In vivo and in vitro evidence that intrinsic upper- and lower-limb skeletal muscle function is unaffected by ageing and disuse in oldest-old humans

Acta Physiologica

Volumn 215, Issue 1, 2015, Pages 58-71

  Venturelli, M ^a,b   Saggin, P ^c   Muti, E ^d   Naro, F ^e   Cancellara, L ^f   Toniolo, L ^f   Tarperi, C ^b   Calabria, E ^b   Richardson, R S ^g,h,i   Reggiani, C ^f,j   Schena, F ^b  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF VERONA   (Italy)

^c City Hospital of Verona   (Italy)

^d Mons Mazzali Foundation   (Italy)

^e SAPIENZA UNIVERSITY OF ROME   (Italy)

^f UNIVERSITY OF PADOVA   (Italy)

^g UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^h VETERANS AFFAIRS MEDICAL CENTER   (United States)

ⁱ UNIVERSITY OF UTAH   (United States)

^j CNR   (Italy)

more..

Author keywords

In vitro; In vivo; Oldest old; Sarcopenia

Indexed keywords

GLUCOSE; HEMOGLOBIN; LOW DENSITY LIPOPROTEIN;

ADULT; AGED; ARM MUSCLE; ARTICLE; BICEPS BRACHII MUSCLE; BODY MASS; BODY WEIGHT; CLINICAL ARTICLE; CONTROLLED STUDY; DIASTOLIC BLOOD PRESSURE; ELECTROSTIMULATION; FEMALE; GLUCOSE BLOOD LEVEL; HEMOGLOBIN BLOOD LEVEL; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INTRINSIC SKELETAL MUSCLE FUNCTION; LEG MUSCLE; MALE; MUSCLE BIOPSY; MUSCLE CONTRACTION; MUSCLE FUNCTION; MUSCLE LENGTH; MUSCLE MASS; NERVE STIMULATION; PRIORITY JOURNAL; QUADRICEPS FEMORIS MUSCLE; SARCOMERE LENGTH; SYSTOLIC BLOOD PRESSURE; ADAPTATION; AGING; ELBOW; LIMB; MUSCLE STRENGTH; PHYSIOLOGY; SKELETAL MUSCLE; VERY ELDERLY; YOUNG ADULT;

ADAPTATION, PHYSIOLOGICAL; ADULT; AGED, 80 AND OVER; AGING; ELBOW; EXTREMITIES; HUMANS; MUSCLE CONTRACTION; MUSCLE STRENGTH; MUSCLE, SKELETAL; QUADRICEPS MUSCLE; YOUNG ADULT;

EID: 84937972047     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/apha.12524     Document Type: Article

References (74)

