Skip to main content
SpringerLink
Log in

Muscle power failure in mobility-limited older adults: preserved single fiber function despite lower whole muscle size, quality and rate of neuromuscular activation

  • Original Article
  • Published:
European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

This study investigated the physiological and gender determinants of the age-related loss of muscle power in 31 healthy middle-aged adults (aged 40–55 years), 28 healthy older adults (70–85 years) and 34 mobility-limited older adults (70–85 years). We hypothesized that leg extensor muscle power would be significantly lower in mobility-limited elders relative to both healthy groups and sought to characterize the physiological mechanisms associated with the reduction of muscle power with aging. Computed tomography was utilized to assess mid-thigh body composition and calculate specific muscle power and strength. Surface electromyography was used to assess rate of neuromuscular activation and muscle biopsies were taken to evaluate single muscle fiber contractile properties. Peak muscle power, strength, muscle cross-sectional area, specific muscle power and rate of neuromuscular activation were significantly lower among mobility-limited elders compared to both healthy groups (P ≤ 0.05). Mobility-limited older participants had greater deposits of intermuscular adipose tissue (P < 0.001). Single fiber contractile properties of type I and type IIA muscle fibers were preserved in mobility-limited elders relative to both healthy groups. Male gender was associated with greater decrements in peak and specific muscle power among mobility-limited participants. Impairments in the rate of neuromuscular activation and concomitant reductions in muscle quality are important physiological mechanisms contributing to muscle power deficits and mobility limitations. The dissociation between age-related changes at the whole muscle and single fiber level suggest that, even among older adults with overt mobility problems, contractile properties of surviving muscle fibers are preserved in an attempt to maintain overall muscle function.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aagaard P, Suetta C, Caserotti P, Magnusson SP, Kjaer M (2010) Role of the nervous system in sarcopenia and muscle atrophy with aging: strength training as a countermeasure. Scand J Med Sci Sports 20:49–64

    Article  PubMed  CAS  Google Scholar 

  • Bassey EJ, Fiatarone MA, O’Neill EF, Kelly M, Evans WJ, Lipsitz LA (1992) Leg extensor power and functional performance in very old men and women. Clin Sci (Lond) 82:321–327

    CAS  Google Scholar 

  • Bean JF, Kiely DK, Herman S, Leveille SG, Mizer K, Frontera WR, Fielding RA (2002) The relationship between leg power and physical performance in mobility-limited older people. J Am Geriatr Soc 50:461–467

    Article  PubMed  Google Scholar 

  • Bergström J (1962) Muscle electrolytes in man. Scand J Clin Lab Invest 14:1–68

    Article  Google Scholar 

  • Borg G (1970) Perceived exertion as an indicator of somatic stress. Scand J Rehabil Med 2:92–98

    PubMed  CAS  Google Scholar 

  • Brooks SV, Faulkner JA (1994) Skeletal muscle weakness in old age: underlying mechanisms. Med Sci Sports Exerc 26:432–439

    PubMed  CAS  Google Scholar 

  • Callahan D, Phillips E, Carabello R, Frontera WR, Fielding RA (2007) Assessment of lower extremity muscle power in functionally-limited elders. Aging Clin Exp Res 19:194–199

    PubMed  Google Scholar 

  • Caserotti P, Aagaard P, Simonsen EB, Puggaard L (2001) Contraction-specific differences in maximal muscle power during stretch-shortening cycle movements in elderly males and females. Eur J Appl Physiol 84:206–212

    Article  PubMed  CAS  Google Scholar 

  • Clark DJ, Patten C, Reid KF, Carabello RJ, Phillips EM, Fielding RA (2010) Impaired voluntary neuromuscular activation limits muscle power in mobility-limited older adults. J Gerontol A Biol Sci Med Sci 65:495–502

    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 

  • D’Antona G, Pellegrino MA, Adami R, Rossi R, Carlizzi CN, Canepari M, Saltin B, Bottinelli R (2003) The effect of ageing and immobilization on structure and function of human skeletal muscle fibres. J Physiol 552:499–511

    Article  PubMed  Google Scholar 

  • D’Antona G, Pellegrino MA, Carlizzi CN, Bottinelli R (2007) Deterioration of contractile properties of muscle fibres in elderly subjects is modulated by the level of physical activity. Eur J Appl Physiol 100:603–611

    Article  PubMed  Google Scholar 

  • De Serres SJ, Enoka RM (1998) Older adults can maximally activate the biceps brachii muscle by voluntary command. J Appl Physiol 84:284–291

    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  PubMed  CAS  Google Scholar 

