Sarcopenia, dynapenia, and the impact of advancing age on human skeletal muscle size and strength; a quantitative review

W Kyle Mitchell, John Williams, Philip Atherton, Mike Larvin, John Lund, Marco Narici, W Kyle Mitchell, John Williams, Philip Atherton, Mike Larvin, John Lund, Marco Narici

Abstract

Changing demographics make it ever more important to understand the modifiable risk factors for disability and loss of independence with advancing age. For more than two decades there has been increasing interest in the role of sarcopenia, the age-related loss of muscle or lean mass, in curtailing active and healthy aging. There is now evidence to suggest that lack of strength, or dynapenia, is a more constant factor in compromised wellbeing in old age and it is apparent that the decline in muscle mass and the decline in strength can take quite different trajectories. This demands recognition of the concept of muscle quality; that is the force generating per capacity per unit cross-sectional area (CSA). An understanding of the impact of aging on skeletal muscle will require attention to both the changes in muscle size and the changes in muscle quality. The aim of this review is to present current knowledge of the decline in human muscle mass and strength with advancing age and the associated risk to health and survival and to review the underlying changes in muscle characteristics and the etiology of sarcopenia. Cross-sectional studies comparing young (18-45 years) and old (>65 years) samples show dramatic variation based on the technique used and population studied. The median of values of rate of loss reported across studies is 0.47% per year in men and 0.37% per year in women. Longitudinal studies show that in people aged 75 years, muscle mass is lost at a rate of 0.64-0.70% per year in women and 0.80-00.98% per year in men. Strength is lost more rapidly. Longitudinal studies show that at age 75 years, strength is lost at a rate of 3-4% per year in men and 2.5-3% per year in women. Studies that assessed changes in mass and strength in the same sample report a loss of strength 2-5 times faster than loss of mass. Loss of strength is a more consistent risk for disability and death than is loss of muscle mass.

Keywords: aging; dynapenia; muscle aging; muscle atrophy; muscle quality; sarcopenia; skeletal muscle; strength.

Figures

Figure 1
Figure 1
Muscle mass in 1280 females aged 18–80 years, measured by DXA. With permission Z. M. Wang and A. M. Silva, adapted from Silva et al. (2009).

References

    1. Al Snih S., Markides K. S., Ottenbacher K. J., Raji M. A. (2004). Hand Grip strength and incident ADL disability in elderly Mexican Americans over a seven-year period. Aging Clin. Exp. Res. 16, 481–486
    1. Aloia J. F., Mcgowan D. M., Vaswani A. N., Ross P., Cohn S. H. (1991). Relationship of menopause to skeletal and muscle mass. Am. J. Clin. Nutr. 53, 1378–1383
    1. Andersen J. L. (2003). Muscle fibre type adaptation in the elderly human muscle. Scand. J. Med. Sci. Sports 13, 40–4710.1034/j.1600-0838.2003.00299.x
    1. Avin K. G., Law L. A. (2011). Age-related differences in muscle fatigue vary by contraction type: a meta-analysis. Phys. Ther. 91, 1153–116510.2522/ptj.20100333
    1. Bajekal M., Wheeler L., Dix D. (2006) Estimating residents and staff in communal establishments from the 2001 census. Health Stat. Q. 31, 42–50
    1. Barreiro E., Coronell C., Lavina B., Ramirez-Sarmiento A., Orozco-Levi M., Gea J. (2006). Aging, sex differences, and oxidative stress in human respiratory and limb muscles. Free Radic. Biol. Med. 41, 797–80910.1016/j.freeradbiomed.2006.05.027
    1. Baumgartner R. N., Koehler K. M., Gallagher D., Romero L., Heymsfield S. B., Ross R. R., Garry P. J., Lindeman R. D. (1998). Epidemiology of sarcopenia among the elderly in New Mexico. Am. J. Epidemiol. 147, 755–76310.1093/oxfordjournals.aje.a009520
    1. Baumgartner R. N., Stauber P. M., Mchugh D., Koehler K. M., Garry P. J. (1995). Cross-sectional age differences in body composition in persons 60+ years of age. J. Gerontol. A Biol. Sci. Med. Sci. 50, M307–M31610.1093/gerona/50A.6.M307
    1. Bautmans I., Njemini R., Lambert M., Demanet C., Mets T. (2005). Circulating acute phase mediators and skeletal muscle performance in hospitalized geriatric patients. J. Gerontol. A Biol. Sci. Med. Sci. 60, 361–36710.1093/gerona/60.3.361
    1. Bigland-Ritchie B., Woods J. J. (1984). Changes in muscle contractile properties and neural control during human muscular fatigue. Muscle Nerve 7, 691–69910.1002/mus.880070902
