Five days of bed rest in young and old adults: Retainment of skeletal muscle mass with neuromuscular electrical stimulation.


Journal

Physiological reports
ISSN: 2051-817X
Titre abrégé: Physiol Rep
Pays: United States
ID NLM: 101607800

Informations de publication

Date de publication:
Aug 2024
Historique:
revised: 01 07 2024
received: 30 04 2024
accepted: 17 07 2024
medline: 19 8 2024
pubmed: 19 8 2024
entrez: 18 8 2024
Statut: ppublish

Résumé

The consequences of short-term disuse are well known, but effective countermeasures remain elusive. This study investigated the effects of neuromuscular electrical stimulation (NMES) during 5 days of bed rest on retaining lower limb muscle mass and muscle function in healthy young and old participants. One leg received NMES of the quadriceps muscle (3 × 30min/day) (NMES), and the other served as a control (CON). Isometric quadriceps strength (MVC), rate of force development (RFD), lower limb lean mass, and muscle thickness were assessed pre-and post-intervention. Muscle thickness remained unaltered with NMES in young and increased in old following bed rest, while it decreased in CON legs. In old participants, mid-thigh lean mass (MTLM) was preserved with NMES while decreased in CON legs. In the young, only a tendency to change with bed rest was detected for MTLM. MVC and early-phase RFD decreased in young and old, irrespective of NMES. In contrast, late-phase RFD was retained in young participants with NMES, while it decreased in young CON legs, and in the old, irrespective of NMES. NMES during short-term bed rest preserved muscle thickness but not maximal muscle strength. While young and old adults demonstrated similar adaptive responses in preventing the loss of skeletal muscle thickness, RFD was retained in the young only.

Identifiants

pubmed: 39155274
doi: 10.14814/phy2.16166
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e16166

Subventions

Organisme : Helsefonden (Health Foundation)
ID : 22-B-0038

Informations de copyright

© 2024 The Author(s). Physiological Reports published by Wiley Periodicals LLC on behalf of The Physiological Society and the American Physiological Society.

