Effects of aging on human skeletal muscle after immobilization and retraining
Abstract
Inactivity is a recognized compounding factor in sarcopenia and muscle weakness in old age. However, while the negative effects of unloading on skeletal muscle in young individuals are well elucidated, only little is known about the consequence of immobilization and the regenerative capacity in elderly individuals. Thus the aim of this study was to examine the effect of aging on changes in muscle contractile properties, specific force, and muscle mass characteristics in 9 old (61–74 yr) and 11 young men (21–27 yr) after 2 wk of immobilization and 4 wk of retraining. Both young and old experienced decreases in maximal muscle strength, resting twitch peak torque and twitch rate of force development, quadriceps muscle volume, pennation angle, and specific force after 2 wk of immobilization ( P < 0.05). The decline in quadriceps volume and pennation angle was smaller in old compared with young ( P < 0.05). In contrast, only old men experienced a decrease in quadriceps activation. After retraining, both young and old regained their initial muscle strength, but old had smaller gains in quadriceps volume compared with young, and pennation angle increased in young only ( P < 0.05). The present study is the first to demonstrate that aging alters the neuromuscular response to short-term disuse and recovery in humans. Notably, immobilization had a greater impact on neuronal motor function in old individuals, while young individuals were more affected at the muscle level. In addition, old individuals showed an attenuated response to retraining after immobilization compared with young individuals.
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Hospitalization-related loss of muscle mass and function can briefly worsen sarcopenia and lead to incomplete recovery, especially in older adults.
“The decline in muscle mass and function during hospitalization can transiently accelerate sarcopenic decline, resulting in incomplete recovery, particularly for older persons (2).”
Cites
Single-Step Method of RNA Isolation by Acid Guanidinium Thiocyanate–Phenol–Chloroform Extraction
Chomczynski, P., & Sacchi, N. (1987) · Analytical Biochemistry · doi:10.1006/abio.1987.9999 · Cited by 65,240 · see citing works
Church, G. M., & Gilbert, W. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.7.1991 · Cited by 8,213 · see citing works
Risk Factors for Falls among Elderly Persons Living in the Community
Tinetti, M. E., Speechley, M. R., & Ginter, S. F. (1988) · New England Journal of Medicine · doi:10.1056/nejm198812293192604 · Cited by 6,507 · see citing works
SATELLITE CELL OF SKELETAL MUSCLE FIBERS
Mauro, A. (1961) · The Journal of Cell Biology · doi:10.1083/jcb.9.2.493 · Cited by 3,683 · see citing works
Spinal and Supraspinal Factors in Human Muscle Fatigue
Gandevia, S. C. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.4.1725 · Cited by 3,655 · see citing works
Identification of ubiquitin ligases required for skeletal muscle atrophy.
Bodine, S. C., Latres, E., Baumhueter, S., Lai, V. K.-M., Nunez, L., Clarke, B. A., Poueymirou, W. T., Panaro, F. J., Na, E., Dharmarajan, K., et al. (2001) · Science · doi:10.1126/science.1065874 · Cited by 3,521 · see citing works
Janssen, I., Heymsfield, S. B., & Ross, R. (2002) · Journal of the American Geriatrics Society · doi:10.1046/j.1532-5415.2002.50216.x · Cited by 3,139 · see citing works
Invited Review: Aging and sarcopenia
Doherty, T. J. (2003) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00347.2003 · Cited by 1,764 · see citing works
Voluntary strength and fatigue
Merton, P. A. (1954) · The Journal of Physiology · doi:10.1113/jphysiol.1954.sp005070 · Cited by 1,448 · see citing works
Aging of skeletal muscle: a 12-yr longitudinal study
Frontera, W. R., Hughes, V. A., Fielding, R. A., Fiatarone, M. A., Evans, W. J., & Roubenoff, R. (2000) · Journal of Applied Physiology · doi:10.1152/jappl.2000.88.4.1321 · Cited by 1,443 · see citing works
Notch-Mediated Restoration of Regenerative Potential to Aged Muscle
Conboy, I. M., Conboy, M. J., Smythe, G. M., & Rando, T. A. (2003) · Science · doi:10.1126/science.1087573 · Cited by 1,121 · see citing works
SALTIN, B., & GRIMBY, G. (1968) · Circulation · doi:10.1161/01.cir.38.6.1104 · Cited by 1,015 · see citing works
Hindlimb unloading rodent model: technical aspects
