A single bout of prior resistance exercise attenuates muscle atrophy and declines in myofibrillar protein synthesis during bed-rest in older men.
disuse
exercise training
muscle anabolism
sarcopenia
Journal
The Journal of physiology
ISSN: 1469-7793
Titre abrégé: J Physiol
Pays: England
ID NLM: 0266262
Informations de publication
Date de publication:
19 Oct 2023
19 Oct 2023
Historique:
received:
14
07
2023
accepted:
05
10
2023
medline:
19
10
2023
pubmed:
19
10
2023
entrez:
19
10
2023
Statut:
aheadofprint
Résumé
Impairments in myofibrillar protein synthesis (MyoPS) during bed rest accelerate skeletal muscle loss in older adults, increasing the risk of adverse secondary health outcomes. We investigated the effect of prior resistance exercise (RE) on MyoPS and muscle morphology during a disuse event in 10 healthy older men (65-80 years). Participants completed a single bout of unilateral leg RE the evening prior to 5 days of in-patient bed-rest. Quadriceps cross-sectional area (CSA) was determined prior to and following bed-rest. Serial muscle biopsies and dual stable isotope tracers were used to determine rates of integrated MyoPS (iMyoPS) over a 7 day habitual 'free-living' phase and the bed-rest phase, and rates of acute postabsorptive and postprandial MyoPS (aMyoPS) at the end of bed rest. Quadriceps CSA at 40%, 60% and 80% of muscle length significantly decreased in exercised (EX) and non-exercised control (CTL) legs with bed-rest. The decline in quadriceps CSA at 40% and 60% of muscle length was attenuated in EX compared with CTL. During bed-rest, iMyoPS rates decreased from habitual values in CTL, but not EX, and were significantly different between legs. Postprandial aMyoPS rates increased above postabsorptive values in EX only. The change in iMyoPS over bed-rest correlated with the change in quadriceps CSA in CTL, but not EX. A single bout of RE attenuated the decline in iMyoPS rates and quadriceps atrophy with 5 days of bed-rest in older men. Further work is required to understand the functional and clinical implications of prior RE in older patient populations. KEY POINTS: Age-related skeletal muscle deterioration, linked to numerous adverse health outcomes, is driven by impairments in muscle protein synthesis that are accelerated during periods of disuse. Resistance exercise can stimulate muscle protein synthesis over several days of recovery and therefore could counteract impairments in this process that occur in the early phase of disuse. In the present study, we demonstrate that the decline in myofibrillar protein synthesis and muscle atrophy over 5 days of bed-rest in older men was attenuated by a single bout of unilateral resistance exercise performed the evening prior to bed-rest. These findings suggest that concise resistance exercise intervention holds the potential to support muscle mass retention in older individuals during short-term disuse, with implications for delaying sarcopenia progression in ageing populations.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/N018214/1
Pays : United Kingdom
Informations de copyright
© 2023 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society.
Références
Baker, C. (2020). NHS key statistics: England, February 2020, (pp. 31). House of Commons Library.
Balshaw, T. G., Fry, A., Maden-Wilkinson, T. M., Kong, P. W., & Folland, J. P. (2017). Reliability of quadriceps surface electromyography measurements is improved by two vs. single site recordings. European Journal of Applied Physiology, 117(6), 1085-1094.
Bergstrom, J. (1975). Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scandinavian Journal of Clinical and Laboratory Investigation, 35(7), 609-616.
Biolo, G., Maggi, S. P., Williams, B. D., Tipton, K. D., & Wolfe, R. R. (1995). Increased rates of muscle protein turnover and amino acid transport after resistance exercise in humans. American Journal of Physiology, 268(3 Pt 1), E514-E520.
Breen, L., & Phillips, S. M. (2011). Skeletal muscle protein metabolism in the elderly: Interventions to counteract the ‘anabolic resistance’ of ageing. Nutrition Metabolism (Lond), 8(1), 68.
Breen, L., Stokes, K. A., Churchward-Venne, T. A., Moore, D. R., Baker, S. K., Smith, K., Atherton, P. J., & Phillips, S. M. (2013). Two weeks of reduced activity decreases leg lean mass and induces “anabolic resistance” of myofibrillar protein synthesis in healthy elderly. Journal of Clinical Endocrinology and Metabolism, 98(6), 2604-2612.
Brook, M. S., Stokes, T., Gorissen, S. H. M., Bass, J. J., McGlory, C., Cegielski, J., Wilkinson, D. J., Phillips, B. E., Smith, K., Phillips, S. M., & Atherton, P. J. (2022). Declines in muscle protein synthesis account for short-term muscle disuse atrophy in humans in the absence of increased muscle protein breakdown. Journal of Cachexia, Sarcopenia and Muscle, 13(4), 2005-2016.