    1. Borkan G. A., Hults D. E., Gerzof S. G., Robbins A. H., Silbert C. K. (1983). Age changes in body composition revealed by computed tomography. J. Gerontol. 38, 673–677
    1. Brown W. F. (1972). A method for estimating the number of motor units in thenar muscles and the changes in motor unit count with ageing. J. Neurol. Neurosurg. Psychiatr. 35, 845–85210.1136/jnnp.35.6.845
    1. Campbell M. J., Mccomas A. J., Petito F. (1973). Physiological changes in ageing muscles. J. Neurol. Neurosurg. Psychiatr. 36, 174–18210.1136/jnnp.36.2.174
    1. Cappola A. R., Xue Q. L., Ferrucci L., Guralnik J. M., Volpato S., Fried L. P. (2003). Insulin-like growth factor I and interleukin-6 contribute synergistically to disability and mortality in older women. J. Clin. Endocrinol. Metab. 88, 2019–202510.1210/jc.2003-030398
    1. Carmelli D., Reed T. (2000). Stability and change in genetic and environmental influences on hand-grip strength in older male twins. J. Appl. Physiol. 89, 1879–1883
    1. Casson P. R., Santoro N., Elkind-Hirsch K., Carson S. A., Hornsby P. J., Abraham G., Buster J. E. (1998). Postmenopausal dehydroepiandrosterone administration increases free insulin-like growth factor-I and decreases high-density lipoprotein: a six-month trial. Fertil. Steril. 70, 107–11010.1016/S0015-0282(98)00121-6
    1. Castaneda C., Charnley J. M., Evans W. J., Crim M. C. (1995). Elderly women accommodate to a low-protein diet with losses of body cell mass, muscle function, and immune response. Am. J. Clin. Nutr. 62, 30–39
    1. Cawthon P. M., Fox K. M., Gandra S. R., Delmonico M. J., Chiou C. F., Anthony M. S., Sewall A., Goodpaster B., Satterfield S., Cummings S. R., Harris T. B. (2009). Do muscle mass, muscle density, strength, and physical function similarly influence risk of hospitalization in older adults? J. Am. Geriatr. Soc. 57, 1411–141910.1111/j.1532-5415.2009.02366.x
    1. Chien M. Y., Huang T. Y., Wu Y. T. (2008). Prevalence of sarcopenia estimated using a bioelectrical impedance analysis prediction equation in community-dwelling elderly people in Taiwan. J. Am. Geriatr. Soc. 56, 1710–171510.1111/j.1532-5415.2008.01854.x
    1. Clark B. C., Manini T. M. (2008). Sarcopenia =/= dynapenia. J. Gerontol. A Biol. Sci. Med. Sci. 63, 829–83410.1093/gerona/63.8.829
    1. Clark B. C., Manini T. M. (2010). Functional consequences of sarcopenia and dynapenia in the elderly. Curr. Opin. Clin. Nutr. Metab. Care 13, 271–27610.1097/MCO.0b013e328337819e
    1. Clement F. J. (1974). Longitudinal and cross-sectional assessments of age changes in physical strength as related to sex, social class, and mental ability. J. Gerontol. 29, 423–429
    1. Coggan A. R., Spina R. J., King D. S., Rogers M. A., Brown M., Nemeth P. M., Holloszy J. O. (1992). Histochemical and enzymatic comparison of the gastrocnemius muscle of young and elderly men and women. J. Gerontol. 47, B71–B76
    1. Coggan A. R., Spina R. J., Rogers M. A., King D. S., Brown M., Nemeth P. M., Holloszy J. O. (1990). Histochemical and enzymatic characteristics of skeletal muscle in master athletes. J. Appl. Physiol. 68, 1896–190110.1063/1.346579
    1. Cohn S. H., Vartsky D., Yasumura S., Sawitsky A., Zanzi I., Vaswani A., Ellis K. J. (1980). Compartmental body composition based on total-body nitrogen, potassium, and calcium. Am. J. Physiol. 239, E524–E530
    1. Cristea A., Qaisar R., Edlund P. K., Lindblad J., Bengtsson E., Larsson L. (2010). Effects of aging and gender on the spatial organization of nuclei in single human skeletal muscle cells. Aging Cell 9, 685–69710.1111/j.1474-9726.2010.00594.x
    1. Cruz-Jentoft A. J., Baeyens J. P., Bauer J. M., Boirie Y., Cederholm T., Landi F., Martin F. C., Michel J. P., Rolland Y., Schneider S. M., Topinkova E., Vandewoude M., Zamboni M. (2010). Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing 39, 412–42310.1093/ageing/afq034
    1. Cuthbertson D., Smith K., Babraj J., Leese G., Waddell T., Atherton P., Wackerhage H., Taylor P. M., Rennie M. J. (2005). Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J. 19, 422–424
    1. D’Antona G., Pellegrino M. A., Adami R., Rossi R., Carlizzi C. N., Canepari M., Saltin B., Bottinelli R. (2003). The effect of ageing and immobilization on structure and function of human skeletal muscle fibres. J. Physiol. (Lond.) 552, 499–51110.1113/jphysiol.2003.046276
    1. Davies Re C. N., Gergely J. (2012). Encyclopedia Britannica Online Academic Edition. Available at:
    1. De Benedetti F., Alonzi T., Moretta A., Lazzaro D., Costa P., Poli V., Martini A., Ciliberto G., Fattori E. (1997). Interleukin 6 causes growth impairment in transgenic mice through a decrease in insulin-like growth factor-I. A model for stunted growth in children with chronic inflammation. J. Clin. Invest. 99, 643–65010.1172/JCI119207