1. Aagaard, P., Suetta, C., Caserotti, P., Magnusson, S.P. & 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.
2. Barns, M., Gondro, C., Tellam, R.L., Radley-Crabb, H.G., Grounds, M.D. & Shavlakadze, T. 2014. Molecular analyses provide insight into mechanisms underlying sarcopenia and myofibre denervation in old skeletal muscles of mice. Int J Biochem Cell Biol 53, 174-185.
3. Berg, H.E., Larsson, L. & Tesch, P.A. 1997. Lower limb skeletal muscle function after 6 wk of bed rest. J Appl Physiol 82, 182-188.
4. Blaauw, B., Schiaffino, S. & Reggiani, C. 2013. Mechanisms modulating skeletal muscle phenotype. Compr Physiol 3, 1645-1687.
5. Bottinelli, R., Pellegrino, M.A., Canepari, M., Rossi, R. & Reggiani, C. 1999. Specific contributions of various muscle fibre types to human muscle performance: an in vitro study. J Electromyogr Kinesiol 9, 87-95.
6. Buford, T.W., Lott, D.J., Marzetti, E., Wohlgemuth, S.E., Vandenborne, K., Pahor, M., Leeuwenburgh, C. & Manini, T.M. 2012. Age-related differences in lower extremity tissue compartments and associations with physical function in older adults. Exp Gerontol 47, 38-44.
7. Callahan, D.M., Bedrin, N.G., Subramanian, M., Berking, J., Ades, P.A., Toth, M.J. & Miller, M.S. 2014a. Age-related structural alterations in human skeletal muscle fibers and mitochondria are sex specific: relationship to single-fiber function. J Appl Physiol (1985), 116, 1582-1592.
8. Callahan, D.M., Miller, M.S., Sweeny, A.P., Tourville, T.W., Slauterbeck, J.R., Savage, P.D., Maugan, D.W., Ades, P.A., Beynnon, B.D. & Toth, M.J. 2014b. Muscle disuse alters skeletal muscle contractile function at the molecular and cellular levels in older adult humans in a sex-specific manner. J Physiol 592, 4555-4573.
9. Campbell, E.L., Seynnes, O.R., Bottinelli, R., McPhee, J.S., Atherton, P.J., Jones, D.A., Butler-Browne, G. & Narici, M.V. 2013. Skeletal muscle adaptations to physical inactivity and subsequent retraining in young men. Biogerontology 14, 247-259.
10. Canepari, M., Pellegrino, M.A., D'Antona, G. & Bottinelli, R. 2010a. Single muscle fiber properties in aging and disuse. Scand J Med Sci Sports 20, 10-19.
11. Canepari, M., Pellegrino, M.A., D'Antona, G. & Bottinelli, R. 2010b. Skeletal muscle fibre diversity and the underlying mechanisms. Acta Physiol (Oxf) 199, 465-476.
12. Ciciliot, S., Rossi, A.C., Dyar, K.A., Blaauw, B. & Schiaffino, S. 2013. Muscle type and fiber type specificity in muscle wasting. Int J Biochem Cell Biol 45, 2191-2199.
13. 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 552, 499-511.
14. Delbono, O. 2003. Neural control of aging skeletal muscle. Aging Cell 2, 21-29.
15. Delbono, O. 2011. Expression and regulation of excitation-contraction coupling proteins in aging skeletal muscle. Curr Aging Sci 4, 248-259.
16. 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., for the Health, Aging, and Body Composition Study. 2009. Longitudinal study of muscle strength, quality, and adipose tissue infiltration. Am J Clin Nutr, 90, 1579-1585.
17. Deschenes, M.R., Britt, A.A. & Chandler, W.C. 2001. A comparison of the effects of unloading in young adult and aged skeletal muscle. Med Sci Sports Exerc 33, 1477-1483.
18. Doherty, T.J. 2003. Invited review: aging and sarcopenia. J Appl Physiol 95, 1717-1727.
19. 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 (1985), 74, 868-874.
20. Doria, C., Toniolo, L., Verratti, V., Cancellara, P., Pietrangelo, T., Marconi, V., Paoli, A., Pogliaghi, S., Fano, G., Reggiani, C. & Capelli, C. 2011. Improved VO2 uptake kinetics and shift in muscle fiber type in high-altitude trekkers. J Appl Physiol (1985), 111, 1597-1605.
21. Dufour, A.B., Hannan, M.T., Murabito, J.M., Kiel, D.P. & McLean, R.R. 2013. Sarcopenia definitions considering body size and fat mass are associated with mobility limitations: the Framingham Study. J Gerontol A Biol Sci Med Sci 68, 168-174.
22. Erskine, R.M., Jones, D.A., Maganaris, C.N. & Degens, H. 2009. In vivo specific tension of the human quadriceps femoris muscle. Eur J Appl Physiol 106, 827-838.
23. Fielding, R.A., Vellas, B., Evans, W.J., Bhasin, S., Morley, J.E., Newman, A.B., Abellan van Kan, G., Andrieu, S., Bauer, J., Breuille, D. et al. 2011. Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc 12, 249-256.
24. 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 (1985), 71, 644-650.