Brown, C. J., Redden, D. T., Flood, K. L., & Allman, R. M. (2009). The underrecognized epidemic of low mobility during hospitalization of older adults. Journal of the American Geriatrics Society, 57(9), 1660-1665.
Buckley, J. P., & Borg, G. A. (2011). Borg's scales in strength training; from theory to practice in young and older adults. Applied Physiology, Nutrition and Metabolism, 36(5), 682-692.
Burd, N. A., Pennings, B., Groen, B. B., Gijsen, A. P., Senden, J. M., & van Loon, L. J. (2012). The single biopsy approach is reliable for the measurement of muscle protein synthesis rates in vivo in older men. Journal of Applied Physiology (Bethesda, Md : 1985), 113(6), 896-902.
Burd, N. A., West, D. W., Moore, D. R., Atherton, P. J., Staples, A. W., Prior, T., Tang, J. E., Rennie, M. J., Baker, S. K., & Phillips, S. M. (2011). Enhanced amino acid sensitivity of myofibrillar protein synthesis persists for up to 24 h after resistance exercise in young men. Journal of Nutrition, 141(4), 568-573.
Carli, F., & Zavorsky, G. S. (2005). Optimizing functional exercise capacity in the elderly surgical population. Current Opinion in Clinical Nutrition and Metabolic Care, 8(1), 23-32.
Covinsky, K. E., Justice, A. C., Rosenthal, G. E., Palmer, R. M., & Landefeld, C. S. (1997). Measuring prognosis and case mix in hospitalized elders. The importance of functional status. Journal of General Internal Medicine, 12(4), 203-208.
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 Journal, 19(3), 1-22.
Damas, F., Phillips, S. M., Libardi, C. A., Vechin, F. C., Lixandrao, M. E., Jannig, P. R., Costa, L. A., Bacurau, A. V., Snijders, T., Parise, G., Tricoli, V., Roschel, H., & Ugrinowitsch, C. (2016). Resistance training-induced changes in integrated myofibrillar protein synthesis are related to hypertrophy only after attenuation of muscle damage. The Journal of Physiology, 594(18), 5209-5222.
Di Girolamo, F. G., Fiotti, N., Milanovic, Z., Situlin, R., Mearelli, F., Vinci, P., Simunic, B., Pisot, R., Narici, M., & Biolo, G. (2021). The aging muscle in experimental bed rest: A systematic review and meta-analysis. Frontiers in Nutrition, 8, 633987.
Dirks, M. L., Wall, B. T., Nilwik, R., Weerts, D. H., Verdijk, L. B., & van Loon, L. J. (2014). Skeletal muscle disuse atrophy is not attenuated by dietary protein supplementation in healthy older men. Journal of Nutrition, 144(8), 1196-1203.
Dourado, M. A. A., Vieira, D. C. L., Boullosa, D., & Bottaro, M. (2023). Different time course recovery of muscle edema within the quadriceps femoris and functional performance after single- vs multi-joint exercises. Biology Sport, 40(3), 767-774.
Drummond, M. J., Dickinson, J. M., Fry, C. S., Walker, D. K., Gundermann, D. M., Reidy, P. T., Timmerman, K. L., Markofski, M. M., Paddon-Jones, D., Rasmussen, B. B., & Volpi, E. (2012). Bed rest impairs skeletal muscle amino acid transporter expression, mTORC1 signaling, and protein synthesis in response to essential amino acids in older adults. American Journal of Physiology. Endocrinology and Metabolism, 302(9), E1113-E1122.
Ema, R., Wakahara, T., Miyamoto, N., Kanehisa, H., & Kawakami, Y. (2013). Inhomogeneous architectural changes of the quadriceps femoris induced by resistance training. European Journal of Applied Physiology, 113(11), 2691-2703.
English, K. L., Mettler, J. A., Ellison, J. B., Mamerow, M. M., Arentson-Lantz, E., Pattarini, J. M., Ploutz-Snyder, R., Sheffield-Moore, M., & Paddon-Jones, D. (2016). Leucine partially protects muscle mass and function during bed rest in middle-aged adults. American Journal of Clinical Nutrition, 103(2), 465-473.
Ethgen, O., Beaudart, C., Buckinx, F., Bruyere, O., & Reginster, J. Y. (2017). The future prevalence of sarcopenia in Europe: A claim for public health action. Calcified Tissue International, 100(3), 229-234.
Fernandes, J. F. T., Lamb, K. L., Norris, J. P., Moran, J., Drury, B., Borges, N. R., & Twist, C. (2021). Aging and recovery after resistance-exercise-induced muscle damage: current evidence and implications for future research. Journal of Aging and Physical Activity, 29(3), 544-551.
Fisher, S. R., Goodwin, J. S., Protas, E. J., Kuo, Y. F., Graham, J. E., Ottenbacher, K. J., & Ostir, G. V. (2011). Ambulatory activity of older adults hospitalized with acute medical illness. Journal of the American Geriatrics Society, 59(1), 91-95.
Fortinsky, R. H., Covinsky, K. E., Palmer, R. M., & Landefeld, C. S. (1999). Effects of functional status changes before and during hospitalization on nursing home admission of older adults. Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 54(10), M521-M526.
Fragala, M. S., Cadore, E. L., Dorgo, S., Izquierdo, M., Kraemer, W. J., Peterson, M. D., & Ryan, E. D. (2019). Resistance training for older adults: position statement from the national strength and conditioning association. Journal of Strength and Conditioning Research, 33(8), 2019-2052.
Goates, S., Du, K., Arensberg, M. B., Gaillard, T., Guralnik, J., & Pereira, S. L. (2019). Economic impact of hospitalizations in US adults with sarcopenia. Journal of Frailty Aging, 8(2), 93-99.
Hardy, E. J. O., Inns, T. B., Hatt, J., Doleman, B., Bass, J. J., Atherton, P. J., Lund, J. N., & Phillips, B. E. (2022). The time course of disuse muscle atrophy of the lower limb in health and disease. Journal of Cachexia, Sarcopenia and Muscle, 13(6), 2616-2629.
Horwath, O., Envall, H., Roja, J., Emanuelsson, E. B., Sanz, G., Ekblom, B., Apro, W., & Moberg, M. (2021). Variability in vastus lateralis fiber type distribution, fiber size, and myonuclear content along and between the legs. Journal of Applied Physiology (1985), 131(1), 158-173.
Jameson, T. S. O., Kilroe, S. P., Fulford, J., Abdelrahman, D. R., Murton, A. J., Dirks, M. L., Stephens, F. B., & Wall, B. T. (2021). Muscle damaging eccentric exercise attenuates disuse-induced declines in daily myofibrillar protein synthesis and transiently prevents muscle atrophy in healthy men. American Journal of Physiology-Endocrinology and Metabolism, 321(5), E674-E688.
Kilroe, S. P., Fulford, J., Holwerda, A. M., Jackman, S. R., Lee, B. P., Gijsen, A. P., van Loon, L. J. C., & Wall, B. T. (2019). Short-term muscle disuse induces a rapid and sustained decline in daily myofibrillar protein synthesis rates. American Journal of Physiology-Endocrinology and Metabolism, 318(2), E117-E130.
Kortebein, P., Ferrando, A., Lombeida, J., Wolfe, R., & Evans, W. J. (2007). Effect of 10 days of bed rest on skeletal muscle in healthy older adults. Journal of the American Medical Association, 297(16), 1772-1774.
Kumar, V., Atherton, P. J., Selby, A., Rankin, D., Williams, J., Smith, K., Hiscock, N., & Rennie, M. J. (2012). Muscle protein synthetic responses to exercise: Effects of age, volume, and intensity. Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 67(11), 1170-1177.
Lee, J., Hong, Y. P., Shin, H. J., & Lee, W. (2016). Associations of sarcopenia and sarcopenic obesity with metabolic syndrome considering both muscle mass and muscle strength. Journal of preventive medicine and public health = Yebang Uihakhoe chi, 49(1), 35-44.
Loyd, C., Beasley, T. M., Miltner, R. S., Clark, D., King, B., & Brown, C. J. (2018). Trajectories of community mobility recovery after hospitalization in older adults. Journal of the American Geriatrics Society, 66(7), 1399-1403.
Marusic, U., Narici, M., Simunic, B., Pisot, R., & Ritzmann, R. (2021). Nonuniform loss of muscle strength and atrophy during bed rest: A systematic review. Journal of Applied Physiology (1985), 131(1), 194-206.
McFarlane, C., Plummer, E., Thomas, M., Hennebry, A., Ashby, M., Ling, N., Smith, H., Sharma, M., & Kambadur, R. (2006). Myostatin induces cachexia by activating the ubiquitin proteolytic system through an NF-kappaB-independent, FoxO1-dependent mechanism. Journal of Cellular Physiology, 209(2), 501-514.