    1. Delbono O., O’Rourke K. S., Ettinger W. H. (1995). Excitation-calcium release uncoupling in aged single human skeletal muscle fibers. J. Membr. Biol. 148, 211–222
    1. Delmonico M. J., Harris T. B., Lee J. S., Visser M., Nevitt M., Kritchevsky S. B., Tylavsky F. A., Newman A. B. (2007). Alternative definitions of sarcopenia, lower extremity performance, and functional impairment with aging in older men and women. J. Am. Geriatr. Soc. 55, 769–77410.1111/j.1532-5415.2007.01140.x
    1. Delmonico M. J., Harris T. B., Visser M., Park S. W., Conroy M. B., Velasquez-Mieyer P., Boudreau R., Manini T. M., Nevitt M., Newman A. B., Goodpaster B. H. (2009). Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am. J. Clin. Nutr. 90, 1579–158510.3945/ajcn.2009.28047
    1. Dey D. K., Bosaeus I., Lissner L., Steen B. (2009). Changes in body composition and its relation to muscle strength in 75-year-old men and women: a 5-year prospective follow-up study of the NORA cohort in Goteborg, Sweden. Nutrition 25, 613–61910.1016/j.nut.2008.11.023
    1. Doherty T. J. (2003). Invited review: aging and sarcopenia. J. Appl. Physiol. 95, 1717–1727
    1. Doherty T. J., Vandervoort A. A., Taylor A. W., Brown W. F. (1993). Effects of motor unit losses on strength in older men and women. J. Appl. Physiol. 74, 868–87410.1063/1.354879
    1. Douchi T., Yamamoto S., Yoshimitsu N., Andoh T., Matsuo T., Nagata Y. (2002). Relative contribution of aging and menopause to changes in lean and fat mass in segmental regions. Maturitas 42, 301–30610.1016/S0378-5122(02)00004-X
    1. Einsiedel L. J., Luff A. R. (1992). Effect of partial denervation on motor units in the ageing rat medial gastrocnemius. J. Neurol. Sci. 112, 178–18410.1016/0022-510X(92)90148-E
    1. Evans W. J. (1995). What is sarcopenia? J. Gerontol. A Biol. Sci. Med. Sci. 50, 5–810.1093/gerona/50A.Special_Issue.5
    1. Evans W. J., Campbell W. W. (1993). Sarcopenia and age-related changes in body composition and functional capacity. J. Nutr. 123, 465–468
    1. Evans W. J., Cyr-Campbell D. (1997). Nutrition, exercise, and healthy aging. J. Am. Diet. Assoc. 97, 632–63810.1016/S0002-8223(97)00160-0
    1. Fischer M., Birren J. (1946). Standardization, of a test of hand strength. J. Appl. Psychol. 30, 380–38710.1037/h0059969
    1. Flynn M. A., Weaver-Osterholtz D., Sharpe-Timms K. L., Allen S., Krause G. (1999). Dehydroepiandrosterone replacement in aging humans. J. Clin. Endocrinol. Metab. 84, 1527–153310.1210/jc.84.5.1527
    1. Frey Law L. A., Avin K. G. (2010). Endurance time is joint-specific: a modelling and meta-analysis investigation. Ergonomics 53, 109–12910.1080/00140130903389068
    1. Frontera W. R., Hughes V. A., Fielding R. A., Fiatarone M. A., Evans W. J., Roubenoff R. (2000). Aging of skeletal muscle: a 12-yr longitudinal study. J. Appl. Physiol. 88, 1321–1326
    1. Frontera W. R., Hughes V. A., Lutz K. J., Evans W. J. (1991). A cross-sectional study of muscle strength and mass in 45- to 78-yr-old men and women. J. Appl. Physiol. 71, 644–650
    1. Frontera W. R., Meredith C. N., O’Reilly K. P., Evans W. J. (1990). Strength training and determinants of VO2max in older men. J. Appl. Physiol. 68, 329–333
    1. Galea V. (1996). Changes in motor unit estimates with aging. J. Clin. Neurophysiol. 13, 253–26010.1097/00004691-199605000-00010
    1. Gallagher D., Visser M., De Meersman R. E., Sepulveda D., Baumgartner R. N., Pierson R. N., Harris T., Heymsfield S. B. (1997). Appendicular skeletal muscle mass: effects of age, gender, and ethnicity. J. Appl. Physiol. 83, 229–239
    1. Ganong W. F. (2005). Review of Medical Physiology. San Francisco: McGraw Hill
    1. Garatachea N., Lucia A. (2011). Genes and the ageing muscle: a review on genetic association studies. Age (Dordr.). [Epub ahead of print].
    1. Gelfi C., Vigano A., Ripamonti M., Pontoglio A., Begum S., Pellegrino M. A., Grassi B., Bottinelli R., Wait R., Cerretelli P. (2006). The human muscle proteome in aging. J. Proteome Res. 5, 1344–135310.1021/pr050414x
    1. Giresi P. G., Stevenson E. J., Theilhaber J., Koncarevic A., Parkington J., Fielding R. A., Kandarian S. C. (2005). Identification of a molecular signature of sarcopenia. Physiol. Genomics 21, 253–26310.1152/physiolgenomics.00249.2004
    1. Goldspink G. (1985). Malleability of the motor system: a comparative approach. J. Exp. Biol. 115, 375–391