  • Doherty TJ (2001) The influence of aging and sex on skeletal muscle mass and strength. Curr Opin Clin Nutr Metab Care 4:503–508

    Article  PubMed  CAS  Google Scholar 

  • Doherty TJ (2003) Invited review: aging and sarcopenia. J Appl Physiol 95:1717–1727

    PubMed  CAS  Google Scholar 

  • Edman KA (1979) The velocity of unloaded shortening and its relation to sarcomere length and isometric force in vertebrate muscle fibres. J Physiol 291:143–159

    PubMed  CAS  Google Scholar 

  • Evans WJ (1995) What is sarcopenia? J Gerontol A Biol Sci Med Sci 50 (spec no 5–8)

  • Evans WJ, Phinney SD, Young VR (1982) Suction applied to a muscle biopsy maximizes sample size. Med Sci Sports Exerc 14:101–102

    PubMed  CAS  Google Scholar 

  • Fabiato A (1988) Computer programs for calculating total from specified free or free from specified total ionic concentrations in aqueous solutions containing multiple metals and ligands. Methods Enzymol 157:378–417

    Article  PubMed  CAS  Google Scholar 

  • Folstein MF, Folstein SE, McHugh PR (1975) Mini-mental state a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  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 71:644–650

    PubMed  CAS  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  Google Scholar 

  • Frontera WR, Suh D, Krivickas LS, Hughes VA, Goldstein R, Roubenoff R (2000b) Skeletal muscle fiber quality in older men and women. Am J Physiol Cell Physiol 279:C611–C618

    PubMed  CAS  Google Scholar 

  • Godt RE, Maughan DW (1977) Swelling of skinned muscle fibers of the frog. Experimental observations. Biophys J 19:103–116

    Article  PubMed  CAS  Google Scholar 

  • Goodpaster BH, Carlson CL, Visser M, Kelley DE, Scherzinger A, Harris TB, Stamm E, Newman AB (2001) Attenuation of skeletal muscle and strength in the elderly: the Health ABC Study. J Appl Physiol 90:2157–2165

    PubMed  CAS  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 

  • 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  PubMed  CAS  Google Scholar 

  • Guralnik JM, Ferrucci L, Simonsick EM, Salive ME, Wallace RB (1995) Lower-extremity function in persons over the age of 70 years as a predictor of subsequent disability. N Engl J Med 332:556–561

    Article  PubMed  CAS  Google Scholar 

  • Guralnik JM, Simonsick EM, Ferrucci L, Glynn RJ, Berkman LF, Blazer DG, Scherr PA, Wallace RB (1994) A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission. J Gerontol 49:M85–M94

    PubMed  CAS  Google Scholar 

  • Hakkinen K, Kallinen M, Izquierdo M, Jokelainen K, Lassila H, Malkia E, Kraemer WJ, Newton RU, Alen M (1998) Changes in agonist-antagonist EMG, muscle CSA, and force during strength training in middle-aged and older people. J Appl Physiol 84:1341–1349

    PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Kamen G, Sison SV, Du CC, Patten C (1995) Motor unit discharge behavior in older adults during maximal-effort contractions. J Appl Physiol 79:1908–1913

    PubMed  CAS  Google Scholar 

  • Kelley DE, Slasky BS, Janosky J (1991) Skeletal muscle density: effects of obesity and non-insulin-dependent diabetes mellitus. Am J Clin Nutr 54:509–515

    PubMed  CAS  Google Scholar 

  • Kent-Braun JA, Ng AV (1999) Specific strength and voluntary muscle activation in young and elderly women and men. J Appl Physiol 87:22–29

    PubMed  CAS  Google Scholar 

  • Kuo HK, Leveille SG, Yen CJ, Chai HM, Chang CH, Yeh YC, Yu YH, Bean JF (2006) Exploring how peak leg power and usual gait speed are linked to late-life disability: data from the National Health and Nutrition Examination Survey (NHANES), 1999–2002. Am J Phys Med Rehabil 85:650–658

    Article  PubMed  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Larsson L, Grimby G, Karlsson J (1979) Muscle strength and speed of movement in relation to age and muscle morphology. J Appl Physiol 46:451–456

    PubMed  CAS  Google Scholar 

  • Larsson L, Moss RL (1993) Maximum velocity of shortening in relation to myosin isoform composition in single fibres from human skeletal muscles. J Physiol 472:595–614

    PubMed  CAS  Google Scholar 

  • Lexell J (1997) Evidence for nervous system degeneration with advancing age. J Nutr 127:1011S–1013S