Références

Aagaard, P., Simonsen, E. B., Andersen, J. L., Magnusson, P., & Dyhre‐Poulsen, P. (2002). Increased rate of force development and neural drive of human skeletal muscle following resistance training. Journal of Applied Physiology, 93, 1318–1326.
Alqurashi, H. B., Robinson, K., O'Connor, D., Piasecki, M., Gordon, A. L., Masud, T., & Gladman, J. R. F. (2023). The effects of neuromuscular electrical stimulation on hospitalised adults: Systematic review and meta‐analysis of randomised controlled trials. Age and Ageing, 52, 1–13.
Bamman, M. M., Clarke, M. S. F., Feeback, D. L., Talmadge, R. J., Stevens, B. R., Lieberman, S. A., & Greenisen, M. C. (1998). Impact of resistance exercise during bed rest on skeletal muscle sarcopenia and myosin isoform distribution. Journal of Applied Physiology, 84, 157–163.
Bickel, C. S., Gregory, C. M., & Dean, J. C. (2011). Motor unit recruitment during neuromuscular electrical stimulation: A critical appraisal. European Journal of Applied Physiology, 111, 2399–2407.
Blazevich, A. J., Collins, D. F., Millet, G. Y., Vaz, M. A., & Maffiuletti, N. A. (2021). Enhancing adaptations to neuromuscular electrical stimulation training interventions. Exercise and Sport Sciences Reviews, 49, 244–252.
Crossland, H., Skirrow, S., Puthucheary, Z. A., Constantin‐Teodosiu, D., & Greenhaff, P. L. (2019). The impact of immobilisation and inflammation on the regulation of muscle mass and insulin resistance: Different routes to similar end‐points. Journal of Physiology, 597, 1259–1270.
Demangel, R., Treffel, L., Py, G., Brioche, T., Pagano, A. F., Bareille, M. P., Beck, A., Pessemesse, L., Candau, R., Gharib, C., Chopard, A., & Millet, C. (2017). Early structural and functional signature of 3‐day human skeletal muscle disuse using the dry immersion model. Journal of Physiology, 595, 4301–4315.
Deschenes, M. R., Holdren, A. N., & Mccoy, R. W. (2008). Adaptations to short‐term muscle unloading in young and aged men. Medicine and Science in Sports and Exercise, 40, 856–863.
Dirks, M. L., Hansen, D., Van Assche, A., Dendale, P., & Van Loon, L. J. C. (2015). Neuromuscular electrical stimulation prevents muscle wasting in critically ill comatose patients. Clinical Science, 128, 357–365.
Dirks, M. L., Wall, B. T., Snijders, T., Ottenbros, C. L. P., Verdijk, L. B., & Van Loon, L. J. C. (2014). Neuromuscular electrical stimulation prevents muscle disuse atrophy during leg immobilization in humans. Acta Physiologica, 210, 628–641.
Dirks, M. L., Wall, B. T., Van De Valk, B., Holloway, T. M., Holloway, G. P., Chabowski, A., Goossens, G. H., & Van Loon, L. J. (2016). One week of bed rest leads to substantial muscle atrophy and induces whole‐body insulin resistance in the absence of skeletal muscle lipid accumulation. Diabetes, 65, 2862–2875.
Folland, J. P., Buckthorpe, M. W., & Hannah, R. (2014). Human capacity for explosive force production: Neural and contractile determinants. Scandinavian Journal of Medicine & Science in Sports, 24, 894–906.
García‐Hermoso, A., Cavero‐Redondo, I., Ramírez‐Vélez, R., Ruiz, J. R., Ortega, F. B., Lee, D. C., & Martínez‐Vizcaíno, V. (2018). Muscular strength as a predictor of all‐cause mortality in an apparently healthy population: A systematic review and meta‐analysis of data from approximately 2 million men and women. Archives of Physical Medicine and Rehabilitation, 99, 2100–2113. e5.
Gondin, J., Duclay, J., & Martin, A. (2006). Soleus‐ and gastrocnemii‐evoked V‐wave responses increase after neuromuscular electrical stimulation training. Journal of Neurophysiology, 95, 3328–3335.
Gravholt, A., Herskind, J., Kloster, C. T., Hvid, L. G., & Overgaard, K. (2023). Torque and discomfort during electrically evoked muscle contractions in healthy Young adults: Influence of stimulation current and pulse frequency. Archives of Physical Medicine and Rehabilitation, 104, 444–450.
Gregory, C. M., & Bickel, C. S. (2005). Recruitment patterns in human skeletal muscle during electrical stimulation. Physical Therapy, 85, 358–364.
Hannah, R., Minshull, C., Buckthorpe, M. W., & Folland, J. P. (2012). Explosive neuromuscular performance of males versus females. Experimental Physiology, 97, 618–629.
Hortobágyi, T., & Maffiuletti, N. A. (2011). Neural adaptations to electrical stimulation strength training. European Journal of Applied Physiology, 111, 2439–2449.
Hvid, L. G., Aagaard, P., Ørtenblad, N., Kjaer, M., & Suetta, C. (2018). Plasticity in central neural drive with short‐term disuse and recovery—effects on muscle strength and influence of aging. Experimental Gerontology, 106, 145–153.
Hvid, L. G., Suetta, C., Aagaard, P., Kjaer, M., Frandsen, U., & Ørtenblad, N. (2013). Four days of muscle disuse impairs single fiber contractile function in young and old healthy men. Experimental Gerontology, 48, 154–161.
Hvid, L. G., Suetta, C., Nielsen, J. H., Jensen, M. M., Frandsen, U., Ørtenblad, N., Kjaer, M., & Aagaard, P. (2014). Aging impairs the recovery in mechanical muscle function following 4 days of disuse. Experimental Gerontology, 52, 1–8.
Karlsen, A., Cullum, C. K., Norheim, K. L., Scheel, F. U., Zinglersen, A. H., Vahlgren, J., Schjerling, P., Kjaer, M., & MacKey, A. L. (2020). Neuromuscular electrical stimulation preserves leg lean mass in geriatric patients. Medicine and Science in Sports and Exercise, 52, 773–784.
Maffiuletti, N. A., Aagaard, P., Blazevich, A. J., Folland, J., Tillin, N., & Duchateau, J. (2016). Rate of force development: Physiological and methodological considerations. European Journal of Applied Physiology, 116, 1091–1116.
Maffiuletti, N. A., Dirks, M. L., Stevens‐Lapsley, J., & McNeil, C. J. (2023). Electrical stimulation for investigating and improving neuromuscular function in vivo: Historical perspective and major advances. Journal of Biomechanics, 152, 111582.