    1. Gonzalez-Freire M., Rodriguez-Romo G., Santiago C., Bustamante-Ara N., Yvert T., Gomez-Gallego F., Serra Rexach J. A., Ruiz J. R., Lucia A. (2010). The K153R variant in the myostatin gene and sarcopenia at the end of the human lifespan. Age (Dordr.) 32, 405–40910.1007/s11357-010-9139-7
    1. Goodpaster B. H., Park S. W., Harris T. B., Kritchevsky S. B., Nevitt M., Schwartz A. V., Simonsick E. M., Tylavsky F. A., Visser M., Newman A. B. (2006). The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J. Gerontol. A Biol. Sci. Med. Sci. 61, 1059–106410.1093/gerona/61.10.1059
    1. Gundersen K., Bruusgaard J. C. (2008). Nuclear domains during muscle atrophy: nuclei lost or paradigm lost? J. Physiol. (Lond.) 586, 2675–268110.1113/jphysiol.2008.154369
    1. Guyton A. C. (1991). Medical Physiology. Philadelphia: W.B. Saunders
    1. Hall Z. W., Ralston E. (1989). Nuclear domains in muscle cells. Cell 59, 771–77210.1016/0092-8674(89)90875-1
    1. Harber M. P., Crane J. D., Dickinson J. M., Jemiolo B., Raue U., Trappe T. A., Trappe S. W. (2009). Protein synthesis and the expression of growth-related genes are altered by running in human vastus lateralis and soleus muscles. Am. J. Physiol. Regul. Integr. Comp. Physiol. 296, R708–R71410.1152/ajpregu.90906.2008
    1. Haren M. T., Banks W. A., Perry Iii H. M., Patrick P., Malmstrom T. K., Miller D. K., Morley J. E. (2008). Predictors of serum testosterone and dheas in African-American men. Int. J. Androl. 31, 50–59
    1. Hiona A., Leeuwenburgh C. (2008). The role of mitochondrial DNA mutations in aging and sarcopenia: implications for the mitochondrial vicious cycle theory of aging. Exp. Gerontol. 43, 24–3310.1016/j.exger.2007.10.001
    1. Hook P., Sriramoju V., Larsson L. (2001). Effects of aging on actin sliding speed on myosin from single skeletal muscle cells of mice, rats, and humans. Am. J. Physiol. Cell Physiol. 280, C782–C788
    1. Howard C., Ferrucci L., Sun K., Fried L. P., Walston J., Varadhan R., Guralnik J. M., Semba R. D. (2007). Oxidative protein damage is associated with poor grip strength among older women living in the community. J. Appl. Physiol. 103, 17–2010.1152/japplphysiol.00133.2007
    1. Hughes V. A., Frontera W. R., Roubenoff R., Evans W. J., Singh M. A. (2002). Longitudinal changes in body composition in older men and women: role of body weight change and physical activity. Am. J. Clin. Nutr. 76, 473–481
    1. Huygens W., Thomis M. A., Peeters M. W., Vlietinck R. F., Beunen G. P. (2004). Determinants and upper-limit heritabilities of skeletal muscle mass and strength. Can. J. Appl. Physiol. 29, 186–20010.1139/h04-014
    1. Iannuzzi-Sucich M., Prestwood K. M., Kenny A. M. (2002). Prevalence of sarcopenia and predictors of skeletal muscle mass in healthy, older men and women. J. Gerontol. A Biol. Sci. Med. Sci. 57, M772–M77710.1093/gerona/57.12.M772
    1. Inouye S. K., Studenski S., Tinetti M. E., Kuchel G. A. (2007). Geriatric syndromes: clinical, research, and policy implications of a core geriatric concept. J. Am. Geriatr. Soc. 55, 780–79110.1111/j.1532-5415.2007.01443.x
    1. Izquierdo M., Ibanez J., Gorostiaga E., Garrues M., Zuniga A., Anton A., Larrion J. L., Hakkinen K. (1999). Maximal strength and power characteristics in isometric and dynamic actions of the upper and lower extremities in middle-aged and older men. Acta Physiol. Scand. 167, 57–6810.1046/j.1365-201x.1999.00590.x
    1. Janssen I., Heymsfield S. B., Ross R. (2002). Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J. Am. Geriatr. Soc. 50, 889–89610.1046/j.1532-5415.2002.50216.x
    1. Janssen I., Heymsfield S. B., Wang Z. M., Ross R. (2000). Skeletal muscle mass and distribution in 468 men and women aged 18–88 yr. J. Appl. Physiol. 89, 81–88
    1. Kadi F., Charifi N., Denis C., Lexell J. (2004). Satellite cells and myonuclei in young and elderly women and men. Muscle Nerve 29, 120–12710.1002/mus.10510
    1. Kanis J. A. (1994). Assessment of fracture risk and its application to screening for postmenopausal osteoporosis: synopsis of a WHO report. WHO Study Group. Osteoporos. Int. 4, 368–38110.1007/BF01622200
    1. Kehayias J. J., Fiatarone M. A., Zhuang H., Roubenoff R. (1997). Total body potassium and body fat: relevance to aging. Am. J. Clin. Nutr. 66, 904–910
    1. Klass M., Baudry S., Duchateau J. (2005). Aging does not affect voluntary activation of the ankle dorsiflexors during isometric, concentric, and eccentric contractions. J. Appl. Physiol. 99, 31–3810.1152/japplphysiol.01426.2004
    1. Klitgaard H., Zhou M., Schiaffino S., Betto R., Salviati G., Saltin B. (1990). Ageing alters the myosin heavy chain composition of single fibres from human skeletal muscle. Acta Physiol. Scand. 140, 55–6210.1111/j.1748-1716.1990.tb08975.x
