The DOI matches its Crossref record; 273 of the 275 references it cites were found in a registry or an index.
Muscle quality in aging: a multi-dimensional approach to muscle functioning with applications for treatment.
Open accessAbstract
Aging is often accompanied by declines in physical functioning which impedes older adults' quality of life, sense of independence, and ability to perform daily tasks. Age-related decreases in skeletal muscle quantity, termed sarcopenia, have traditionally been blamed for these physical decrements. However, recent evidence suggests that the quality of muscle tissue may be more functionally relevant than its quantity. 'Muscle quality' has been emerging as a means to elucidate and describe the intricate intramuscular changes associated with muscle performance in the context of aging and sarcopenia. While muscle quality has most commonly been defined in terms of muscle composition or relative strength, at the core, muscle quality really describes muscle's ability to function. Skeletal muscle displays a strong structure-function relationship by which several architectural characteristics factor into its functional capacity. This review describes the structural, physiological, and functional determinants of muscle quality at the tissue and cellular level, while also introducing other novel parameters such as sarcomere spacing and integrity, circulating biomarkers, and the muscle quality index. Muscle qualitative features are described from the perspective of how physical exercise may improve muscle quality in older adults. This broad, multidimensional perspective of muscle quality in the context of aging and sarcopenia offers comprehensive insights for consideration and integration in developing improved prognostic tools for research and clinical care, while also promoting translational approaches to the design of novel targeted intervention strategies designed to maintain function and mobility into late life.
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“Also, the effectiveness of some other nutritional supplements such as omega-3 fatty acids, creatine, and β-hydroxy β-methylbutyrate, to promote muscle functions were reported (Fragala et al., 2015).”
From Effect of resistance training and fish protein intake on motor unit firing pattern and motor function of elderly (2018) · cites this paper as Fragala et al., 2015
Citations
Cites
Items 201–273 of 273
Fielding, R. A. (1995) · Journal of the American College of Nutrition · doi:10.1080/07315724.1995.10718547 · Cited by 94
Fragala, M. S., Jajtner, A. R., Beyer, K. S., Townsend, J. R., Emerson, N. S., Scanlon, T. C., Oliveira, L. P., Hoffman, J. R., & Stout, J. R. (2014) · Journal of Cachexia, Sarcopenia and Muscle · doi:10.1007/s13539-013-0120-z · Cited by 94
Self-citationThe muscle ultrastructure: a structural perspective of the sarcomere
Au, Y. (2004) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-004-4282-x · Cited by 93
Correa‐de‐Araujo, R., & Hadley, E. (2014) · The Journals of Gerontology Series A · doi:10.1093/gerona/glt208 · Cited by 93
Effects of Muscle Strength Training and Testosterone in Frail Elderly Males
Sullivan, D. H., Roberson, P. K., Johnson, L. E., Bishara, O., Evans, W. J., Smith, E. S., & PRICE, J. A. (2005) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000181840.54860.8b · Cited by 92
Myofilament lengths of cat skeletal muscle: Theoretical considerations and functional implications
Herzog, W., Kamal, S., & Clarke, H. D. (1992) · Journal of Biomechanics · doi:10.1016/0021-9290(92)90235-s · Cited by 91
Sex hormones and sarcopenia in older persons
Maggio, M. G., Lauretani, F., & Ceda, G. P. (2012) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0b013e32835b6044 · Cited by 91
Functional Impact of Relative Versus Absolute Sarcopenia in Healthy Older Women
Estrada, M. R., Kleppinger, A., Judge, J. O., Walsh, S. J., & Kuchel, G. A. (2007) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2007.01436.x · Cited by 89
Self-citationRousseau, J. H., Kleppinger, A., & Kenny, A. M. (2009) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2008.01870.x · Cited by 88
Estrogen Replacement, Muscle Composition, and Physical Function: The Health ABC Study
Taaffe, D. R., Newman, A. B., Haggerty, C. L., Colbert, L. H., de Rekeneire, N., Visser, M., Goodpaster, B. H., Nevitt, M. C., Tylavsky, F. A., & Harris, T. B. (2005) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000181678.28092.31 · Cited by 88
Effects of Exercise on Senescent Muscle
Evans, W. J. (2002) · Clinical Orthopaedics and Related Research · doi:10.1097/00003086-200210001-00025 · Cited by 88
The association between dehydroepiandosterone and frailty in older men and women
Voznesensky, M., Walsh, S., Dauser, D., Brindisi, J., & Kenny, A. M. (2009) · Age and Ageing · doi:10.1093/ageing/afp015 · Cited by 88 · cited 2×
“Hormonal interventions have typically been explored as a treatment for muscle wasting based on the cross-sectional associations between circulating hormone concentrations and skeletal muscle mass and characteristics of frailty in older men and women [179, 180].”