Mayer, K. P., Thompson Bastin, M. L., Montgomery‐Yates, A. A., Pastva, A. M., Dupont‐Versteegden, E. E., Parry, S. M., & Morris, P. E. (2020). Acute skeletal muscle wasting and dysfunction predict physical disability at hospital discharge in patients with critical illness. Critical Care, 24, 1–12.
Merhi, Y., Betancur, P. F., Ripolles, T. S., Suetta, C., Brage‐andersen, M. R., Hansen, S. K., Frydenlund, A., Nygaard, J. V., Mikkelsen, P. H., Boix, P. P., & Agarwala, S. (2023). Printed dry electrode for neuromuscular electrical stimulation (NMES) for e‐textile †. Nanoscale, 15, 5337–5344. https://doi.org/10.1039/d2nr06008f
Mikines, K. J., Richter, E. A., Dela, F., & Galbo, H. (1991). Seven days of bed rest decrease insulin action on glucose uptake in leg and whole body. Journal of Applied Physiology, 70, 1245–1254.
Mulder, E., Clément, G., Linnarsson, D., Paloski, W. H., Wuyts, F. P., Zange, J., Frings‐Meuthen, P., Johannes, B., Shushakov, V., Grunewald, M., Maassen, N., Buehlmeier, J., & Rittweger, J. (2015). Musculoskeletal effects of 5 days of bed rest with and without locomotion replacement training. European Journal of Applied Physiology, 115, 727–738.
Norheim, K. L., Cullum, C. K., Andersen, J. L., Kjaer, M., & Karlsen, A. (2017). Inflammation relates to resistance training‐induced hypertrophy in elderly patients. Medicine and Science in Sports and Exercise, 49, 1079–1085.
Oates, B. R., Glover, E. I., West, D. W., Fry, J. L., Tarnopolsky, M. A., & Phillips, S. M. (2010). Low‐volume resistance exercise attenuates the decline in strength and muscle mass associated with immobilization. Muscle & Nerve, 42, 539–546.
Reidy, P. T., Edvalson, L. T., McKenzie, A. I., Petrocelli, J. J., Mahmassani, Z. S., & Drummonds, M. J. (2020). Neuromuscular electrical stimulation and protein during bed rest increases CD11b+ skeletal muscle macrophages but does not correspond to muscle size or insulin sensitivity. Applied Physiology, Nutrition and Metabolism, 45, 1261–1269.
Reidy, P. T., Lindsay, C. C., McKenzie, A. I., Fry, C. S., Supiano, M. A., Marcus, R. L., LaStayo, P. C., & Drummond, M. J. (2018). Aging‐related effects of bed rest followed by eccentric exercise rehabilitation on skeletal muscle macrophages and insulin sensitivity. Experimental Gerontology, 107, 37–49.
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, 449–461.
Smeuninx, B., Elhassan, Y. S., Sapey, E., Rushton, A. B., Morgan, P. T., Korzepa, M., Belfield, A. E., Philp, A., Brook, M. S., Gharahdaghi, N., Wilkinson, D., Smith, K., Atherton, P. J., & Breen, L. (2023). A single bout of prior resistance exercise attenuates muscle atrophy and declines in myofibrillar protein synthesis during bed‐rest in older men. Journal of Physiology, 0, 1–19.
Smorawiński, J., Kaciuba‐Uściłko, H., Nazar, K., Kubala, P., Kamińska, E., Ziemba, A. W., Adrian, J., & Greenleaf, J. E. (2000). Effects of three‐day bed rest on metabolic, hormonal and circulatory responses to an oral glucose load in endurance or strength trained athletes and untrained subjects. Journal of Physiology and Pharmacology, 51, 279–289.
Stuart, C. A., Shangraw, R. E., Prince, M. J., Peters, E. J., & Wolfe, R. R. (1988). Bed‐rest‐induced insulin resistance occurs primarily in muscle. Metabolism, 37, 802–806.
Stump, C. S., Henriksen, E. J., Wei, Y., & Sowers, J. R. (2006). The metabolic syndrome: Role of skeletal muscle metabolism. Annals of Medicine, 38, 389–402.
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. Journal of Applied Physiology, 1985(97), 1954–1961.
Suetta, C., Andersen, J. L., Dalgas, U., Berget, J., Koskinen, S., Aagaard, P., Magnusson, S. P., & Kjaer, M. (2008). Resistance training induces qualitative changes in muscle morphology, muscle architecture, and muscle function in elderly postoperative patients. Journal of Applied Physiology, 105, 180–186.
Suetta, C., Frandsen, U., Jensen, L., Jensen, M. M., Jespersen, J. G., Hvid, L. G., Bayer, M., Petersson, S. J., Schrøder, H. D., Andersen, J. L., Heinemeier, K. M., Aagaard, P., Schjerling, P., & Kjaer, M. (2012). Aging affects the transcriptional regulation of human skeletal muscle disuse atrophy. PLoS One, 7, e51238. https://doi.org/10.1371/journal.pone.0051238
Suetta, C., Frandsen, U., Mackey, A. L., Jensen, L., Hvid, L. G., Bayer, M. L., Petersson, S. J., Schrøder, H. D., Andersen, J. L., Aagaard, P., Schjerling, P., & Kjaer, M. (2013). Ageing is associated with diminished muscle re‐growth and myogenic precursor cell expansion early after immobility‐induced atrophy in human skeletal muscle. Journal of Physiology, 591, 3789–3804.
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, 107, 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. Journal of Physiology, 593, 4259–4273.
Wall, B. T., Dirks, M. L., Snijders, T., Senden, J. M. G., Dolmans, J., & Van Loon, L. J. C. (2014). Substantial skeletal muscle loss occurs during only 5 days of disuse. Acta Physiologica, 210, 600–611.
Wall, B. T., Dirks, M. L., & Van Loon, L. J. C. (2013). Skeletal muscle atrophy during short‐term disuse: Implications for age‐related sarcopenia. Ageing Research Reviews, 12, 898–906.
Wang, D. X. M., Yao, J., Zirek, Y., Reijnierse, E. M., & Maier, A. B. (2020). Muscle mass, strength, and physical performance predicting activities of daily living: A meta‐analysis. Journal of Cachexia, Sarcopenia and Muscle, 11, 3–25.
Wang, Z., Heshka, S., Gallagher, D., Boozer, C. N., Kotler, D. P., & Heymsfield, S. B. (2000). Resting energy expenditure‐fat‐free mass relationship: New insights provided by body composition modeling. American Journal of Physiology. Endocrinology and Metabolism, 279, 539–545.