    1. Koster A., Ding J., Stenholm S., Caserotti P., Houston D. K., Nicklas B. J., You T., Lee J. S., Visser M., Newman A. B., Schwartz A. V., Cauley J. A., Tylavsky F. A., Goodpaster B. H., Kritchevsky S. B., Harris T. B. (2011). Does the amount of fat mass predict age-related loss of lean mass, muscle strength, and muscle quality in older adults? J. Gerontol. A Biol. Sci. Med. Sci. 66, 888–89510.1093/gerona/glr070
    1. Kumar V., Selby A., Rankin D., Patel R., Atherton P., Hildebrandt W., Williams J., Smith K., Seynnes O., Hiscock N., Rennie M. J. (2009). Age-related differences in the dose-response relationship of muscle protein synthesis to resistance exercise in young and old men. J. Physiol. (Lond.) 587, 211–21710.1113/jphysiol.2008.164483
    1. Kyle U. G., Genton L., Hans D., Karsegard L., Slosman D. O., Pichard C. (2001). Age-related differences in fat-free mass, skeletal muscle, body cell mass and fat mass between 18 and 94 years. Eur. J. Clin. Nutr. 55, 663–67210.1038/sj.ejcn.1601198
    1. Lamberts S. W., Van Den Beld A. W., Van Der Lely A. J. (1997). The endocrinology of aging. Science 278, 419–42410.1126/science.278.5337.419
    1. Landi F., Russo A., Liperoti R., Pahor M., Tosato M., Capoluongo E., Bernabei R., Onder G. (2005). Midarm muscle circumference, physical performance and mortality: results from the aging and longevity study in the Sirente geographic area (ilSIRENTE study). Clin. Nutr. 29, 441–44710.1016/j.clnu.2009.12.006
    1. Larsson L. (1978). Morphological and functional characteristics of the ageing skeletal muscle in man. A cross-sectional study. Acta Physiol. Scand. Suppl. 457, 1–3610.1111/j.1748-1716.1978.tb06041.x
    1. Larsson L. (1995). Motor units: remodeling in aged animals. J. Gerontol. A Biol. Sci. Med. Sci. 50, 91–95
    1. Larsson L., Karlsson J. (1978). Isometric and dynamic endurance as a function of age and skeletal muscle characteristics. Acta Physiol. Scand. 104, 129–13610.1111/j.1748-1716.1978.tb06259.x
    1. Larsson L., Li X., Frontera W. R. (1997). Effects Of aging on shortening velocity and myosin isoform composition in single human skeletal muscle cells. Am. J. Physiol. 272, C638–C649
    1. Laukkanen P., Heikkinen E., Kauppinen M. (1995). Muscle strength and mobility as predictors of survival in 75–84-year-old people. Age Ageing 24, 468–47310.1093/ageing/24.6.468
    1. Leger B., Derave W., De Bock K., Hespel P., Russell A. P. (2008). Human sarcopenia reveals an increase in SOCS-3 and myostatin and a reduced efficiency of Akt phosphorylation. Rejuvenation Res. 11, 163–175b10.1089/rej.2007.0588
    1. Lelbach A., Scharf J. G., Ramadori G. (2001). Regulation of insulin-like growth factor-I and of insulin-like growth factor binding protein-1, -3 and -4 in cocultures of rat hepatocytes and Kupffer cells by interleukin-6. J. Hepatol. 35, 558–56710.1016/S0168-8278(01)00170-2
    1. Lexell J., Downham D. Y. (1991). The occurrence of fibre-type grouping in healthy human muscle: a quantitative study of cross-sections of whole vastus lateralis from men between 15 and 83 years. Acta Neuropathol. 81, 377–38110.1007/BF00293457
    1. Lexell J., Henriksson-Larsen K., Winblad B., Sjostrom M. (1983). Distribution of different fiber types in human skeletal muscles: effects of aging studied in whole muscle cross sections. Muscle Nerve 6, 588–59510.1002/mus.880060809
    1. Lexell J., Taylor C. C., Sjostrom M. (1988). What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J. Neurol. Sci. 84, 275–29410.1016/0022-510X(88)90132-3
    1. Lieber R. L., Friden J. (2001). Clinical significance of skeletal muscle architecture. Clin. Orthop. Relat. Res. 140–15110.1097/00003086-200102000-00016
    1. Ling C. H., Taekema D., De Craen A. J., Gussekloo J., Westendorp R. G., Maier A. B. (2010). Handgrip strength and mortality in the oldest old population: the Leiden 85-plus study. CMAJ 182, 429–43510.1503/cmaj.091278
    1. Liu C. J., Latham N. K. (2009). Progressive resistance strength training for improving physical function in older adults. Cochrane Database Syst. Rev. 3, CD002759.
    1. Loos R., Thomis M., Maes H. H., Beunen G., Claessens A. L., Derom C., Legius E., Derom R., Vlietinck R. (1997). Gender-specific regional changes in genetic structure of muscularity in early adolescence. J. Appl. Physiol. 82, 1802–1810
    1. Luff A. R. (1998). Age-associated changes in the innervation of muscle fibers and changes in the mechanical properties of motor units. Ann. N. Y. Acad. Sci. 854, 92–10110.1111/j.1749-6632.1998.tb09895.x