Morey, E. R., & Globus, R. K. (2002) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00969.2001 · Cited by 998 · see citing works
Conboy, I. M., & Rando, T. A. (2002) · Developmental Cell · doi:10.1016/s1534-5807(02)00254-x · Cited by 905 · see citing works
Skeletal Muscle Strength as a Predictor of All-Cause Mortality in Healthy Men
Metter, E. J., Talbot, L. A., Schrager, M., & CONWIT, R. A. (2002) · The Journals of Gerontology Series A · doi:10.1093/gerona/57.10.b359 · Cited by 843 · see citing works
Aging of the human neuromuscular system
Vandervoort, A. A. (2001) · Muscle & Nerve · doi:10.1002/mus.1215 · Cited by 813 · see citing works
Gross and microscopic anatomy of the human intrinsic cardiac nervous system
Armour, J. A., Murphy, D. A., Yuan, B.-X., Macdonald, S. E., & Hopkins, D. A. (1997) · The Anatomical Record · doi:10.1002/(sici)1097-0185(199702)247:2 · Cited by 763 · see citing works
Aagaard, P., Andersen, J. L., Dyhre‐Poulsen, P., Leffers, A., Wagner, A., Magnusson, S. P., Halkjær‐Kristensen, J., & Simonsen, E. B. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.t01-1-00613.x · Cited by 733 · see citing works
Self-citationMuscle strength and body mass index as long-term predictors of mortality in initially healthy men
Rantanen, T., Harris, T., Leveille, S. G., Visser, M., Foley, D., Masaki, K., & Guralnik, J. M. (2000) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/55.3.m168 · Cited by 647 · see citing works
Atrophy of the soleus muscle by hindlimb unweighting
Thomason, D. B., & Booth, F. W. (1990) · Journal of Applied Physiology · doi:10.1152/jappl.1990.68.1.1 · Cited by 631 · see citing works
KLITGAARD, H., MANTONI, M., SCHIAFFINO, S., AUSONI, S., GORZA, L., LAURENT‐WINTER, C., SCHNOHR, P., & SALTIN, B. (1990) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1990.tb08974.x · Cited by 568 · see citing works
Predictability of skeletal muscle tension from architectural determinations in guinea pig hindlimbs
Powell, P. L., Roy, R. R., Kanim, P., Bello, M. A., & Edgerton, V. R. (1984) · Journal of Applied Physiology · doi:10.1152/jappl.1984.57.6.1715 · Cited by 553 · see citing works
Balagopal, P., Rooyackers, O., Adey, D., Ades, P. A., & Nair, K. S. (1997) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1997.273.4.e790 · Cited by 541 · see citing works
Esmarck, B., Andersen, J. L., Olsen, S., Richter, E. A., Mizuno, M., & Kjær, M. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.00301.x · Cited by 540 · see citing works
The effect of ageing and immobilization on structure and function of human skeletal muscle fibres
D’Antona, G. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.046276 · Cited by 477 · see citing works
Skeletal muscle weakness in old age: underlying mechanisms.
Brooks, S. V., & Faulkner, J. A. (1994) · PubMed · Cited by 463 · see citing works
Velocity Specificity of Resistance Training
Behm, D. G., & Sale, D. G. (1993) · Sports Medicine · doi:10.2165/00007256-199315060-00003 · Cited by 460 · see citing works
Mantón, K. G., Corder, L. S., & Stallard, E. (1993) · Journal of Gerontology · doi:10.1093/geronj/48.4.s153 · Cited by 438 · see citing works
Petrella, J. K., Kim, J.-S., Mayhew, D. L., Cross, J. M., & Bamman, M. M. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01215.2007 · Cited by 435 · see citing works
Neuromuscular fatigue after maximal stretch-shortening cycle exercise
Strojnik, V., & Komi, P. V. (1998) · Journal of Applied Physiology · doi:10.1152/jappl.1998.84.1.344 · Cited by 418 · see citing works
Jones, S. W., Hill, R. J. W., Krasney, P. A., O'Conner, B., Peirce, N. S., & Greenhaff, P. L. (2004) · The FASEB Journal · doi:10.1096/fj.03-1228fje · Cited by 406 · see citing works
Whole-muscle and single-fibre contractile properties and myosin heavy chain isoforms in humans
Harridge, S. D. R., Bottinelli, R., Canepari, M., Pellegrino, M. A., Reggiani, C., Esbjörnsson, M., & Saltin, B. (1996) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s004240050215 · Cited by 402 · see citing works
Apoptosis in skeletal muscle with aging
Dirks, A., & Leeuwenburgh, C. (2002) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00458.2001 · Cited by 377 · see citing works
Allen, D. L., Linderman, J. K., Roy, R. R., Bigbee, A. J., Grindeland, R. E., Mukku, V. R., & Edgerton, V. R. (1997) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1997.273.2.c579 · Cited by 364 · see citing works
Satellite cell activity is required for hypertrophy of overloaded adult rat muscle