BackgroundMeasurement of muscle disease by quantitative second-harmonic generation imaging
Plotnikov, S. V., Kenny, R. A., Walsh, S. J., Zubrowski, B., Joseph, C., Scranton, V. L., Kuchel, G. A., Dauser, D., Xu, M., Pilbeam, C. C., et al. (2008) · Journal of Biomedical Optics · doi:10.1117/1.2967536 · Cited by 86
Self-citationBulk magnetic susceptibility effects on the assessment of intra‐ and extramyocellular lipids in vivo
Szczepaniak, L. S., Dobbins, R. L., Stein, D. T., & McGarry, J. (2002) · Magnetic Resonance in Medicine · doi:10.1002/mrm.10086 · Cited by 85
Exercise and sex steroid hormones in skeletal muscle
Sato, K., & Iemitsu, M. (2014) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2014.03.009 · Cited by 84
Sarcopenia and Hypertrophy: A Role for Insulin-Like Growth Factor-1 in Aged Muscle?
Hameed, M., Harridge, S. D. R., & Goldspink, G. (2002) · Exercise and Sport Sciences Reviews · doi:10.1097/00003677-200201000-00004 · Cited by 77
The incidence of abnormality in control human peripheral nerves studied by single axon dissection.
Arnold, N., & Harriman, D. G. F. (1970) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.33.1.55 · Cited by 77
Sarcopenia: Pharmacology of Today and Tomorrow
Brotto, M., & de Abreu, E. L. (2012) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.112.191759 · Cited by 76
Gollapudi, S. K., & Lin, D. C. (2009) · Journal of Biomechanics · doi:10.1016/j.jbiomech.2009.06.013 · Cited by 73
MOTONEURONE DISEASE AND AGEING
McComas, A. J., Upton, A. R. M., & Sica, R. E. P. (1973) · The Lancet · doi:10.1016/s0140-6736(73)92735-9 · Cited by 69
Molecular and cell-based therapies for muscle degenerations: a road under construction
Berardi, E., Annibali, D., Cassano, M., Crippa, S., & Sampaolesi, M. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00119 · Cited by 69
Baker, W. L., Karan, S., & Kenny, A. M. (2011) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2011.03410.x · Cited by 68
Self-citationFuller, N., Hardingham, C. R., Graves, M. J., Screaton, N. J., Dixon, A. K., Ward, L. C., & Elia, M. (1999) · International Journal of Obesity · doi:10.1038/sj.ijo.0801070 · Cited by 68
Age-Related Changes in Intramyocellular Lipid in Humans by in vivo 1H-MR Spectroscopy
Nakagawa, Y., Hattori, M., Harada, K., Shirase, R., Bando, M., & OKANO, G. (2007) · Gerontology · doi:10.1159/000100869 · Cited by 68
Qaisar, R., Renaud, G., Morine, K., Barton, E. R., Sweeney, H. L., & Larsson, L. (2011) · The FASEB Journal · doi:10.1096/fj.11-192195 · Cited by 68
Debio-025 is more effective than prednisone in reducing muscular pathology in mdx mice
Wissing, E. R., Millay, D. P., Vuagniaux, G., & Molkentin, J. D. (2010) · Neuromuscular Disorders · doi:10.1016/j.nmd.2010.06.016 · Cited by 66
The Role of Muscle microRNAs in Repairing the Neuromuscular Junction
Valdez, G., Heyer, M. P., Feng, G., & Sanes, J. R. (2014) · PLoS ONE · doi:10.1371/journal.pone.0093140 · Cited by 65
Ruan, X. Y., Gallagher, D., Harris, T. B., Albu, J., Heymsfield, S. B., Kuznia, P., & Heshka, S. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00304.2006 · Cited by 65
Androgen therapy improves muscle mass and strength but not muscle quality: results from two studies
Schroeder, E. T., Terk, M. R., & Sattler, F. R. (2003) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00032.2003 · Cited by 64
Gender Differences in Anthropometric Predictors of Physical Performance in Older Adults
Fragala, M. S., Clark, M. H., Walsh, S. J., Kleppinger, A., Judge, J. O., Kuchel, G. A., & Kenny, R. A. (2012) · Gender Medicine · doi:10.1016/j.genm.2012.10.004 · Cited by 62
Self-citationBhasin, S., He, E. J., Kawakubo, M., Schroeder, E. T., Yarasheski, K., Opiteck, G. J., Reicin, A., Chen, F., Lam, R., Tsou, J. A., et al. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-1434 · Cited by 62
Cadilla, R., & Turnbull, P. (2006) · Current Topics in Medicinal Chemistry · doi:10.2174/156802606776173456 · Cited by 59
Kirkeby, S., & Garbarsch, C. (2000) · PubMed · doi:10.14670/hh-15.61 · Cited by 57
Greenhalgh, C., Prent, N., Green, C., Cisek, R., Major, A. A., Stewart, B. A., & Barzda, V. (2007) · Applied Optics · doi:10.1364/ao.46.001852 · Cited by 57
Associated hormonal declines in aging: DHEAS.