    1. Macaluso A., De Vito G. (2004). Muscle strength, power and adaptations to resistance training in older people. Eur. J. Appl. Physiol. 91, 450–47210.1007/s00421-003-0991-3
    1. Marx J. O., Kraemer W. J., Nindl B. C., Larsson L. (2002). Effects Of aging on human skeletal muscle myosin heavy-chain mRNA content and protein isoform expression. J. Gerontol. A Biol. Sci. Med. Sci. 57, B232–B23810.1093/gerona/57.6.B232
    1. Meltzer D. E. (1994). Age dependence of Olympic weightlifting ability. Med. Sci. Sports Exerc. 26, 1053–1067
    1. Metter E. J., Talbot L. A., Schrager M., Conwit R. (2002). Skeletal muscle strength as a predictor of all-cause mortality in healthy men. J. Gerontol. A Biol. Sci. Med. Sci. 57, B359–B36510.1093/gerona/57.10.B359
    1. Moore D. H., II. (1975). A study of age group track and field records to relate age and running speed. Nature 253, 264–26510.1038/253525b0
    1. Morley J. E. (1997). Anorexia of aging: physiologic and pathologic. Am. J. Clin. Nutr. 66, 760–773
    1. Morley J. E., Baumgartner R. N., Roubenoff R., Mayer J., Nair K. S. (2001). Sarcopenia. J. Lab. Clin. Med. 137, 231–24310.1067/mlc.2001.113504
    1. Morse C. I., Thom J. M., Mian O. S., Muirhead A., Birch K. M., Narici M. V. (2005). Muscle strength, volume and activation following 12-month resistance training in 70-year-old males. Eur. J. Appl. Physiol. 95, 197–20410.1007/s00421-005-1342-3
    1. Muller-Delp J. M., Spier S. A., Ramsey M. W., Delp M. D. (2002). Aging impairs endothelium-dependent vasodilatation in rat skeletal muscle arterioles. Am. J. Physiol. Heart Circ. Physiol. 283, H1662–H1672
    1. Narici M. V., Maffulli N. (2010). Sarcopenia: characteristics, mechanisms and functional significance. Br. Med. Bull. 95, 139–15910.1093/bmb/ldq008
    1. Narici M. V., Maganaris C. N. (2007). Plasticity of the muscle-tendon complex with disuse and aging. Exerc. Sport Sci. Rev. 35, 126–134
    1. Narici M. V., Maganaris C. N., Reeves N. D., Capodaglio P. (2003). Effect of aging on human muscle architecture. J. Appl. Physiol. 95, 2229–2234
    1. National Institutes of Health N. (2004). Exercise: A Guide from the National Institute on Aging. Bethesda: U.S. Department of Health and Human Services
    1. Newman A. B., Kupelian V., Visser M., Simonsick E. M., Goodpaster B. H., Kritchevsky S. B., Tylavsky F. A., Rubin S. M., Harris T. B. (2006). Strength, but not muscle mass, is associated with mortality in the health, aging and body composition study cohort. J. Gerontol. A Biol. Sci. Med. Sci. 61, 72–7710.1093/gerona/61.1.72
    1. Novak L. P. (1972). Aging, total body potassium, fat-free mass, and cell mass in males and females between ages 18 and 85 years. J. Gerontol. 27, 438–443
    1. Nygaard E., Sanchez J. (1982). Intramuscular variation of fiber types in the brachial biceps and the lateral vastus muscles of elderly men: how representative is a small biopsy sample? Anat. Rec. 203, 451–45910.1002/ar.1092030404
    1. Office of Fair Trading O. (2005). Care Homes for Older People in the UK – A Market Study. OFT780, OFT780. Available at:
    1. Ojanen T., Rauhala T., Hakkinen K. (2007). Strength and power profiles of the lower and upper extremities in master throwers at different ages. J. Strength Cond. Res. 21, 216–22210.1519/00124278-200702000-00039
    1. Peake J., Della Gatta P., Cameron-Smith D. (2010). Aging and its effects on inflammation in skeletal muscle at rest and following exercise-induced muscle injury. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298, R1485–R149510.1152/ajpregu.00467.2009
    1. Pedersen M., Bruunsgaard H., Weis N., Hendel H. W., Andreassen B. U., Eldrup E., Dela F., Pedersen B. K. (2003). Circulating levels of TNF-alpha and IL-6-relation to truncal fat mass and muscle mass in healthy elderly individuals and in patients with type-2 diabetes. Mech. Ageing Dev. 124, 495–50210.1016/S0047-6374(03)00027-7
    1. Percheron G., Hogrel J. Y., Denot-Ledunois S., Fayet G., Forette F., Baulieu E. E., Fardeau M., Marini J. F. (2003). Effect of 1-year oral administration of dehydroepiandrosterone to 60- to 80-year-old individuals on muscle function and cross-sectional area: a double-blind placebo-controlled trial. Arch. Intern. Med. 163, 720–72710.1001/archinte.163.6.720
    1. Phillips S. K., Woledge R. C., Bruce S. A., Young A., Levy D., Yeo A., Martin F. C. (1998). A study of force and cross-sectional area of adductor pollicis muscle in female hip fracture patients. J. Am. Geriatr. Soc. 46, 999–1002
