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Longitudinal impact of aging on muscle quality in middle-aged men

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Abstract

The present follow-up study aims at assessing the longitudinal changes in muscle quality after an interval of 9.45 years in middle-aged men. In addition, the relative contribution of muscle mass, muscle strength, and muscle power at middle age to these changes was investigated. The results showed a small, though unexpected, increase in total body and leg muscle mass (respectively 0.22 ± 0.04 and 0.29 ± 0.06 % yearly, p < 0.0001), whereas basic strength (−0.71 to −0.87 % yearly, p < 0.0001) and velocity-dependent strength and power (−1.19 to −1.86 % yearly, p < 0.0001) declined. Consequently, muscle quality, defined as the ratio of basic strength or velocity-dependent strength and power to muscle mass decreased (−1.46 to −2.43 % yearly, p < 0.0001) from baseline to follow-up. We found that baseline basic strength is a strong determinant of the decline in muscle quality basic strength with advancing age, whereas only a small part of the age-associated decline in muscle quality based on velocity-dependent strength and power could be explained. To conclude, our results indicate that muscle becomes less efficient at middle age and that baseline muscle strength is a strong predictor of this change. These findings imply that unmeasured neural factors, influencing both contraction speed and the capacity of muscle to produce strength, are possibly other involved determinants. Therefore, timely interventions including strength training and higher-velocity strength training at middle age are recommended.

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References

  • Barbat-Artigas S, Rolland Y, Zamboni M, ubertin-Leheudre M (2012) How to assess functional status: a new muscle quality index. J Nutr Health Aging 16:67–77

    Article  CAS  PubMed  Google Scholar 

  • Bautmans I, Vantieghem S, Gorus E, Grazzini YR, Fierens Y, Pool-Goudzwaard A, Mets T (2011) Age-related differences in pre-movement antagonist muscle co-activation and reaction-time performance. Exp Gerontol 46:637–642

    PubMed  Google Scholar 

  • Brooks GA, Butte NF, Rand WM, Flatt JP, Caballero B (2004) Chronicle of the Institute of Medicine physical activity recommendation: how a physical activity recommendation came to be among dietary recommendations. Am J Clin Nutr 79:921S–930S

    CAS  PubMed  Google Scholar 

  • Clark BC, Manini TM (2008) Sarcopenia =/=dynapenia. J Gerontol A Biol Sci Med Sci 63:829–834

    Article  PubMed  Google Scholar 

  • Clark DJ, Patten C, Reid KF, Carabello RJ, Phillips EM, Fielding RA (2011) Muscle performance and physical function are associated with voluntary rate of neuromuscular activation in older adults. J Gerontol A Biol Sci Med Sci 66:115–121

    Article  PubMed  Google Scholar 

  • Delmonico MJ, Harris TB, Visser M, Park SW, Conroy MB, Velasquez-Mieyer P, Boudreau R, Manini TM, Nevitt M, Newman AB, Goodpaster BH (2009) Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr 90:1579–1585

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Drouin JM, Valovich-mcLeod TC, Shultz SJ, Gansneder BM, Perrin DH (2004) Reliability and validity of the Biodex system 3 pro isokinetic dynamometer velocity, torque and position measurements. Eur J Appl Physiol 91:22–29

    Article  PubMed  Google Scholar 

  • Fantin F, Di Francesco V, Fontana G, Zivelonghi A, Bissoli L, Zoico E, Rossi A, Micciolo R, Bosello O, Zamboni M (2007) Longitudinal body composition changes in old men and women: interrelationships with worsening disability. J Gerontol A Biol Sci Med Sci 62:1375–1381

    Article  PubMed  Google Scholar 

  • Fleg JL, Morrell CH, Bos AG, Brant LJ, Talbot LA, Wright JG, Lakatta EG (2005) Accelerated longitudinal decline of aerobic capacity in healthy older adults. Circulation 112:674–682