25. Frontera, W.R., Suh, D., Krivickas, L.S., Hughes, V.A., Goldstein, R. & Roubenoff, R. 2000. Skeletal muscle fiber quality in older men and women. Am J Physiol Cell Physiol 279, C611-C618.
26. Frontera, W.R., Reid, K.F., Phillips, E.M., Krivickas, L.S., Hughes, V.A., Roubenoff, R. & Fielding, R.A. 2008. Muscle fiber size and function in elderly humans: a longitudinal study. J Appl Physiol (1985), 105, 637-642.
27. Galea, V. 1996. Changes in motor unit estimates with aging. J Clin Neurophysiol 13, 253-260.
28. 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 (1985), 83, 229-239.
29. 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, 1059-1064.
30. Hakkinen, K., Kallinen, M., Izquierdo, M., Jokelainen, K., Lassila, H., Malkia, E., Kraemer, W.J., Newton, R.U. & Alen, M. 1998. Changes in agonist-antagonist EMG, muscle CSA, and force during strength training in middle-aged and older people. J Appl Physiol (1985), 84, 1341-1349.
31. Hughes, V.A., Frontera, W.R., Wood, M., Evans, W.J., Dallal, G.E., Roubenoff, R. & Fiatarone Singh, M.A. 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.
32. Hvid, L., Aagaard, P., Justesen, L., Bayer, M.L., Andersen, J.L., Ortenblad, N., Kjaer, M. & Suetta, C. 2010. Effects of aging on muscle mechanical function and muscle fiber morphology during short-term immobilization and subsequent retraining. J Appl Physiol (1985), 109, 1628-1634.
33. Hvid, L.G., Ortenblad, N., Aagaard, P., Kjaer, M. & Suetta, C. 2011. Effects of ageing on single muscle fibre contractile function following short-term immobilisation. J Physiol 589, 4745-4757.
34. Izquierdo, M., Aguado, X., Gonzalez, R., Lopez, J.L. & Hakkinen, K. 1999. Maximal and explosive force production capacity and balance performance in men of different ages. Eur J Appl Physiol Occup Physiol 79, 260-267.
35. 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 (1985), 89, 81-88.
36. 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, 889-896.
37. Kamen, G., Sison, S.V., Du, C.C. & Patten, C. 1995. Motor unit discharge behavior in older adults during maximal-effort contractions. J Appl Physiol (1985), 79, 1908-1913.
38. Kragstrup, T.W., Kjaer, M. & Mackey, A.L. 2011. Structural, biochemical, cellular, and functional changes in skeletal muscle extracellular matrix with aging. Scand J Med Sci Sports 21, 749-757.
39. 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.
40. Lexell, J. 1997. Evidence for nervous system degeneration with advancing age. J Nutr 127, 1011S-1013S.
41. Maganaris, C.N., Baltzopoulos, V., Ball, D. & Sargeant, A.J. 2001. In vivo specific tension of human skeletal muscle. J Appl Physiol (1985), 90, 865-872.
42. Merton, P.A. 1954. Voluntary strength and fatigue. J Physiol, 123, 553-564.
43. 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-B365.
44. Murray, W.M., Buchanan, T.S. & Delp, S.L. 2000. The isometric functional capacity of muscles that cross the elbow. J Biomech 33, 943-952.
45. Narici, M.V. & Maffulli, N. 2010. Sarcopenia: characteristics, mechanisms and functional significance. Br Med Bull 95, 139-159.
46. Ochala, J., Frontera, W.R., Dorer, D.J., Van Hoecke, J. & Krivickas, L.S. 2007. Single skeletal muscle fiber elastic and contractile characteristics in young and older men. J Gerontol A Biol Sci Med Sci 62, 375-381.
47. Onder, G., Penninx, B.W., Ferrucci, L., Fried, L.P., Guralnik, J.M. & Pahor, M. 2005. Measures of physical performance and risk for progressive and catastrophic disability: results from the Women's Health and Aging Study. J Gerontol A Biol Sci Med Sci 60, 74-79.
48. Paoli, A., Pacelli, Q.F., Toniolo, L., Miotti, D. & Reggiani, C. 2010. Latissimus dorsi fine needle muscle biopsy: a novel and efficient approach to study proximal muscles of upper limbs. J Surg Res 164, e257-e263.
49. Payne, A.M. & Delbono, O. 2004. Neurogenesis of excitation-contraction uncoupling in aging skeletal muscle. Exerc Sport Sci Rev 32, 36-40.
50. Pereon, Y., Navarro, J., Hamilton, M., Booth, F.W. & Palade, P. 1997. Chronic stimulation differentially modulates expression of mRNA for dihydropyridine receptor isoforms in rat fast twitch skeletal muscle. Biochem Biophys Res Commun 235, 217-222.
51. Petrella, J.K., Kim, J.S., Mayhew, D.L., Cross, J.M. & Bamman, M.M. 2008. Potent myofiber hypertrophy during resistance training in humans is associated with satellite cell-mediated myonuclear addition: a cluster analysis. J Appl Physiol (1985), 104, 1736-1742.