    1. Porter M. M., Vandervoort A. A., Kramer J. F. (1997). Eccentric peak torque of the plantar and dorsiflexors is maintained in older women. J. Gerontol. A Biol. Sci. Med. Sci. 52, B125–B13110.1093/gerona/52A.2.B125
    1. Pousson M., Lepers R., Van Hoecke J. (2001). Changes in isokinetic torque and muscular activity of elbow flexors muscles with age. Exp. Gerontol. 36, 1687–169810.1016/S0531-5565(01)00143-7
    1. Power G. A., Dalton B. H., Behm D. G., Doherty T. J., Vandervoort A. A., Rice C. L. (2012). Motor unit survival in life-long runners is muscle-dependent. Med. Sci. Sports Exerc. 44, 1235–1242
    1. Prior S. J., Roth S. M., Wang X., Kammerer C., Miljkovic-Gacic I., Bunker C. H., Wheeler V. W., Patrick A. L., Zmuda J. M. (2007). Genetic and environmental influences on skeletal muscle phenotypes as a function of age and sex in large, multigenerational families of African heritage. J. Appl. Physiol. 103, 1121–112710.1152/japplphysiol.00120.2007
    1. Proctor D. N., Shen P. H., Dietz N. M., Eickhoff T. J., Lawler L. A., Ebersold E. J., Loeffler D. L., Joyner M. J. (1998). Reduced leg blood flow during dynamic exercise in older endurance-trained men. J. Appl. Physiol. 85, 68–75
    1. Purves D., Augustine G., Fitzpatrick D., Katz L. C., Lamantia A. S., Mcnamara J. O., Williams S. M. (ed.). (2001). Neurosciences. Sunderland, MA: Sinauer Associates
    1. Ratkevicius A., Joyson A., Selmer I., Dhanani T., Grierson C., Tommasi A. M., Devries A., Rauchhaus P., Crowther D., Alesci S., Yaworsky P., Gilbert F., Redpath T. W., Brady J., Fearon K. C., Reid D. M., Greig C. A., Wackerhage H. (2011). Serum concentrations of myostatin and myostatin-interacting proteins do not differ between young and sarcopenic elderly men. J. Gerontol. A Biol. Sci. Med. Sci. 66, 620–62610.1093/gerona/glr025
    1. Raue U., Slivka D., Minchev K., Trappe S. (2009). Improvements in whole muscle and myocellular function are limited with high-intensity resistance training in octogenarian women. J. Appl. Physiol. 106, 1611–161710.1152/japplphysiol.91587.2008
    1. Roberts S. B. (1995). Effects of aging on energy requirements and the control of food intake in men. J. Gerontol. A Biol. Sci. Med. Sci. 50, 101–106
    1. Roig M., Macintyre D. L., Eng J. J., Narici M. V., Maganaris C. N., Reid W. D. (2010). Preservation of eccentric strength in older adults: evidence, mechanisms and implications for training and rehabilitation. Exp. Gerontol. 45, 400–40910.1016/j.exger.2010.03.008
    1. Rolland Y., Czerwinski S., Abellan Van Kan G., Morley J. E., Cesari M., Onder G., Woo J., Baumgartner R., Pillard F., Boirie Y., Chumlea W. M., Vellas B. (2008). Sarcopenia: its assessment, etiology, pathogenesis, consequences and future perspectives. J. Nutr. Health Aging 12, 433–45010.1007/BF02982704
    1. Rosenberg I. (1989). Summary comments. Am. J. Clin. Nutr. 50, 1231–1233
    1. Roubenoff R., Harris T. B., Abad L. W., Wilson P. W., Dallal G. E., Dinarello C. A. (1998). Monocyte cytokine production in an elderly population: effect of age and inflammation. J. Gerontol. A Biol. Sci. Med. Sci. 53, M20–M2610.1093/gerona/53A.1.M20
    1. Roubenoff R., Hughes V. A. (2000). Sarcopenia: current concepts. J. Gerontol. A Biol. Sci. Med. Sci. 55, M716–M72410.1093/gerona/55.12.M757
    1. Rudman D., Feller A. G., Nagraj H. S., Gergans G. A., Lalitha P. Y., Goldberg A. F., Schlenker R. A., Cohn L., Rudman I. W., Mattson D. E. (1990). Effects of human growth hormone in men over 60 years old. N. Engl. J. Med. 323, 1–610.1056/NEJM199007053230101
    1. Sayhoun N. (1992). “Nutrient intake by the NSS elderly population,” in Nutrition in the Elderly: The Boston Nutritional Survey, eds Hartz S. R., Russell R. M., Rosenbeerg I. H. (London: Smith-Gordon and Company; ).
    1. Sehl M. E. (2001). Senescence, frailty and mortality: mathematical models of aging. Med. Health RI 84, 360–364
    1. Seibert M. J., Xue Q. L., Fried L. P., Walston J. D. (2001). Polymorphic variation in the human myostatin (GDF-8) gene and association with strength measures in the Women’s Health and Aging Study II cohort. J. Am. Geriatr. Soc. 49, 1093–109610.1046/j.1532-5415.2001.49214.x
    1. Silva A. M., Shen W., Heo M., Gallagher D., Wang Z., Sardinha L. B., Heymsfield S. B. (2009). Ethnicity-related skeletal muscle differences across the lifespan. Am. J. Hum. Biol. 22, 76–8210.1002/ajhb.20956
    1. Siriett V., Platt L., Salerno M. S., Ling N., Kambadur R., Sharma M. (2006). Prolonged absence of myostatin reduces sarcopenia. J. Cell. Physiol. 209, 866–87310.1002/jcp.20778
    1. Sirola J., Kroger H. (2011). Similarities in acquired factors related to postmenopausal osteoporosis and sarcopenia. J. Osteoporos. 2011, 536735.