    Article  PubMed  Google Scholar 

  • Frontera WR, Hughes VA, Lutz KJ, Evans WJ (1991) A cross-sectional study of muscle strength and mass in 45- to 78-yr-old men and women. J Appl Physiol (1985) 71:644–650

    CAS  Google Scholar 

  • Frontera WR, Hughes VA, Fielding RA, Fiatarone MA, Evans WJ, Roubenoff R (2000) Aging of skeletal muscle: a 12-yr longitudinal study. J Appl Physiol 88:1321–1326

    CAS  PubMed  Google Scholar 

  • Frontera WR, Reid KF, Phillips EM, Krivickas LS, Hughes VA, Roubenoff R, Fielding RA (2008) Muscle fiber size and function in elderly humans: a longitudinal study. J Appl Physiol 105:637–642

    Article  PubMed Central  PubMed  Google Scholar 

  • Goodpaster BH, Park SW, Harris TB, Kritchevsky SB, Nevitt M, Schwartz AV, Simonsick EM, Tylavsky FA, Visser M, Newman AB (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 61:1059–1064

    Article  PubMed  Google Scholar 

  • Guo SS, Zeller C, Chumlea WC, Siervogel RM (1999) Aging, body composition, and lifestyle: the Fels Longitudinal Study. Am J Clin Nutr 70:405–411

    CAS  PubMed  Google Scholar 

  • Guralnik JM, Ferrucci L, Pieper CF, Leveille SG, Markides KS, Ostir GV, Studenski S, Berkman LF, Wallace RB (2000) Lower extremity function and subsequent disability: consistency across studies, predictive models, and value of gait speed alone compared with the short physical performance battery. J Gerontol A Biol Sci Med Sci 55:M221–M231

    Article  CAS  PubMed  Google Scholar 

  • Hawkins S, Wiswell R (2003) Rate and mechanism of maximal oxygen consumption decline with aging: implications for exercise training. Sports Med 33:877–888

    Article  PubMed  Google Scholar 

  • Hicks GE, Shardell M, Alley DE, Miller RR, Bandinelli S, Guralnik J, Lauretani F, Simonsick EM, Ferrucci L (2012) Absolute strength and loss of strength as predictors of mobility decline in older adults: the InCHIANTI study. J Gerontol A Biol Sci Med Sci 67:66–73

  • Hofer SM, Flaherty BP, Hofmann L (2006) Cross-sectional analysis of time-dependent data: mean-induced association in age-heterogeneous samples and an alternative method based on sequential narrow age-cohort samples. Multivar Behav Res 41:165–187

    Article  Google Scholar 

  • Hughes VA, Frontera WR, Wood M, Evans WJ, Dallal GE, Roubenoff R, Fiatarone Singh MA (2001) Longitudinal muscle strength changes in older adults: influence of muscle mass, physical activity, and health. J Gerontol A Biol Sci Med Sci 56:B209–B217

    Article  CAS  PubMed  Google Scholar 

  • Hughes VA, Frontera WR, Roubenoff R, Evans WJ, Singh MA (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

    CAS  PubMed  Google Scholar 

  • Izquierdo M, Ibanez J, Gorostiaga E, Garrues M, Zuniga A, Anton A, Larrion JL, 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 167:57–68

    Article  CAS  PubMed  Google Scholar 

  • Kitamura I, Koda M, Otsuka R, Ando F, Shimokata H (2014) Six-year longitudinal changes in body composition of middle-aged and elderly Japanese: age and sex differences in appendicular skeletal muscle mass. Geriatr Gerontol Int 14:354–361

  • Koster A, Ding J, Stenholm S, Caserotti P, Houston DK, Nicklas BJ, You T, Lee JS, Visser M, Newman AB, Schwartz AV, Cauley JA, Tylavsky FA, Goodpaster BH, Kritchevsky SB, Harris TB (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 66A:888–895