Perrini, S., Laviola, L., Natalicchio, A., & Giorgino, F. (2005) · PubMed · Cited by 56
Iglay, H. B., Apolzan, J. W., Gerrard, D. E., Eash, J. K., Anderson, J. C., & Campbell, W. W. (2009) · The journal of nutrition health & aging · doi:10.1007/s12603-009-0016-y · Cited by 56
Sharman, M. J., Newton, R. U., Triplett-McBride, T., McGuigan, M. R., McBride, J. M., HÄKKINEN, A. H., Häkkinen, K., & Kraemer, W. J. (2001) · European Journal of Applied Physiology · doi:10.1007/s004210000334 · Cited by 56
McCormack, W. P., Stout, J. R., Emerson, N. S., Scanlon, T. C., Warren, A. M., Wells, A. J., Gonzalez, A. M., Mangine, G. T., Robinson, E. H., Fragala, M. S., et al. (2013) · Experimental Gerontology · doi:10.1016/j.exger.2013.06.003 · Cited by 53
Self-citationCellular and molecular aspects of muscle growth, adaptation and ageing
Goldspink, G. (1998) · Gerodontology · doi:10.1111/j.1741-2358.1998.00035.x · Cited by 52
Control of muscle fibre size: a crucial factor in ageing
Hughes, S. M., & Schiaffino, S. (1999) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.1999.00619.x · Cited by 51
Effects of Ultra‐Low‐Dose Estrogen Therapy on Muscle and Physical Function in Older Women
Kenny, A. M., Kleppinger, A., Wang, Y., & Prestwood, K. M. (2005) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2005.53567.x · Cited by 50
Control of muscle fibre size: a crucial factor in ageing.
Hughes, S. M., & Schiaffino, S. (1999) · PubMed · doi:10.1046/j.1365-201x.1999.00622.x · Cited by 50
Malatesta, M., Perdoni, F., Muller, S., Zancanaro, C., & Pellicciari, C. (2009) · European Journal of Histochemistry · doi:10.4081/ejh.2009.e12 · Cited by 48
Multi‐photon excitation microscopy in intact animals
Rothstein, E. C., NAUMAN, M., Chesnick, S., & Balaban, R. S. (2006) · Journal of Microscopy · doi:10.1111/j.1365-2818.2006.01570.x · Cited by 47
Vellas, B. J., Pahor, M., Manini, T. M., Rooks, D., Guralnik, J. M., Morley, J. E., Studenski, S. A., Evans, W. J., Asbrand, C., Fariello, R. G., et al. (2013) · The journal of nutrition health & aging · doi:10.1007/s12603-013-0362-7 · Cited by 46
Villareal, D. T. (2004) · Age and Ageing · doi:10.1093/ageing/afh044 · Cited by 44
Trip, J., Pillen, S., Faber, C. G., van Engelen, B. G. M., Zwarts, M. J., & Drost, G. (2009) · Neuromuscular Disorders · doi:10.1016/j.nmd.2009.06.369 · Cited by 44
Luther, P. K., Padrón, R., Ritter, S., Craig, R. W., & Squire, J. M. (2003) · Journal of Molecular Biology · doi:10.1016/s0022-2836(03)00883-0 · Cited by 43
Observations on the number of nuclei within the fibres of some red and white muscles
Burleigh, I. G. (1977) · Journal of Cell Science · doi:10.1242/jcs.23.1.269 · Cited by 43
Nordal, H. J., Dietrichson, P., Eldevik, P., & Grønseth, K. (1988) · Acta Neurologica Scandinavica · doi:10.1111/j.1600-0404.1988.tb05881.x · Cited by 42
Myogenesis of avian striated muscle in vitro: role of collagen in myofiber formation.