Rosenblatt, J. D., Yong, D., & Parry, D. J. (1994) · Muscle & Nerve · doi:10.1002/mus.880170607 · Cited by 356 · see citing works
Hortobágyi, T., Dempsey, L. E., Fraser, D. D., Zheng, D., Hamilton, G., Lambert, J., & Dohm, L. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.00293.x · Cited by 354 · see citing works
Lower limb skeletal muscle function after 6 wk of bed rest
Berg, H. E., Larsson, L., & Tesch, P. A. (1997) · Journal of Applied Physiology · doi:10.1152/jappl.1997.82.1.182 · Cited by 352 · see citing works
The satellite cell and muscle regeneration
Bischoff, R. (1994) · Medical Entomology and Zoology · Cited by 336 · see citing works
Skeletal muscle satellite cells: Changes in proliferation potential as a function of age
Schultz, E., & Lipton, B. H. (1982) · Mechanisms of Ageing and Development · doi:10.1016/0047-6374(82)90105-1 · Cited by 335 · see citing works
Hespel, P., Op't Eijnde, B., Leemputte, M. V., Ursø, B., Greenhaff, P. L., Labarque, V., Dymarkowski, S., Hecke, P. V., & Richter, E. A. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.0625c.xd · Cited by 335 · see citing works
Klass, M., Baudry, S., & Duchateau, J. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00550.2007 · Cited by 323 · see citing works
Age‐related differences in absolute numbers of skeletal muscle satellite cells
Gibson, M. C., & Schultz, E. (1983) · Muscle & Nerve · doi:10.1002/mus.880060807 · Cited by 321 · see citing works
Regenerative potential of human skeletal muscle during aging
Renault, V. M., Thorne, L., Eriksson, P., Butler-Browne, G. S., & Mouly, V. (2002) · Aging Cell · doi:10.1046/j.1474-9728.2002.00017.x · Cited by 318 · see citing works
Muscle fibre type adaptation in the elderly human muscle
Andersen, J. L. (2003) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1034/j.1600-0838.2003.00299.x · Cited by 316 · see citing works
Training-Related Adaptations in Motor Unit Discharge Rate in Young and Older Adults
Kamen, G., & Knight, C. A. (2004) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/59.12.1334 · Cited by 312 · see citing works
Webster, C., & Blau, H. M. (1990) · Somatic Cell and Molecular Genetics · doi:10.1007/bf01233096 · Cited by 298 · see citing works
Effect of resistance training on skeletal muscle-specific force in elderly humans
Reeves, N. D., Narici, M. V., & Maganaris, C. N. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00688.2003 · Cited by 293 · see citing works
Boer, M. D. D., Maganaris, C. N., Seynnes, O., Rennie, M. J., & Narici, M. V. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.135392 · Cited by 284 · see citing works
Satellite cells and myonuclei in young and elderly women and men
Kadi, F., Charifi, N., Denis, C., & Lexell, J. E. (2003) · Muscle & Nerve · doi:10.1002/mus.10510 · Cited by 283 · see citing works
" CATABOLIC " LOSS OF BODY NITROGEN IN RESPONSE TO SURGERY
O’Keefe, S. J., Sender, P. M., & James, W. P. T. (1974) · The Lancet · doi:10.1016/s0140-6736(74)92149-7 · Cited by 269 · see citing works
Age‐associated Changes in the Response of Skeletal Muscle Cells to Exercise and Regenerationa
Grounds, M. D. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb09894.x · Cited by 264 · see citing works
Effect of Age on Muscle Hypertrophy Induced by Resistance Training
Welle, S. L., Totterman, S. M. S., & Thornton, C. (1996) · The Journals of Gerontology Series A · doi:10.1093/gerona/51a.6.m270 · Cited by 247 · see citing works
VOLUNTARY ACTIVATION OF HUMAN MOTOR AXONS IN THE ABSENCE OF MUSCLE AFFERENT FEEDBACK
Gandevia, S. C., Macefield, V. G., Burke, D. J., & McKenzie, D. K. (1990) · Brain · doi:10.1093/brain/113.5.1563 · Cited by 244 · see citing works
Lipman, R. D., Chrisp, C. E., Hazzard, D. G., & Bronson, R. T. (1996) · The Journals of Gerontology Series A · doi:10.1093/gerona/51a.1.b54 · Cited by 242 · see citing works
Plasticity of myonuclear number in hypertrophied and atrophied mammalian skeletal muscle fibers
Allen, D. L., Monke, S. R., Talmadge, R. J., Roy, R. R., & Edgerton, V. R. (1995) · Journal of Applied Physiology · doi:10.1152/jappl.1995.78.5.1969 · Cited by 240 · see citing works
Isometric or dynamic training: differential effects on mechanical properties of a human muscle
Duchateau, J., & Hainaut, K. (1984) · Journal of Applied Physiology · doi:10.1152/jappl.1984.56.2.296 · Cited by 239 · see citing works
Contraction-induced injury: recovery of skeletal muscles in young and old mice
Brooks, S. V., & Faulkner, J. A. (1990) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1990.258.3.c436 · Cited by 238 · see citing works
Structural and functional responses to prolonged hindlimb suspension in rat muscle
Desplanches, D., Mayet, M. H., SEMPORE, B., et al. (1987) · Journal of Applied Physiology · doi:10.1152/jappl.1987.63.2.558 · Cited by 236 · see citing works
Suetta, C., Magnusson, S. P., Rosted, A., Aagaard, P., Jakobsen, A. K., Larsen, L. H., Duus, B. R., & Kjær, M. (2004) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2004.52557.x · Cited by 220 · see citing works
Self-citationApoptosis in muscle atrophy: Relevance to sarcopenia
Dupont‐Versteegden, E. E. (2005) · Experimental Gerontology · doi:10.1016/j.exger.2005.04.003 · Cited by 207 · see citing works
In vivo human muscle structure and function: adaptations to resistance training in old age
Reeves, N. D., Narici, M. V., & Maganaris, C. N. (2004) · Experimental Physiology · doi:10.1113/expphysiol.2004.027797 · Cited by 205 · see citing works
Molecular and cell biology of skeletal muscle regeneration
Grounds, M. D., & Yablonka‐Reuveni, Z. (1993) · Springer eBooks · doi:10.1007/978-94-011-1528-5_9 · Cited by 192 · see citing works
Population of Muscle Satellite Cells in Relation to Age and Mitotic Activity
Allbrook, D. B., Han, M., & Hellmuth, A. E. (1971) · Pathology · doi:10.1080/00313027109073739 · Cited by 192 · see citing works
In vivo specific tension of human skeletal muscle
Maganaris, C. N., Baltzopoulos, V., Ball, D., & Sargeant, A. J. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.90.3.865 · Cited by 192 · see citing works
Adaptations in maximal motor unit discharge rate to strength training in young and older adults
Patten, C., Kamen, G., & Rowland, D. M. (2001) · Muscle & Nerve · doi:10.1002/mus.1038 · Cited by 188 · see citing works
Suetta, C., Andersen, J. L., Dalgas, U., Berget, J., Koskinen, S., Aagaard, P., Magnusson, S. P., & Kjaer, M. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01354.2007 · Cited by 184 · see citing works
Self-citationMuscle function in elite master weightlifters
PEARSON, S. J., YOUNG, A., MACALUSO, A., DEVITO, G., NIMMO, M. A., COBBOLD, M., & HARRIDGE, S. D. R. (2002) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-200207000-00023 · Cited by 184 · see citing works
Ageing and Human Muscle: Observations From Sweden
Lexell, J. E. (1993) · Canadian Journal of Applied Physiology · doi:10.1139/h93-002 · Cited by 183 · see citing works
Factors contributing to neuromuscular impairment and sarcopenia during aging
Edström, E., Altun, M., Bergman, E., Johnson, H., Kullberg, S., Ramírez-León, V., & Ulfhake, B. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.05.040 · Cited by 181 · see citing works
Skeletal muscle regeneration and the mitotic clock
Renault, V. M., Piron-Hamelin, G., Forestier, C.-L., Donna, S. D., Decary, S., Hentati, F., Saillant, G., Butler-Browne, G. S., & Mouly, V. (2000) · Experimental Gerontology · doi:10.1016/s0531-5565(00)00151-0 · Cited by 179 · see citing works
Hikida, R. S., Gollnick, P. D., Dudley, G. A., Convertino, V. A., & Buchanan, P. (1989) · PubMed · Cited by 173 · see citing works
Apoptotic responses to hindlimb suspension in gastrocnemius muscles from young adult and aged rats
Siu, P. M., Pistilli, E. E., & Alway, S. E. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00198.2005 · Cited by 170 · see citing works
Hindlimb suspension suppresses muscle growth and satellite cell proliferation
Darr, K. C., & Schultz, E. (1989) · Journal of Applied Physiology · doi:10.1152/jappl.1989.67.5.1827 · Cited by 170 · see citing works
Effects of disuse on the structure and function of skeletal muscle
Booth, F. W., & Gollnick, P. D. (1983) · Medicine & Science in Sports & Exercise · doi:10.1249/00005768-198315050-00013 · Cited by 165 · see citing works
Activation of an adipogenic program in adult myoblasts with age
Taylor-Jones, J. M., McGehee, R. E., Rando, T. A., Lecka‐Czernik, B., Lipschitz, D. A., & Peterson, C. A. (2002) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(01)00411-0 · Cited by 165 · see citing works
Voluntary activation during maximal contraction with advancing age: a brief review
Klass, M., Baudry, S., & Duchateau, J. (2006) · European Journal of Applied Physiology · doi:10.1007/s00421-006-0205-x · Cited by 165 · see citing works
Suetta, C., Aagaard, P., Magnusson, S. P., Andersen, L. L., Sipilä, S., Rosted, A., Jakobsen, A. K. M., Duus, B. R., & Kjær, M. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00067.2006 · Cited by 165 · see citing works
Self-citationA muscle precursor cell-dependent pathway contributes to muscle growth after atrophy
Mitchell, P. O., & Pavlath, G. K. (2001) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2001.281.5.c1706 · Cited by 164 · see citing works
Early change in skeletal muscle protein synthesis after limb immobilization of rats
Booth, F. W., & Seider, M. J. (1979) · Journal of Applied Physiology · doi:10.1152/jappl.1979.47.5.974 · Cited by 163 · see citing works
Jacob, M. V., Pichler, P., Ryssel, H., & Falster, R. J. (1997) · Journal of Applied Physics · doi:10.1063/1.365796 · Cited by 159 · see citing works
Whitman, S. A., Wacker, M. J., Richmond, S. R., & Godard, M. P. (2005) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-005-1473-8 · Cited by 156 · see citing works
Mechanical Muscle Function, Morphology, and Fiber Type in Lifelong Trained Elderly
Aagaard, P., Magnusson, S. P., Larsson, B., Kjær, M., & Krustrup, P. (2007) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e31814fb402 · Cited by 149 · see citing works
Self-citationCellular and Molecular Basis of Age-Related Sarcopenia
Welle, S. L. (2002) · Canadian Journal of Applied Physiology · doi:10.1139/h02-002 · Cited by 145 · see citing works
Myogenic regulatory factors during regeneration of skeletal muscle in young, adult, and old rats
Marsh, D. R., Criswell, D. S., Carson, J. A., & Booth, F. W. (1997) · Journal of Applied Physiology · doi:10.1152/jappl.1997.83.4.1270 · Cited by 144 · see citing works
Plasticity of the Muscle-Tendon Complex With Disuse and Aging
Narici, M. V., & Maganaris, C. N. (2007) · Exercise and Sport Sciences Reviews · doi:10.1097/jes.0b013e3180a030ec · Cited by 142 · see citing works
Tibiofemoral joint forces during isokinetic knee extension
Nisell, R., Ericson, M. O., Németh, G., & Ekholm, J. (1989) · The American Journal of Sports Medicine · doi:10.1177/036354658901700108 · Cited by 133 · see citing works
Skeletal Muscle Adaptations with Age, Inactivity, and Therapeutic Exercise
Thompson, L. V. (2002) · Journal of Orthopaedic and Sports Physical Therapy · doi:10.2519/jospt.2002.32.2.44 · Cited by 130 · see citing works
Kim, J.-S., Kosek, D. J., Petrella, J. K., Cross, J. M., & Bamman, M. M. (2005) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00513.2005 · Cited by 128 · see citing works
Skeletal muscle function and hypertrophy are diminished in old age
Degens, H., & Alway, S. E. (2003) · Muscle & Nerve · doi:10.1002/mus.10314 · Cited by 125 · see citing works
Dupont‐Versteegden, E. E., Murphy, R. J. L., Houlé, J. D., Gurley, C. M., & Peterson, C. A. (1999) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1999.277.3.c589 · Cited by 125 · see citing works
Dupont‐Versteegden, E. E., Houlé, J. D., Gurley, C. M., & Peterson, C. A. (1998) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1998.275.4.c1124 · Cited by 122 · see citing works
Satellite cell regulation of muscle mass is altered at old age
Gallegly, J. C., Turesky, N. A., Strotman, B. A., Gurley, C. M., Peterson, C. A., & Dupont‐Versteegden, E. E. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00006.2004 · Cited by 114 · see citing works
Activation of Skeletal Muscle Satellite Cells and the Role of Fibroblast Growth Factor Receptors
Johnson, S., & Allen, R. E. (1995) · Experimental Cell Research · doi:10.1006/excr.1995.1251 · Cited by 103 · see citing works
Impaired Expression of Notch Signaling Genes in Aged Human Skeletal Muscle
Carey, K. A., Farnfield, M. M., Tarquinio, S. D., & Cameron‐Smith, D. (2007) · The Journals of Gerontology Series A · doi:10.1093/gerona/62.1.9 · Cited by 96 · see citing works
Denervation stimulates apoptosis but not Id2 expression in hindlimb muscles of aged rats
Alway, S. E., Degens, H., Krishnamurthy, G., & Chaudhrai, A. (2003) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/58.8.b687 · Cited by 96 · see citing works
Interleukin-15 responses to aging and unloading-induced skeletal muscle atrophy
Pistilli, E. E., Siu, P. M., & Alway, S. E. (2006) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00496.2006 · Cited by 80 · see citing works
Dupont‐Versteegden, E. E., Murphy, R. J. L., Houlé, J. D., Gurley, C. M., & Peterson, C. A. (2000) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.2000.279.6.c1677 · Cited by 78 · see citing works
MyoD and myogenin protein expression in skeletal muscles of senile rats
Dedkov, E. I., Kostrominova, T. Y., Borisov, A. B., & Carlson, B. M. (2003) · Cell and Tissue Research · doi:10.1007/s00441-002-0686-9 · Cited by 77 · see citing works
Patellar Forces During Knee Extension
Nisell, R., & Ekholm, J. (1985) · Journal of Rehabilitation Medicine · doi:10.2340/1650197785176374 · Cited by 67 · see citing works
Adaptations to Short-Term Muscle Unloading in Young and Aged Men
Deschenes, M. R., Holdren, A. N., & McCoy, R. W. (2008) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e318164f4b6 · Cited by 67 · see citing works
Pattison, J. S., Folk, L. C., Madsen, R., & Booth, F. W. (2003) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00500.2003 · Cited by 66 · see citing works
Alway, S. E., Lowe, D. A., & Chen, K. D. (2001) · Experimental Physiology · doi:10.1113/eph8602235 · Cited by 66 · see citing works
Contraction time, histochemical type, and terminal cisternae volume of rat motor units
Kugelberg, E., & Thornell, L. (1983) · Muscle & Nerve · doi:10.1002/mus.880060211 · Cited by 65 · see citing works
Carson, J. A., & Alway, S. E. (1996) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1996.270.2.c578 · Cited by 63 · see citing works
Single soleus muscle fiber function after hindlimb unweighting in adult and aged rats
Thompson, L. V., Johnson, S. A., & Shoeman, J. A. (1998) · Journal of Applied Physiology · doi:10.1152/jappl.1998.84.6.1937 · Cited by 62 · see citing works
Muscle Atrophy During Long Duration Bed Rest
LeBlanc, A., Rowe, R., Evans, H., West, S., Shackelford, L., & Schneider, V. (1997) · International Journal of Sports Medicine · doi:10.1055/s-2007-972726 · Cited by 58 · see citing works
Zarzhevsky, N., Carmeli, E., Fuchs, D., Coleman, R., Stein, H. J., & Reznick, A. Z. (2001) · Experimental Gerontology · doi:10.1016/s0531-5565(00)00189-3 · Cited by 57 · see citing works
Immobilization effects in young and older adults
Urso, M. L., Clarkson, P. M., & Price, T. B. (2005) · European Journal of Applied Physiology · doi:10.1007/s00421-005-0109-1 · Cited by 55 · see citing works
Mosoni, L., Malmezat, T., VALLUY, M.-C., Houlier, M. L., Attaix, D., & Mirand, P. P. (1999) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1999.277.4.e608 · Cited by 55 · see citing works
Alterations in skeletal muscle related to impaired physical mobility: An empirical model
Kasper, C. E., McNulty, A. L., Otto, A. J., & Thomas, D. P. (1993) · Research in Nursing & Health · doi:10.1002/nur.4770160405 · Cited by 51 · see citing works
Muscle adaptations to hindlimb suspension in mature and old Fischer 344 rats
Stump, C. S., Tipton, C. M., & Henriksen, E. J. (1997) · Journal of Applied Physiology · doi:10.1152/jappl.1997.82.6.1875 · Cited by 49 · see citing works
Pierotti, D. J., Roy, R. R., Flores, V., et al. (1990) · PubMed · Cited by 48 · see citing works
Capacity for Recovery and Possible Mechanisms in Immobilization Atrophy of Young and Old Animals
Zarzhevsky, N., Menashe, O., Carmeli, E., Stein, H. J., & Reznick, A. Z. (2001) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2001.tb05651.x · Cited by 46 · see citing works
A comparison of the effects of unloading in young adult and aged skeletal muscle
Deschenes, M. R., Britt, A. A., & CHANDLER, W. C. (2001) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-200109000-00009 · Cited by 46 · see citing works
Alley, K. A., & Thompson, L. V. (1997) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/s0003-9993(97)90004-6 · Cited by 46 · see citing works
Morphometric analyses on the muscles of exercise trained and untrained dogs
Čabrić, M., & James, N. T. (1983) · American Journal of Anatomy · doi:10.1002/aja.1001660309 · Cited by 44 · see citing works
Massive Nitrogen Loss in Critical Surgical Illness
Hill, A. A. V., Plank, L. D., Finn, P., WHALLEY, G. A., Sharpe, N., Clark, M. A., & Hill, G. L. (1997) · Annals of Surgery · doi:10.1097/00000658-199708000-00011 · Cited by 43 · see citing works
Widrick, J. J., Bangart, J. J., Karhánek, M., et al. (1996) · Journal of Applied Physiology · doi:10.1152/jappl.1996.80.3.981 · Cited by 41 · see citing works
Dodson, M. V., & Allen, R. E. (1987) · Mechanisms of Ageing and Development · doi:10.1016/0047-6374(87)90003-0 · Cited by 41 · see citing works
Intermittent acceleration as a countermeasure to soleus muscle atrophy
D'Aunno, D. S., Robinson, R. R., Smith, G. S., Thomason, D. B., & Booth, F. W. (1992) · Journal of Applied Physiology · doi:10.1152/jappl.1992.72.2.428 · Cited by 40 · see citing works
Effects of lengthening contraction on calcium kinetics and skeletal muscle contractility in humans
Nielsen, J. S., Madsen, K., Jørgensen, L. V., & Sahlin, K. (2005) · Acta Physiologica Scandinavica · doi:10.1111/j.1365-201x.2005.01449.x · Cited by 37 · see citing works
Bonavaud, S. M., Thibert, P., Gherardi, R. K., et al. (1997) · Biology of the Cell · doi:10.1111/j.1768-322x.1997.tb01011.x · Cited by 35 · see citing works
Nucleo-cytoplasmic ratio in ageing skeletal muscle
Manta, P., Vassilopoulos, D., & Spengos, M. N. (1987) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/bf00383854 · Cited by 33 · see citing works
Natural Occurrence of Myofiber Cytoplasmic Enlargement Accompanied by Decrease in Myonuclear Number
Wada, K., Katsuta, S., & Soya, H. (2003) · The Japanese Journal of Physiology · doi:10.2170/jjphysiol.53.145 · Cited by 29 · see citing works
Bangart, J. J., Widrick, J. J., & Fitts, R. H. (1997) · Journal of Applied Physiology · doi:10.1152/jappl.1997.82.6.1905 · Cited by 29 · see citing works
Karyometric Changes in Human Muscle with Age
Vassilopoulos, D., Lumb, E. M., & Emery, A. E. H. (2008) · European Neurology · doi:10.1159/000114877 · Cited by 27 · see citing works
Simard, C., Lacaille, M., & Vallières, J. (1987) · Experimental Neurology · doi:10.1016/0014-4886(87)90285-8 · Cited by 27 · see citing works
Differential effects of reduced muscle use (hindlimb unweighting) on skeletal muscle with aging
Brown, M., & Hasser, E. M. (1996) · Aging Clinical and Experimental Research · doi:10.1007/bf03339562 · Cited by 26 · see citing works
Aging alters the reduction of pro-apoptotic signaling in response to loading-induced hypertrophy
Siu, P. M., & Alway, S. E. (2006) · Experimental Gerontology · doi:10.1016/j.exger.2005.11.004 · Cited by 24 · see citing works
Contractile function of single muscle fibers after hindlimb unweighting in aged rats
Thompson, L. V., & Shoeman, J. A. (1998) · Journal of Applied Physiology · doi:10.1152/jappl.1998.84.1.229 · Cited by 23 · see citing works
Welle, S. L., & Thornton, C. A. (1997) · Journal of Endocrinology · doi:10.1677/joe.0.1550093 · Cited by 21 · see citing works
Cell Culture Systems as Tools for Studying Age-Related Changes in Skeletal Muscle
Holloszy, J. O., & Peterson, C. A. (1995) · The Journals of Gerontology Series A · doi:10.1093/gerona/50a.special_issue.142 · Cited by 16 · see citing works
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Sarcopenia: Aging-Related Loss of Muscle Mass and Function
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Booth, F. W., Roberts, C. K., Thyfault, J. P., Ruegsegger, G. N., & Toedebusch, R. G. (2017) · Physiological Reviews · doi:10.1152/physrev.00019.2016 · Cited by 696 · see citing works
Aagaard, P., Suetta, C., Caserotti, P., Magnusson, S. P., & Kjær, M. (2010) · Scandinavian Journal of Medicine & Science in Sports · doi:10.1111/j.1600-0838.2009.01084.x · Cited by 709 · see citing works
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Wall, B. T., Dirks, M. L., & van Loon, L. J. C. (2013) · Ageing Research Reviews · doi:10.1016/j.arr.2013.07.003 · Cited by 400 · see citing works
Breen, L., Stokes, K. A., Churchward-Venne, T. A., Moore, D. R., Baker, S. K., Smith, K., Atherton, P. J., & Phillips, S. M. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-1502 · Cited by 395 · see citing works
Tanner, R. E., Brunker, L. B., Agergaard, J., Barrows, K. M., Briggs, R. A., Kwon, O. S., Young, L. M., Hopkins, P. N., Volpi, E., Marcus, R. L., et al. (2015) · The Journal of Physiology · doi:10.1113/jp270699 · Cited by 223 · see citing works
Hvid, L., Aagaard, P., Justesen, L., Bayer, M. L., Andersen, J. L., Ørtenblad, N., Kjaer, M., & Suetta, C. (2010) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00637.2010 · Cited by 195 · see citing works
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Hao, Y., Jackson, J. R., Wang, Y., Edens, N., Pereira, S. L., & Alway, S. E. (2011) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00840.2010 · Cited by 124 · see citing works
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Bennett, B. T., Mohamed, J. S., & Alway, S. E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0083518 · Cited by 116 · see citing works
Alway, S. E., Pereira, S. L., Edens, N. K., Hao, Y., & Bennett, B. T. (2013) · Experimental Gerontology · doi:10.1016/j.exger.2013.06.005 · Cited by 114 · see citing works
Devries, M. C., Breen, L., Von Allmen, M., MacDonald, M. J., Moore, D. R., Offord, E. A., Horcajada, M.-N., Breuillé, D., & Phillips, S. M. (2015) · Physiological Reports · doi:10.14814/phy2.12493 · Cited by 107 · see citing works
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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 · see citing works
Effect of bimagrumab on thigh muscle volume and composition in men with casting‐induced atrophy
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Backx, E. M. P., Hangelbroek, R., Snijders, T., Verscheijden, M.-L., Verdijk, L. B., de Groot, L. C. P. G. M., & van Loon, L. J. C. (2017) · Sports Medicine · doi:10.1007/s40279-016-0670-2 · Cited by 61 · see citing works
Wall, B. T., Dirks, M. L., Snijders, T., Stephens, F. B., Senden, J. M. G., Verscheijden, M.-L., & van Loon, L. J. C. (2015) · Experimental Gerontology · doi:10.1016/j.exger.2014.11.019 · Cited by 52 · see citing works
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Lynch, G. M., Murphy, C. H., Castro, E. D. M., & Roche, H. M. (2020) · Proceedings of the Nutrition Society · doi:10.1017/s0029665120007119 · Cited by 41 · see citing works
Martins, A. D., Fernandes, O., Pereira, A., Oliveira, R., Alderete Goñi, F. D., Leite, N. J. C., & Brito, J. P. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph19095390 · Cited by 24 · see citing works
Drummond, M. J., Marcus, R. L., & LaStayo, P. C. (2012) · Journal of Aging Research · doi:10.1155/2012/486930 · Cited by 28 · see citing works
Fully Automated Analysis of Muscle Architecture from B-Mode Ultrasound Images with DL_Track_US
Ritsche, P., Franchi, M. V., Faude, O., Finni, T., Seynnes, O., & Cronin, N. J. (2024) · Ultrasound in Medicine & Biology · doi:10.1016/j.ultrasmedbio.2023.10.011 · Cited by 20 · see citing works
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Goswami, N., Blaber, A. P., Valenti, G., Hinghofer-Szalkay, H., Evans, J., Bailey, D. M., Vernikos, J., Choukér, A., Green, D. A., White, O., et al. (2026) · Physiological Reviews · doi:10.1152/physrev.00055.2024 · Cited by 25 · see citing works
Vigelsø, A., Gram, M., Wiuff, C., Hansen, C. N., Prats, C., Dela, F., & Helge, J. W. (2016) · European Journal of Applied Physiology · doi:10.1007/s00421-015-3302-x · Cited by 13 · see citing works
- Authors
- Suetta, C., Hvid, L. G., Justesen, L., Christensen, U., Neergaard, K., Simonsen, L., Ortenblad, N., Magnusson, S. P., Kjaer, M., & Aagaard, P.
- Affiliations
- University of Copenhagen (DK)
- Institute of Sports Sciences and Clinical Biomechanics, University of Southern Denmark; and
- Institute of Sports Medicine and Centre of Healthy Aging, Faculty of Health Science, University of Copenhagen, Bispebjerg Hospital;
- University of Southern Denmark (DK)
- Corresponding author
- Suetta, C.
- Venue
- Journal of Applied Physiology
- Publisher
- American Physiological Society
- Published
- 2009-10
- Volume
- 107
- Issue
- 4
- Pages
- 1172-1180
- ISSN
- 0161-7567 (ISSN-L)
- 8750-7587
- 1522-1601
- OpenAlex
- W2104683776
- Cited by
- 400
- References
- 133
- Citations by year
- 2026: 20 · 2025: 21 · 2024: 23 · 2023: 41 · 2022: 25 · 2021: 26 · 2020: 30 · 2019: 34 · 2018: 23 · 2017: 28 · 2016: 22 · 2015: 22 · 2014: 14 · 2013: 34 · 2012: 17
- FWCI
- 4.94
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Applied Physiology (publishedVersion)
- PubMed (publishedVersion)
- University of Southern Denmark Research Portal (University of Southern Denmark) (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Health Sciences › Medicine › Physiology › Nutrition and Health in Aging
- Health Sciences › Medicine › Physiology › Spaceflight effects on biology
- Keywords
- aging, skeletal muscle, immobilization, disuse, retraining, sarcopenia, muscle strength, specific force, quadriceps, pennation angle, muscle volume, twitch response, muscle activation, older men
- MeSH terms
- Adult, Age Factors, Aged, Aging, Electric Stimulation, Humans, Immobilization, Male, Middle Aged, Motor Neurons, Muscle Contraction, Neuromuscular Junction, Organ Size, Time Factors, Muscle Weakness, Torque, Recovery of Function, Physical Therapy Modalities, Quadriceps Muscle, Muscle Strength, Young Adult, Sarcopenia
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
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