  • Kostka T (2005) Quadriceps maximal power and optimal shortening velocity in 335 men aged 23-88 years. Eur J Appl Physiol 95:140–145

    Article  PubMed  Google Scholar 

  • Kyle UG, Genton L, Hans D, Karsegard L, Slosman DO, 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 55:663–672

    Article  CAS  PubMed  Google Scholar 

  • Lanza IR, Towse TF, Caldwell GE, Wigmore DM, Kent-Braun JA (2003) Effects of age on human muscle torque, velocity, and power in two muscle groups. J Appl Physiol 95:2361–2369

    CAS  PubMed  Google Scholar 

  • Lee RC, Wang ZM, Heymsfield SB (2001) Skeletal muscle mass and aging: regional and whole-body measurement methods. Can J Appl Physiol 26:102–122

    Article  CAS  PubMed  Google Scholar 

  • Lexell J, Downham D, Sjostrom M (1986) Distribution of different fibre types in human skeletal muscles. Fibre type arrangement in m. vastus lateralis from three groups of healthy men between 15 and 83 years. J Neurol Sci 72:211–222

    Article  CAS  PubMed  Google Scholar 

  • Macaluso A, De Vito G (2004) Muscle strength, power and adaptations to resistance training in older people. Eur J Appl Physiol 91:450–472

    Article  PubMed  Google Scholar 

  • Macaluso A, Nimmo MA, Foster JE, Cockburn M, McMillan NC, De VG (2002) Contractile muscle volume and agonist-antagonist coactivation account for differences in torque between young and older women. Muscle Nerve 25:858–863

    Article  PubMed  Google Scholar 

  • Manini TM, Clark BC (2012) Dynapenia and aging: an update. J Gerontol A Biol Sci Med Sci 67(1):28–40

    Article  PubMed  Google Scholar 

  • Matton L, Beunen G, Duvigneaud N, Wijndaele K, Philippaerts R, Claessens A, Vanreusel B, Thomis M, Lefevre J (2007) Methodological issues associated with longitudinal research: findings from the Leuven Longitudinal Study on Lifestyle, Fitness and Health (1. J Sports Sci 25:1011–1024

    Article  PubMed  Google Scholar 

  • Metter EJ, Conwit R, Tobin J, Fozard JL (1997) Age-associated loss of power and strength in the upper extremities in women and men. J Gerontol A Biol Sci Med Sci 52:B267–B276

    Article  CAS  PubMed  Google Scholar 

  • Metter EJ, Lynch N, Conwit R, Lindle R, Tobin J, Hurley B (1999) Muscle quality and age: cross-sectional and longitudinal comparisons. J Gerontol A Biol Sci Med Sci 54:B207–B218

    Article  CAS  PubMed  Google Scholar 

  • Mitchell WK, Williams J, Atherton P, Larvin M, Lund J, Narici M (2012) Sarcopenia, dynapenia, and the impact of advancing age on human skeletal muscle size and strength; a quantitative review. Front Physiol 3:260

    Article  PubMed Central  PubMed  Google Scholar 

  • Narici MV, Maganaris CN, Reeves ND, Capodaglio P (2003) Effect of aging on human muscle architecture. J Appl Physiol 95:2229–2234

    CAS  PubMed  Google Scholar 

  • Osternig LR (1986) Isokinetic dynamometry: implications for muscle testing and rehabilitation. Exerc Sport Sci Rev 14:45–80

    Article  CAS  PubMed  Google Scholar 

  • Raj IS, Bird SR, Shield AJ (2010) Aging and the force-velocity relationship of muscles. Exp Gerontol 45:81–90

    Article  CAS  PubMed  Google Scholar 

  • Rantanen T, Masaki KH, Foley D, Izmirlian G, White L, Guralnik J (1998) Grip strength changes over 27 yr in Japanese-American men. J Appl Physiol 85:2047–2053