    1. Skelton D. A., Greig C. A., Davies J. M., Young A. (1994). Strength, power and related functional ability of healthy people aged 65–89 years. Age Ageing 23, 371–37710.1093/ageing/23.5.371
    1. Solerte S. B., Gazzaruso C., Bonacasa R., Rondanelli M., Zamboni M., Basso C., Locatelli E., Schifino N., Giustina A., Fioravanti M. (2008). Nutritional supplements with oral amino acid mixtures increases whole-body lean mass and insulin sensitivity in elderly subjects with sarcopenia. Am. J. Cardiol. 101, 69e–77e10.1016/j.amjcard.2007.07.050
    1. Sweeney H. L., Bowman B. F., Stull J. T. (1993). Myosin light chain phosphorylation in vertebrate striated muscle: regulation and function. Am. J. Physiol. 264, C1085–C1095
    1. Taekema D. G., Gussekloo J., Maier A. B., Westendorp R. G., de Craen A. J. (2010). Handgrip strength as a predictor of functional, psychological and social health. A prospective population-based study among the oldest old. Age Ageing 39, 331–33710.1093/ageing/afq022
    1. Tan L. J., Liu S. L., Lei S. F., Papasian C. J., Deng H. W. (2012). Molecular genetic studies of gene identification for sarcopenia. Hum. Genet. 131, 1–3110.1007/s00439-011-1040-7
    1. Tanko L. B., Movsesyan L., Mouritzen U., Christiansen C., Svendsen O. L. (2002). Appendicular lean tissue mass and the prevalence of sarcopenia among healthy women. Metab. Clin. Exp. 51, 69–7410.1053/meta.2002.28960
    1. Thom J. M., Morse C. I., Birch K. M., Narici M. V. (2007). Influence of muscle architecture on the torque and power-velocity characteristics of young and elderly men. Eur. J. Appl. Physiol. 100, 613–61910.1007/s00421-007-0481-0
    1. Thomas D. R. (2007). Loss of skeletal muscle mass in aging: examining the relationship of starvation, sarcopenia and cachexia. Clin. Nutr. 26, 389–39910.1016/j.clnu.2007.03.008
    1. Tomlinson B. E., Irving D. (1977). The numbers of limb motor neurons in the human lumbosacral cord throughout life. J. Neurol. Sci. 34, 213–21910.1016/0022-510X(77)90069-7
    1. Tomlinson B. E., Walton J. N., Rebeiz J. J. (1969). The effects of ageing and of cachexia upon skeletal muscle. A histopathological study. J. Neurol. Sci. 9, 321–34610.1016/0022-510X(69)90079-3
    1. Tzankoff S. P., Norris A. H. (1977). Effect of muscle mass decrease on age-related BMR changes. J. Appl. Physiol. 43, 1001–1006
    1. Urban R. J., Bodenburg Y. H., Gilkison C., Foxworth J., Coggan A. R., Wolfe R. R., Ferrando A. (1995). Testosterone administration to elderly men increases skeletal muscle strength and protein synthesis. Am. J. Physiol. 269, E820–E86
    1. Visser M., Deeg D. J., Lips P. (2003). Low vitamin D and high parathyroid hormone levels as determinants of loss of muscle strength and muscle mass (sarcopenia): the Longitudinal Aging Study Amsterdam. J. Clin. Endocrinol. Metab. 88, 5766–577210.1210/jc.2003-030604
    1. Visser M., Goodpaster B. H., Kritchevsky S. B., Newman A. B., Nevitt M., Rubin S. M., Simonsick E. M., Harris T. B. (2005). Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons. J. Gerontol. A Biol. Sci. Med. Sci. 60, 324–33310.1093/gerona/60.3.324
    1. Visser M., Harris T. B., Langlois J., Hannan M. T., Roubenoff R., Felson D. T., Wilson P. W., Kiel D. P. (1998a). Body fat and skeletal muscle mass in relation to physical disability in very old men and women of the Framingham Heart Study. J. Gerontol. A Biol. Sci. Med. Sci. 53, M214–M22110.1093/gerona/53A.3.M214
    1. Visser M., Langlois J., Guralnik J. M., Cauley J. A., Kronmal R. A., Robbins J., Williamson J. D., Harris T. B. (1998b). High body fatness, but not low fat-free mass, predicts disability in older men and women: the Cardiovascular Health Study. Am. J. Clin. Nutr. 68, 584–590
    1. Volpi E., Nazemi R., Fujita S. (2004). Muscle tissue changes with aging. Curr. Opin. Clin. Nutr. Metab. Care 7, 405–41010.1097/01.mco.0000134362.76653.b2
    1. Wang Z. M., Visser M., Ma R., Baumgartner R. N., Kotler D., Gallagher D., Heymsfield S. B. (1996). Skeletal muscle mass: evaluation of neutron activation and dual-energy X-ray absorptiometry methods. J. Appl. Physiol. 80, 824–831
    1. Whittemore L. A., Song K., Li X., Aghajanian J., Davies M., Girgenrath S., Hill J. J., Jalenak M., Kelley P., Knight A., Maylor R., O’Hara D., Pearson A., Quazi A., Ryerson S., Tan X. Y., Tomkinson K. N., Veldman G. M., Widom A., Wright J. F., Wudyka S., Zhao L., Wolfman N. M. (2003). Inhibition of myostatin in adult mice increases skeletal muscle mass and strength. Biochem. Biophys. Res. Commun. 300, 965–97110.1016/S0006-291X(02)02953-4
    1. Wilkes E. A., Selby A. L., Atherton P. J., Patel R., Rankin D., Smith K., Rennie M. J. (2009). Blunting of insulin inhibition of proteolysis in legs of older subjects may contribute to age-related sarcopenia. Am. J. Clin. Nutr. 90, 1343–135010.3945/ajcn.2009.27543
    1. Wroblewski A. P., Amati F., Smiley M. A., Goodpaster B., Wright V. (2011). Chronic exercise preserves lean muscle mass in masters athletes. Phys. Sportsmed. 39, 172–17810.3810/psm.2011.09.1933
    1. Yende S., Waterer G. W., Tolley E. A., Newman A. B., Bauer D. C., Taaffe D. R., Jensen R., Crapo R., Rubin S., Nevitt M., Simonsick E. M., Satterfield S., Harris T., Kritchevsky S. B. (2006). Inflammatory markers are associated with ventilatory limitation and muscle dysfunction in obstructive lung disease in well functioning elderly subjects. Thorax 61, 10–1610.1136/thx.2004.034181
    1. Young A., Stokes M., Crowe M. (1985). The size and strength of the quadriceps muscles of old and young men. Clin. Physiol. 5, 145–15410.1111/j.1475-097X.1985.tb00590.x
    1. Yu F., Hedstrom M., Cristea A., Dalen N., Larsson L. (2007). Effects of ageing and gender on contractile properties in human skeletal muscle and single fibres. Acta Physiol. (Oxf.) 190, 229–24110.1111/j.1748-1716.2007.01699.x

Source: PubMed

Sponsors and Collaborators

Medical Conditions

Drug Interventions

3
Subscribe