    PubMed  CAS  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 

  • Martin JC, Farrar RP, Wagner BM, Spirduso WW (2000) Maximal power across the lifespan. J Gerontol A Biol Sci Med Sci 55:M311–M316

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Moss RL (1979) Sarcomere length-tension relations of frog skinned muscle fibres during calcium activation at short lengths. J Physiol 292:177–192

    PubMed  CAS  Google Scholar 

  • Petrella JK, Kim JS, Tuggle SC, Hall SR, Bamman MM (2005) Age differences in knee extension power, contractile velocity, and fatigability. J Appl Physiol 98:211–220

    Article  PubMed  Google Scholar 

  • 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 106:1611–1617

    Article  PubMed  Google Scholar 

  • Reid KF, Callahan DM, Carabello RJ, Phillips EM, Frontera WR, Fielding RA (2008) Lower extremity power training in elderly subjects with mobility limitations: a randomized controlled trial. Aging Clin Exp Res 20:337–343

    PubMed  Google Scholar 

  • Schaap LA, Pluijm SM, Smit JH, van Schoor NM, Visser M, Gooren LJ, Lips P (2005) The association of sex hormone levels with poor mobility, low muscle strength and incidence of falls among older men and women. Clin Endocrinol (Oxf) 63:152–160

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Slivka D, Raue U, Hollon C, Minchev K, Trappe S (2008) Single muscle fiber adaptations to resistance training in old (>80 yr) men: evidence for limited skeletal muscle plasticity. Am J Physiol Regul Integr Comp Physiol 295:R273–R280

    Article  PubMed  CAS  Google Scholar 

  • Suzuki T, Bean JF, Fielding RA (2001) Muscle power of the ankle flexors predicts functional performance in community-dwelling older women. J Am Geriatr Soc 49:1161–1167

    Article  PubMed  CAS  Google Scholar 

  • Trappe S, Gallagher P, Harber M, Carrithers J, Fluckey J, Trappe T (2003) Single muscle fibre contractile properties in young and old men and women. J Physiol 552:47–58

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the National Institute on Aging grant number AG18844 and based upon work supported by the U.S. Department of Agriculture, under agreement No. 58-1950-7-707. Any opinions, findings, conclusion, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the U.S. Department of Agriculture. This research was also supported by the Boston Claude D. Pepper Older Americans Independence Center (1P30AG031679) and the Boston Rehabilitation Outcomes Center, funded by NIH Infrastructure Grant (1R24HD065688-01A1).

Conflict of interest

None.

Author information

Authors and Affiliations

  1. Nutrition, Exercise Physiology and Sarcopenia Laboratory, Jean Mayer United States Department of Agriculture Human Nutrition Research Center on Aging at Tufts University, 711 Washington Street, 02111, Boston, MA, USA

    Kieran F. Reid, Robert J. Carabello, Gregory J. Cloutier, Edward M. Phillips & Roger A. Fielding

  2. Department of Biostatistics, Boston University School of Public Health, Boston, MA, USA

    Gheorghe Doros

  3. Brain Rehabilitation Research Center, Malcom Randall VA Medical Center, Gainesville, FL, USA

    David J. Clark & Carolynn Patten

  4. Department of Aging and Geriatric Research, University of Florida, Gainesville, FL, USA

    David J. Clark

  5. Department of Physical Therapy, University of Florida, Gainesville, FL, USA

    Carolynn Patten

  6. Department of Physical Medicine and Rehabilitation, Harvard Medical School and Spaulding Rehabilitation Hospital, Boston, MA, USA

    Edward M. Phillips, Lisa S. Krivickas & Walter R. Frontera

  7. Department of Physical Medicine and Rehabilitation, University of Puerto Rico School of Medicine, San Juan, PR, USA

    Walter R. Frontera

  8. Department of Physiology, University of Puerto Rico School of Medicine, San Juan, PR, USA

    Walter R. Frontera

Authors
  1. Kieran F. Reid
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gheorghe Doros
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David J. Clark
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carolynn Patten
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Robert J. Carabello
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gregory J. Cloutier
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Edward M. Phillips
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Lisa S. Krivickas
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Walter R. Frontera
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Roger A. Fielding
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kieran F. Reid.

Additional information

Communicated by Arnold de Haan.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Reid, K.F., Doros, G., Clark, D.J. et al. Muscle power failure in mobility-limited older adults: preserved single fiber function despite lower whole muscle size, quality and rate of neuromuscular activation. Eur J Appl Physiol 112, 2289–2301 (2012). https://doi.org/10.1007/s00421-011-2200-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-011-2200-0

Keywords

Search

Navigation