    CAS  PubMed  Google Scholar 

  • Reid KF, Pasha E, Doros G, Clark DJ, Patten C, Phillips EM, Frontera WR, Fielding RA (2014) Longitudinal decline of lower extremity muscle power in healthy and mobility-limited older adults: influence of muscle mass, strength, composition, neuromuscular activation and single fiber contractile properties. Eur J Appl Physiol 114:29–39

  • Rolland Y, Czerwinski S, Abellan Van KG, Morley JE, Cesari M, Onder G, Woo J, Baumgartner R, Pillard F, Boirie Y, Chumlea WM, Vellas B (2008) Sarcopenia: its assessment, etiology, pathogenesis, consequences and future perspectives. J Nutr Health Aging 12:433–450

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Roubenoff R, Hughes VA (2000) Sarcopenia: current concepts. J Gerontol A Biol Sci Med Sci 55:M716–M724

    Article  CAS  PubMed  Google Scholar 

  • Russ DW, Gregg-Cornell K, Conaway MJ, Clark BC (2012) Evolving concepts on the age-related changes in “muscle quality”. J Cachex Sarcopenia Muscle 3:95–109

    Article  Google Scholar 

  • Saris WH, Blair SN, van Baak MA, Eaton SB, Davies PS, Di PL, Fogelholm M, Rissanen A, Schoeller D, Swinburn B, Tremblay A, Westerterp KR, Wyatt H (2003) How much physical activity is enough to prevent unhealthy weight gain? Outcome of the IASO 1st Stock Conference and consensus statement. Obes Rev 4:101–114

    Article  CAS  PubMed  Google Scholar 

  • Singh MA (2002) Exercise comes of age: rationale and recommendations for a geriatric exercise prescription. J Gerontol A Biol Sci Med Sci 57:M262–M282

    Article  PubMed  Google Scholar 

  • Skelton DA, Greig CA, Davies JM, Young A (1994) Strength, power and related functional ability of healthy people aged 65-89 years. Age Ageing 23:371–377

    Article  CAS  PubMed  Google Scholar 

  • Stenholm S, Tiainen K, Rantanen T, Sainio P, Heliovaara M, Impivaara O, Koskinen S (2012) Long-term determinants of muscle strength decline: prospective evidence from the 22-year mini-Finland follow-up survey. J Am Geriatr Soc 60:77–85

    Article  PubMed  Google Scholar 

  • Thompson BJ, Ryan ED, Sobolewski EJ, Conchola EC, Cramer JT (2013) Age related differences in maximal and rapid torque characteristics of the leg extensors and flexors in young, middle-aged and old men. Exp Gerontol 48:277–282

    Article  PubMed  Google Scholar 

  • von Haehling S, Morley JE, Anker SD (2010) An overview of sarcopenia: facts and numbers on prevalence and clinical impact. J Cachex Sarcopenia Muscle 1:129–133

    Article  Google Scholar 

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Acknowledgments

This study was conducted under the authority of the Policy Research Center “Sports,” with financial support from the Flemish Government.

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Authors and Affiliations

  1. Physical Activity, Sports and Health Research Group, Department of Kinesiology, Faculty of Kinesiology and Rehabilitation Sciences, Katholieke Universiteit Leuven, Tervuursevest 101, 3001, Leuven, Belgium

    Eva Kennis, Evelien Van Roie, Martine Thomis, Johan Lefevre & Christophe Delecluse

  2. Research Group for Musculoskeletal Rehabilitation, Department of Rehabilitation Sciences, Faculty of Kinesiology and Rehabilitation Sciences, Katholieke Universiteit Leuven, Leuven, Belgium

    Sabine Verschueren

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  1. Eva Kennis
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  2. Sabine Verschueren
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  6. Christophe Delecluse
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Correspondence to Eva Kennis.

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Kennis, E., Verschueren, S., Van Roie, E. et al. Longitudinal impact of aging on muscle quality in middle-aged men. AGE 36, 9689 (2014). https://doi.org/10.1007/s11357-014-9689-1

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