Haba, G. D. L., Kamali, H. M., & Tiede, D. M. (1975) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.72.7.2729 · Cited by 42
Gaweł, M., & Kostera‐Pruszczyk, A. (2014) · Journal of Clinical Neurophysiology · doi:10.1097/wnp.0000000000000066 · Cited by 40
Update on emerging drugs for sarcopenia – age-related muscle wasting
Lynch, G. S. (2008) · Expert Opinion on Emerging Drugs · doi:10.1517/14728210802544476 · Cited by 36
Muscle biopsy and muscle fiber hypercontraction: a brief review
Roth, S. M., Martel, G. F., & Rogers, M. A. (2000) · European Journal of Applied Physiology · doi:10.1007/s004210000287 · Cited by 36
Exercise training effects on skeletal muscle plasticity and IGF-1 receptors in frail elders
Urso, M. L., Singh, M. A. F., Ding, W., Evans, W. J., Cosmas, A. C., & Manfredi, T. G. (2005) · AGE · doi:10.1007/s11357-005-1629-7 · Cited by 36
ACE inhibitors for sarcopenia--as good as exercise training?
Witham, M. D., Sumukadas, D., & McMurdo, M. E. T. (2008) · Age and Ageing · doi:10.1093/ageing/afn124 · Cited by 36
Sarcomere lengths in human extensor carpi radialis brevis measured by microendoscopy
Cromie, M. J., Sanchez, G. N., Schnitzer, M. J., & Delp, S. L. (2012) · Muscle & Nerve · doi:10.1002/mus.23760 · Cited by 36
Yamauchi, J., Mishima, C., Nakayama, S., & Ishii, N. (2009) · Gerontology · doi:10.1159/000235814 · Cited by 34
Delbono, O. (2000) · PubMed · Cited by 32
Lee, E.-J., de Winter, J. M., Buck, D. E., Jasper, J. R., Malik, F. I., Labeit, S., Ottenheijm, C. A. C., & Granzier, H. L. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0055861 · Cited by 32
SALLINEN, J. M., Ojanen, T., Karavirta, L., Ahtiainen, J. P., & Häkkinen, K. (2008) · PubMed · Cited by 31
Considerations in the Development of Drugs to Treat Sarcopenia
Brass, E. P., & Sietsema, K. E. (2011) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2010.03285.x · Cited by 31
Malatesta, M., Perdoni, F., Muller, S., Zancanaro, C., & Pellicciari, C. (2009) · European Journal of Histochemistry · doi:10.4081/ejh.2009.106 · Cited by 28
Use of a single-mode fiber coupler for second-harmonic-generation microscopy
Fu, L., Gan, X. S., & Gu, M. (2005) · Optics Letters · doi:10.1364/ol.30.000385 · Cited by 27
Inactivation of myosin heavy chain genes in the mouse: Diverse and unexpected phenotypes
Allen, D. L., Harrison, B. C., & Leinwand, L. A. (2000) · Microscopy Research and Technique · doi:10.1002/1097-0029(20000915)50:6 · Cited by 26
Ramamurthy, B., & Larsson, L. (2013) · Biogerontology · doi:10.1007/s10522-013-9430-y · Cited by 26
Phillips, S. K., WOLEDGE, R. C., Bruce, S., Young, A., Levy, D., Yeo, A.-L., & Martin, F. C. (1998) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.1998.tb02756.x · Cited by 25
Quantitative evaluation of skeletal muscle defects in second harmonic generation images
Liu, W., Ralston, E., & Raben, N. (2013) · Journal of Biomedical Optics · doi:10.1117/1.jbo.18.2.026005 · Cited by 25
Transposed firing activation of motor units
Luca, C. J. D., Kline, J. C., & Contessa, P. (2014) · Journal of Neurophysiology · doi:10.1152/jn.00619.2013 · Cited by 22
Nass, R. M. (2013) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2013.02.001 · Cited by 16
A novel quantitative morphometry approach to assess regeneration in dystrophic skeletal muscle