52. Pojednic, R.M., Clark, D.J., Patten, C., Reid, K., Phillips, E.M. & Fielding, R.A. 2012. The specific contributions of force and velocity to muscle power in older adults. Exp Gerontol 47, 608-613.
53. Powell, P.L., Roy, R.R., Kanim, P., Bello, M.A. & Edgerton, V.R. 1984. Predictability of skeletal muscle tension from architectural determinations in guinea pig hindlimbs. J Appl Physiol Respir Environ Exerc Physiol 57, 1715-1721.
54. Purves-Smith, F.M., Sgarioto, N. & Hepple, R.T. 2014. Fiber typing in aging muscle. Exerc Sport Sci Rev 42, 45-52.
55. 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 (1985), 106, 1611-1617.
56. Reid, K.F., Doros, G., Clark, D.J., Patten, C., Carabello, R.J., Cloutier, G.J., Phillips, E.M., Krivickas, L.S., Frontera, W.R. & Fielding, R.A. 2012. 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.
57. Saborido, A., Molano, F., Moro, G. & Megias, A. 1995. Regulation of dihydropyridine receptor levels in skeletal and cardiac muscle by exercise training. Pflugers Arch 429, 364-369.
58. Sandiford, S.D., Green, H.J., Duhamel, T.A., Schertzer, J.D., Perco, J.D. & Ouyang, J. 2005. Muscle Na-K-pump and fatigue responses to progressive exercise in normoxia and hypoxia. Am J Physiol Regul Integr Comp Physiol 289, R441-R449.
59. Sayer, A.A., Robinson, S.M., Patel, H.P., Shavlakadze, T., Cooper, C. & Grounds, M.D. 2013. New horizons in the pathogenesis, diagnosis and management of sarcopenia. Age Ageing 42, 145-150.
60. Schiaffino, S. & Reggiani, C. 2011. Fiber types in mammalian skeletal muscles. Physiol Rev 91, 1447-1531.
61. Suetta, C. & Kjaer, M. 2010. What are the mechanisms behind disuse and age-related skeletal muscle atrophy? Scand J Med Sci Sports 20, 167-168.
62. Suetta, C., Aagaard, P., Rosted, A., Jakobsen, A.K., Duus, B., Kjaer, M. & Magnusson, S.P. 2004. Training-induced changes in muscle CSA, muscle strength, EMG, and rate of force development in elderly subjects after long-term unilateral disuse. J Appl Physiol (1985), 97, 1954-1961.
63. Suetta, C., Aagaard, P., Magnusson, S.P., Andersen, L.L., Sipila, S., Rosted, A., Jakobsen, A.K., Duus, B. & Kjaer, M. 2007. Muscle size, neuromuscular activation, and rapid force characteristics in elderly men and women: effects of unilateral long-term disuse due to hip-osteoarthritis. J Appl Physiol (1985), 102, 942-948.
64. Suetta, C., Hvid, L.G., Justesen, L., Christensen, U., Neergaard, K., Simonsen, L., Ortenblad, N., Magnusson, S.P., Kjaer, M. & Aagaard, P. 2009. Effects of aging on human skeletal muscle after immobilization and retraining. J Appl Physiol (1985), 107, 1172-1180.
65. Talmadge, R.J. & Roy, R.R. 1993. Electrophoretic separation of rat skeletal muscle myosin heavy-chain isoforms. J Appl Physiol (1985), 75, 2337-2340.
66. Tinetti, M.E. 1986. Performance-oriented assessment of mobility problems in elderly patients. J Am Geriatr Soc 34, 119-126.
67. Toniolo, L., Maccatrozzo, L., Patruno, M., Pavan, E., Caliaro, F., Rossi, R., Rinaldi, C., Canepari, M., Reggiani, C. & Mascarello, F. 2007. Fiber types in canine muscles: myosin isoform expression and functional characterization. Am J Physiol Cell Physiol 292, C1915-C1926.
68. 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.
69. Vandervoort, A.A. 2002. Aging of the human neuromuscular system. Muscle Nerve 25, 17-25.
70. Venturelli, M., Schena, F. & Richardson, R.S. 2012. The role of exercise capacity in the health and longevity of centenarians. Maturitas 73, 115-120.
71. Venturelli, M., Morgan, G.R., Donato, A.J., Reese, V., Bottura, R., Tarperi, C., Milanese, C., Schena, F., Reggiani, C., Naro, F., Cawthon, R.M. & Richardson, R.S. 2014. Cellular aging of skeletal muscle: telomeric and free radical evidence that physical inactivity is responsible and not age. Clin Sci (Lond) 127, 5.
72. Yozbatiran, N., Der-Yeghiaian, L. & Cramer, S.C. 2008. A standardized approach to performing the action research arm test. Neurorehabil Neural Repair 22, 78-90.
73. 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, 229-241.
74. Zimmerman, S.D., McCormick, R.J., Vadlamudi, R.K. & Thomas, D.P. 1993. Age and training alter collagen characteristics in fast- and slow-twitch rat limb muscle. J Appl Physiol (1985), 75, 1670-1674.