McGlory, C., von Allmen, M. T., Stokes, T., Morton, R. W., Hector, A. J., Lago, B. A., Raphenya, A. R., Smith, B. K., McArthur, A. G., Steinberg, G. R., Baker, S. K., & Phillips, S. M. (2018). Failed Recovery of glycemic control and myofibrillar protein synthesis with 2 wk of physical inactivity in overweight, prediabetic older adults. Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 73(8), 1070-1077.
McKendry, J., Shad, B. J., Smeuninx, B., Oikawa, S. Y., Wallis, G., Greig, C., Phillips, S. M., & Breen, L. (2019). Comparable rates of integrated myofibrillar protein synthesis between endurance-trained master athletes and untrained older individuals. Frontiers in Physiology, 10, 1084.
Miller, B. F., Olesen, J. L., Hansen, M., Dossing, S., Crameri, R. M., Welling, R. J., Langberg, H., Flyvbjerg, A., Kjaer, M., Babraj, J. A., Smith, K., & Rennie, M. J. (2005). Coordinated collagen and muscle protein synthesis in human patella tendon and quadriceps muscle after exercise. The Journal of Physiology, 567(3), 1021-1033.
Moore, D. R., Churchward-Venne, T. A., Witard, O., Breen, L., Burd, N. A., Tipton, K. D., & Phillips, S. M. (2015). Protein ingestion to stimulate myofibrillar protein synthesis requires greater relative protein intakes in healthy older versus younger men. Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 70(1), 57-62.
Narici, M. V., Hoppeler, H., Kayser, B., Landoni, L., Claassen, H., Gavardi, C., Conti, M., & Cerretelli, P. (1996). Human quadriceps cross-sectional area, torque and neural activation during 6 months strength training. Acta Physiologica Scandinavica, 157(2), 175-186.
Ostir, G. V., Berges, I. M., Kuo, Y. F., Goodwin, J. S., Fisher, S. R., & Guralnik, J. M. (2013). Mobility activity and its value as a prognostic indicator of survival in hospitalized older adults. Journal of the American Geriatrics Society, 61(4), 551-557.
Papalia, R., Zampogna, B., Torre, G., Papalia, G. F., Vorini, F., Bravi, M., Albo, E., De Vincentis, A., & Denaro, V. (2021). Preoperative and perioperative predictors of length of hospital stay after primary total hip arthroplasty-our experience on 743 cases. Journal of Clinical Medicine, 10(21), 5053.
Pennings, B., Koopman, R., Beelen, M., Senden, J. M., Saris, W. H., & van Loon, L. J. (2011). Exercising before protein intake allows for greater use of dietary protein-derived amino acids for de novo muscle protein synthesis in both young and elderly men. American Journal of Clinical Nutrition, 93(2), 322-331.
Phillips, S. M., Tipton, K. D., Aarsland, A., Wolf, S. E., & Wolfe, R. R. (1997). Mixed muscle protein synthesis and breakdown after resistance exercise in humans. American Journal of Physiology, 273(1 Pt 1), E99-E107.
Prado, C. M., Purcell, S. A., Alish, C., Pereira, S. L., Deutz, N. E., Heyland, D. K., Goodpaster, B. H., Tappenden, K. A., & Heymsfield, S. B. (2018). Implications of low muscle mass across the continuum of care: A narrative review. Annals of Medicine, 50(8), 675-693.
Reidy, P. T., McKenzie, A. I., Brunker, P., Nelson, D. S., Barrows, K. M., Supiano, M., LaStayo, P. C., & Drummond, M. J. (2017). Neuromuscular electrical stimulation combined with protein ingestion preserves thigh muscle mass but not muscle function in healthy older adults during 5 days of bed rest. Rejuvenation Research, 20(6), 449-461.
Rejc, E., Floreani, M., Taboga, P., Botter, A., Toniolo, L., Cancellara, L., Narici, M., Simunic, B., Pisot, R., Biolo, G., Passaro, A., Rittweger, J., Reggiani, C., & Lazzer, S. (2018). Loss of maximal explosive power of lower limbs after 2 weeks of disuse and incomplete recovery after retraining in older adults. The Journal of Physiology, 596(4), 647-665.
Rezus, E., Burlui, A., Cardoneanu, A., Rezus, C., Codreanu, C., Parvu, M., Rusu Zota, G., & Tamba, B. I. (2020). Inactivity and skeletal muscle metabolism: A vicious cycle in old age. International Journal of Molecular Sciences, 21(2), 592.
Sallis, R., Roddy-Sturm, Y., Chijioke, E., Litman, K., Kanter, M. H., Huang, B. Z., Shen, E., & Nguyen, H. Q. (2015). Stepping toward discharge: Level of ambulation in hospitalized patients. Journal of Hospital Medicine, 10(6), 384-389.
Shad, B. J., Thompson, J. L., & Breen, L. (2016). Does the muscle protein synthetic response to exercise and amino acid-based nutrition diminish with advancing age? A systematic review. American Journal of Physiology. Endocrinology and Metabolism, 311(5), E803-E817.
Shad, B. J., Thompson, J. L., Holwerda, A. M., Stocks, B., Elhassan, Y. S., Philp, A., LJC, V., & Wallis, G. A. (2019). One week of step reduction lowers myofibrillar protein synthesis rates in young men. Medicine and Science in Sports and Exercise, 51(10), 2125-2134.
Smeuninx, B., Elhassan, Y. S., Manolopoulos, K. N., Sapey, E., Rushton, A. B., Edwards, S. J., Morgan, P. T., Philp, A., Brook, M. S., Gharahdaghi, N., Smith, K., Atherton, P. J., & Breen, L. (2021). The effect of short-term exercise prehabilitation on skeletal muscle protein synthesis and atrophy during bed rest in older men. Journal of Cachexia, Sarcopenia and Muscle, 12(1), 52-69.
Smeuninx, B., McKendry, J., Wilson, D., Martin, U., & Breen, L. (2017). Age-related anabolic resistance of myofibrillar protein synthesis is exacerbated in obese inactive individuals. Journal of Clinical Endocrinology and Metabolism, 102(9), 3535-3545.
Sousa, A. S., Guerra, R. S., Fonseca, I., Pichel, F., & Amaral, T. F. (2016). Sarcopenia and length of hospital stay. European Journal of Clinical Nutrition, 70(5), 595-601.
Steffl, M., Sima, J., Shiells, K., & Holmerova, I. (2017). The increase in health care costs associated with muscle weakness in older people without long-term illnesses in the Czech Republic: Results from the Survey of Health, Ageing and Retirement in Europe (SHARE). CIA, 12, 2003-2007.
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. Journal of Applied Physiology (1985), 107(4), 1172-1180.
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., LaStayo, P. C., & Drummond, M. J. (2015). Age-related differences in lean mass, protein synthesis and skeletal muscle markers of proteolysis after bed rest and exercise rehabilitation. The Journal of Physiology, 593(18), 4259-4273.
Veronese, N., Demurtas, J., Soysal, P., Smith, L., Torbahn, G., Schoene, D., Schwingshackl, L., Sieber, C., Bauer, J., Cesari, M., Bruyere, O., Reginster, J.-Y., Beaudart, C., Cruz-Jentoft, A. J., Cooper, C., Petrovic, M., & Maggi, S., & Reviews tSIGiS, Sarcopenia M-afha, Frailty & Society riopotEGM. (2019). Sarcopenia and health-related outcomes: An umbrella review of observational studies. European Geriatric Medicine, 10(6), 853-862.
Wall, B. T., Dirks, M. L., Snijders, T., Senden, J. M., Dolmans, J., & van Loon, L. J. (2014). Substantial skeletal muscle loss occurs during only 5 days of disuse. Acta Physiologica (Oxf), 210(3), 600-611.
Wilkinson, D. J., Franchi, M. V., Brook, M. S., Narici, M. V., Williams, J. P., Mitchell, W. K., Szewczyk, N. J., Greenhaff, P. L., Atherton, P. J., & Smith, K. (2014). A validation of the application of D(2)O stable isotope tracer techniques for monitoring day-to-day changes in muscle protein subfraction synthesis in humans. American journal of physiology Endocrinology and metabolism, 306(5), E571-E579.
Wilkinson, S. B., Phillips, S. M., Atherton, P. J., Patel, R., Yarasheski, K. E., Tarnopolsky, M. A., & Rennie, M. J. (2008). Differential effects of resistance and endurance exercise in the fed state on signalling molecule phosphorylation and protein synthesis in human muscle. The Journal of Physiology, 586(15), 3701-3717.
Yang, Y., Breen, L., Burd, N. A., Hector, A. J., Churchward-Venne, T. A., Josse, A. R., Tarnopolsky, M. A., & Phillips, S. M. (2012). Resistance exercise enhances myofibrillar protein synthesis with graded intakes of whey protein in older men. British Journal of Nutrition, 108(10), 1780-1788.
Zhu, S., Qian, W., Jiang, C., Ye, C., & Chen, X. (2017). Enhanced recovery after surgery for hip and knee arthroplasty: A systematic review and meta-analysis. Postgraduate Medical Journal, 93(1106), 736-742.