Buttgereit, A., Weber, C., & Friedrich, O. (2014) · Neuromuscular Disorders · doi:10.1016/j.nmd.2014.04.011 · Cited by 16
Stereological analysis of the number of nuclei in skeletal muscle fibres
Atherton, G. W., & James, N. T. (1980) · Cells Tissues Organs · doi:10.1159/000145248 · Cited by 15
Miljkovic, I., Cauley, J. A., Dressen, A., Gordon, C. L., Goodpaster, B. H., Kuller, L. H., Bunker, C. H., Patrick, A. L., Wheeler, V. W., ORWOLL, E. S., et al. (2011) · Metabolism · doi:10.1016/j.metabol.2010.12.014 · Cited by 9
Research works printed but not linked: 3
- Lynch NA, Metter EJ, Lindle RS, et al. Muscle quality. I. Age-associated differences between arm and leg muscle groups. J Appl Physiol. 1999;86(1):188–94. · DOI
- Kraemer WJ, Hakkinen K, Newton RU, et al. Effects of heavy-resistance training on hormonal response patterns in younger vs. older men. J Appl Physiol (1985). 1999;87(3):982–92. · DOI
- Goodpaster BH, Chomentowski P, Ward BK, et al. Effects of physical activity on strength and skeletal muscle fat infiltration in older adults: a randomized controlled trial. J Appl Physiol (1985). 2008;105(5):1498–503. · DOI · Paper page
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Self-citationBrook, M. S., Wilkinson, D. J., Mitchell, W. K., Lund, J. N., Phillips, B. E., Szewczyk, N. J., Greenhaff, P. L., Smith, K., & Atherton, P. J. (2016) · The Journal of Physiology · doi:10.1113/jp272857 · Cited by 204
Stock, M. S., & Thompson, B. J. (2020) · European Journal of Applied Physiology · doi:10.1007/s00421-020-04556-6 · Cited by 203
Sarcopenia: a chronic complication of type 2 diabetes mellitus
Trierweiler, H., Kisielewicz, G., Jonasson, T. H., Petterle, R. R., Moreira, C. A., & Borba, V. Z. C. (2018) · Diabetology & Metabolic Syndrome · doi:10.1186/s13098-018-0326-5 · Cited by 174
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Metadata
- Authors
- Fragala, M. S., Kenny, A. M., & Kuchel, G. A.
- Affiliations
- University of Central Florida (US)
- University of Connecticut (US)
- Corresponding author
- Fragala, Maren S.
- Venue
- Sports Medicine
- Published
- 2015-02-06
- Volume
- 45
- Issue
- 5
- Pages
- 641-658
- ISSN
- 0112-1642 (ISSN-L)
- 1179-2035
- OpenAlex
- W1989017729
- Cited by
- 246
- References
- 275
- Citations by year
- 2026: 19 · 2025: 28 · 2024: 27 · 2023: 31 · 2022: 31 · 2021: 33 · 2020: 19 · 2019: 11 · 2018: 24 · 2017: 11 · 2016: 8 · 2015: 4
- FWCI
- 1.92
- Type
- journal article
- Language
- en
- Open access
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Sports Medicine (publishedVersion)
- PubMed (publishedVersion)
- Journal of International Crisis and Risk Communication Research (submittedVersion)
- Topics
- Health Sciences › Medicine › Physiology (medical) › Nutrition and Health in Aging
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Nursing › Nutrition and Dietetics › Muscle metabolism and nutrition
- Keywords
- muscle quality, aging, sarcopenia, skeletal muscle, muscle architecture, muscle quality index, circulating biomarkers, elderly exercise, muscle function, structure-function relationship
- MeSH terms
- Aging, Body Composition, Humans, Motor Activity, Gonadal Steroid Hormones, Ultrasonography, Biomarkers, Exercise, Muscle, Skeletal, Dietary Supplements, Muscle Strength, Sarcopenia
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