Auteurs

Sofie K Hansen (SK)

Geriatric Research Unit, Copenhagen University Hospital - Bispebjerg and Frederiksberg, Copenhagen, Denmark.
CopenAge, Copenhagen Center for Clinical age Research, University of Copenhagen, Copenhagen, Denmark.

Pernille Hansen (P)

Geriatric Research Unit, Copenhagen University Hospital - Bispebjerg and Frederiksberg, Copenhagen, Denmark.
CopenAge, Copenhagen Center for Clinical age Research, University of Copenhagen, Copenhagen, Denmark.

Hanne Nygaard (H)

Geriatric Research Unit, Copenhagen University Hospital - Bispebjerg and Frederiksberg, Copenhagen, Denmark.
CopenAge, Copenhagen Center for Clinical age Research, University of Copenhagen, Copenhagen, Denmark.
Department of Emergency Medicine, Copenhagen University Hospital - Bispebjerg and Frederiksberg, Copenhagen, Denmark.

Hans D Grønbæk (HD)

Geriatric Research Unit, Copenhagen University Hospital - Bispebjerg and Frederiksberg, Copenhagen, Denmark.

Tania W Berry (TW)

Geriatric Research Unit, Copenhagen University Hospital - Bispebjerg and Frederiksberg, Copenhagen, Denmark.

Camilla M Olsen (CM)

Geriatric Research Unit, Copenhagen University Hospital - Bispebjerg and Frederiksberg, Copenhagen, Denmark.

Per Aagaard (P)

Department of Sport and Clinical Biomechanics, University of Southern Denmark, Odense, Denmark.

Lars G Hvid (LG)

Exercise Biology, Department of Public Health, Aarhus University, Aarhus, Denmark.
The Danish MS Hospitals, Ry and Haslev, Haslev, Denmark.

Jakob Agergaard (J)

Department of Orthopedic Surgery, Institute of Sports Medicine Copenhagen, Copenhagen University Hospital-Bispebjerg and Frederiksberg, Copenhagen, Denmark.
Department of Clinical Medicine, Center for Healthy Aging, University of Copenhagen, Copenhagen, Denmark.

Flemming Dela (F)

CopenAge, Copenhagen Center for Clinical age Research, University of Copenhagen, Copenhagen, Denmark.
Xlab, Department of Biomedical Sciences, University of Copenhagen, Copenhagen, Denmark.
Department of Physiology and Biochemistry, Riga Stradins University, Riga, Latvia.

Charlotte Suetta (C)

Geriatric Research Unit, Copenhagen University Hospital - Bispebjerg and Frederiksberg, Copenhagen, Denmark.
CopenAge, Copenhagen Center for Clinical age Research, University of Copenhagen, Copenhagen, Denmark.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH