lahti, K., Nissén, M., Taskinen, M.-R., & Groop, L. (2001) · Diabetes Care · doi:10.2337/diacare.24.4.683 · Cited by 4,760 · see citing works
What is the cause of the ageing atrophy?
Lexell, J. E., Taylor, C. C., & Sjöstróm, M. (1988) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(88)90132-3 · Cited by 2,080 · see citing works
Aging of skeletal muscle: a 12-yr longitudinal study
Frontera, W. R., Hughes, V. A., Fielding, R. A., Fiatarone, M. A., Evans, W. J., & Roubenoff, R. (2000) · Journal of Applied Physiology · doi:10.1152/jappl.2000.88.4.1321 · Cited by 1,443 · see citing works
Decline in skeletal muscle mitochondrial function with aging in humans
Short, K. R., Bigelow, M. L., Kahl, J., Singh, R., Coenen-Schimke, J., Raghavakaimal, S., & Nair, K. S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0501559102 · Cited by 1,333 · see citing works
Goodpaster, B. H. (2001) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.86.12.5755 · Cited by 1,194 · see citing works
Borkman, M., Storlien, L. H., Pan, D. A., Jenkins, A. B., Chisholm, D. J., & Campbell, L. V. (1993) · New England Journal of Medicine · doi:10.1056/nejm199301283280404 · Cited by 835 · see citing works
Sarcopenia: etiology, clinical consequences, intervention, and assessment
Lang, T., Streeper, T., Cawthon, P. M., Baldwin, K., Taaffe, D. R., & Harris, T. B. (2009) · Osteoporosis International · doi:10.1007/s00198-009-1059-y · Cited by 780 · see citing works
Physiological changes in ageing muscles
Campbell, M. J., McComas, A. J., & Petito, F. (1973) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.36.2.174 · Cited by 738 · see citing works
Metabolic Syndrome: A Multiplex Cardiovascular Risk Factor
Grundy, S. M. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-0513 · Cited by 658 · see citing works
He, J., Watkins, S., & Kelley, D. E. (2001) · Diabetes · doi:10.2337/diabetes.50.4.817 · Cited by 518 · see citing works
Kosek, D. J., Kim, J.-S., Petrella, J. K., Cross, J. M., & Bamman, M. M. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01474.2005 · Cited by 503 · see citing works
Simoneau, J., Veerkamp, J. H., Turcotte, L. P., & Kelley, D. E. (1999) · The FASEB Journal · doi:10.1096/fasebj.13.14.2051 · Cited by 491 · see citing works
Satellite cell content is specifically reduced in type II skeletal muscle fibers in the elderly
Verdijk, L. B., Koopman, R., Schaart, G., Meijer, K., Savelberg, H. H. C. M., & van Loon, L. J. C. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00278.2006 · Cited by 489 · see citing works
FORD, E. S., LI, C., & ZHAO, G. (2010) · Journal of Diabetes · doi:10.1111/j.1753-0407.2010.00078.x · Cited by 471 · see citing works
Skeletal muscle adaptations to endurance training in 60- to 70-yr-old men and women
Coggan, A. R., Spina, R. J., King, D. S., Rogers, M. A., Brown, M., Nemeth, P. M., & Holloszy, J. O. (1992) · Journal of Applied Physiology · doi:10.1152/jappl.1992.72.5.1780 · Cited by 457 · see citing works
Effect of barbiturates on ‘quantal’ synaptic transmission in spinal motoneurones
Weakly, J. N. (1969) · The Journal of Physiology · doi:10.1113/jphysiol.1969.sp008898 · Cited by 432 · see citing works
Jones, P. R., & PEARSON, J. S. (1969) · PubMed · Cited by 429 · see citing works
Syndrome X and Mortality: A Population-based Study
Trevisan, M., Liu, J., Bahsas, F. B., & Menotti, A. (1998) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a009572 · Cited by 389 · see citing works
MALDI Imaging of Lipid Biochemistry in Tissues by Mass Spectrometry
Berry, K. A. Z., Hankin, J. A., Barkley, R. M., Spraggins, J. M., Caprioli, R. M., & Murphy, R. C. (2011) · Chemical Reviews · doi:10.1021/cr200280p · Cited by 388 · see citing works
Larsson, L., Li, X., & Frontera, W. R. (1997) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1997.272.2.c638 · Cited by 367 · see citing works
Skeletal Muscle Mitochondria and Aging: A Review
Peterson, C. M., Johannsen, D. L., & Ravussin, É. (2012) · Journal of Aging Research · doi:10.1155/2012/194821 · Cited by 318 · see citing works
Muscle fibre type adaptation in the elderly human muscle
Andersen, J. L. (2003) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1034/j.1600-0838.2003.00299.x · Cited by 316 · see citing works
Intramuscular and Liver Triglycerides Are Increased in the Elderly
Cree‐Green, M., Newcomer, B. R., Katsanos, C. S., Sheffield‐Moore, M., Chinkes, D. L., Aarsland, A. A., Urban, R. J., & Wolfe, R. R. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-031986 · Cited by 273 · see citing works
The Effect of Aging on Human Skeletal Muscle Mitochondrial and Intramyocellular Lipid Ultrastructure
Crane, J. D., Devries, M. C., Safdar, A., Hamadeh, M. J., & Tarnopolsky, M. A. (2010) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/glp179 · Cited by 262 · see citing works
Satellite cell numbers in young and older men 24 hours after eccentric exercise
Dreyer, H. C., Blanco, C. E., Sattler, F. R., Schroeder, E. T., & Wiswell, R. A. (2006) · Muscle & Nerve · doi:10.1002/mus.20461 · Cited by 256 · see citing works
Denervation Causes Fiber Atrophy and Myosin Heavy Chain Co-Expression in Senescent Skeletal Muscle
Rowan, S. L., Rygiel, K. A., Purves-Smith, F. M., Solbak, N. M., Turnbull, D. M., & Hepple, R. T. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029082 · Cited by 246 · see citing works
Fibre types in skeletal muscle: a personal account
Schiaffino, S. (2010) · Acta Physiologica · doi:10.1111/j.1748-1716.2010.02130.x · Cited by 227 · see citing works
Fat content in individual muscle fibers of lean and obese subjects.
Malenfant, P., Joanisse, D., Thériault, R., Goodpaster, B., Kelley, D., & Simoneau, J.-A. (2001) · International Journal of Obesity · doi:10.1038/sj.ijo.0801733 · Cited by 227 · see citing works
Lexell, J. E., & Downham, D. Y. (1991) · Acta Neuropathologica · doi:10.1007/bf00293457 · Cited by 188 · see citing works
Russell, A. P., Gastaldi, G., Bobbioni-Harsch, E., Arboit, P., Gobelet, C., Dériaz, O., Golay, A., Witztum, J. L., & Giacobino, J.-P. (2003) · FEBS Letters · doi:10.1016/s0014-5793(03)00875-5 · Cited by 166 · see citing works
Gavin, T. P., Stallings, H. W., Zwetsloot, K. A., Westerkamp, L. M., Ryan, N. A., Moore, R. A., Pofahl, W. E., & Hickner, R. C. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00353.2004 · Cited by 148 · see citing works
Watt, M. J., & Hoy, A. J. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00561.2011 · Cited by 142 · see citing works
Heart involvement in muscular dystrophies due to sarcoglycan gene mutations
Melacini, P., Fanin, M., Duggan, D. J., Freda, M. P., Berardinelli, A. L., Danieli, G. A., Barchitta, A., Hoffman, E. P., Volta, S. D., & Angelini, C. I. (1999) · Muscle & Nerve · doi:10.1002/(sici)1097-4598(199904)22:4 · Cited by 136 · see citing works
Barthélemy, J., Pichot, V., Dauphinot, V., Celle, S., Laurent, B., Garcin, A., Maudoux, D., Kerleroux, J., Lacour, J.-R., Kossovsky, M. P., et al. (2007) · Neuroepidemiology · doi:10.1159/000108914 · Cited by 121 · see citing works
Self-citationJohannsen, D. L., Conley, K. E., Bajpeyi, S., Punyanitya, M., Gallagher, D., Zhang, Z., Covington, J. D., Smith, S. R., & Ravussin, É. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-1798 · Cited by 107 · see citing works
Age-associated Decrease of Type IIA/B Human Skeletal Muscle Fibers
Lee, W., Cheung, W., Qin, L., Tang, N., & Leung, K. (2006) · Clinical Orthopaedics and Related Research · doi:10.1097/01.blo.0000218757.97063.21 · Cited by 103 · see citing works
Age changes in size and number of muscle fibers in human minor pectoral muscle
Sato, T., Akatsuka, H., Kito, K., Tokoro, Y., Tauchi, H., & Kato, K. (1984) · Mechanisms of Ageing and Development · doi:10.1016/0047-6374(84)90156-8 · Cited by 92 · see citing works
Verney, J., Kadi, F., Saafi, M. A., Piehl‐Aulin, K., & Denis, C. (2006) · European Journal of Applied Physiology · doi:10.1007/s00421-006-0175-z · Cited by 69 · see citing works
Self-citationEffect of Training on Muscle Triacylglycerol and Structural Lipids
Helge, J. W., & Dela, F. (2003) · Diabetes · doi:10.2337/diabetes.52.8.1881 · Cited by 66 · see citing works
Yang, E. J., Lim, S. K., Lim, J., Kim, K. W., Jang, H. C., & Paik, N. (2011) · Metabolism · doi:10.1016/j.metabol.2011.07.005 · Cited by 64 · see citing works
Kirkeby, S., & Garbarsch, C. (2000) · PubMed · doi:10.14670/hh-15.61 · Cited by 57 · see citing works
Meunier, B., Picard, B. B., Astruc, T., et al. (2010) · Histochemistry and Cell Biology · doi:10.1007/s00418-010-0733-7 · Cited by 47 · see citing works
Self-citationA Questionnaire-Based Assessment of Daily Physical Activity in Heart Failure
Garet, M., Barthélemy, J., Degache, F., Costes, F., Dacosta, A., Isaaz, K., Lacour, J. R., & Roche, F. (2004) · European Journal of Heart Failure · doi:10.1016/j.ejheart.2003.11.022 · Cited by 41 · see citing works
Self-citationKim, J., Hinchcliff, K. W., Yamaguchi, M., Beard, L. A., Markert, C. D., & Devor, S. T. (2004) · The Veterinary Journal · doi:10.1016/j.tvjl.2004.03.016 · Cited by 38 · see citing works
Severe atrophy of slow myofibers in aging muscle is concealed by myosin heavy chain co-expression
Purves-Smith, F. M., Solbak, N. M., Rowan, S. L., & Hepple, R. T. (2012) · Experimental Gerontology · doi:10.1016/j.exger.2012.07.013 · Cited by 31 · see citing works
Does Methylene Blue Protect the Kidney Tissues from Damage Induced by Ciclosporin A Treatment?
Rezzani, R., Rodella, L. F., Corsetti, G., et al. (2001) · The Nephron journals/Nephron journals · doi:10.1159/000046094 · Cited by 28 · see citing works
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Hamrick, M. W., McGee-Lawrence, M. E., & Frechette, D. M. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00069 · Cited by 372 · see citing works
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Rogeri, P. S., Zanella, R., Martins, G. L., Garcia, M. D. A., Leite, G., Lugaresi, R., Gasparini, S. O., Sperandio, G. A., Ferreira, L. H. B., Souza-Junior, T. P., et al. (2021) · Nutrients · doi:10.3390/nu14010052 · Cited by 181 · see citing works
St‐Jean‐Pelletier, F., Pion, C. H., Leduc‐Gaudet, J., Sgarioto, N., Zovilé, I., Barbat‐Artigas, S., Reynaud, O., Alkaterji, F., Lemieux, F. C., Grenon, A., et al. (2017) · Journal of Cachexia, Sarcopenia and Muscle · doi:10.1002/jcsm.12139 · Cited by 156 · see citing works
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“However, aging and disuse, even in the absence of insulin resistance are associated with increased IMCLs [57, 60–63].”
- Authors
- Gueugneau, M., Coudy-Gandilhon, C., Théron, L., Meunier, B., Barboiron, C., Combaret, L., Taillandier, D., Polge, C., Attaix, D., Picard, B., Verney, J., Roche, F., Féasson, L., Barthélémy, J.-C., & Béchet, D.
- Affiliations
- Université Clermont Auvergne (FR)
- Unité de Nutrition Humaine (FR)
- Université de Lyon (FR)
- ORCID
- Venue
- The Journals of Gerontology Series A: Biological Sciences and Medical Sciences
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-06-17
- Volume
- 70
- Issue
- 5
- Pages
- 566-576
- ISSN
- 1079-5006 (ISSN-L)
- 1758-535X
- OpenAlex
- W2113223144
- Cited by
- 137
- References
- 47
- Citations by year
- 2026: 8 · 2025: 15 · 2024: 15 · 2023: 11 · 2022: 15 · 2021: 12 · 2020: 14 · 2019: 9 · 2018: 9 · 2017: 9 · 2016: 14 · 2015: 4 · 2014: 2
- FWCI
- 3.96
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journals of Gerontology Series A (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Directorate for Biological Sciences
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Physiology › Nutrition and Health in Aging
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Keywords
- skeletal muscle aging, sarcopenia, metabolic syndrome, muscle fiber type, intramyocellular lipid, lipid droplets, cytochrome c oxidase, oxidative activity, type I muscle fibers, muscle mass and strength, older men
- MeSH terms
- Aged, Aging, Biopsy, Body Composition, Electron Transport Complex IV, Energy Metabolism, Humans, Male, Absorptiometry, Photon, Muscle Fibers, Skeletal, Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization, Metabolic Syndrome, Lipid Metabolism, Muscle Strength, Young Adult, Sarcopenia
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