Effects of Exercise Training on Muscle Quality in Older Individuals: A Systematic Scoping Review with Meta-Analyses
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, scoping review
PubMed
37278947
PubMed Central
PMC10244313
DOI
10.1186/s40798-023-00585-5
PII: 10.1186/s40798-023-00585-5
Knihovny.cz E-zdroje
- Klíčová slova
- Aging, Intramuscular fat, Muscle mass, Neurological disease, Resistance training,
- Publikační typ
- časopisecké články MeSH
- scoping review MeSH
BACKGROUND: The quantity and quality of skeletal muscle are important determinants of daily function and metabolic health. Various forms of physical exercise can improve muscle function, but this effect can be inconsistent and has not been systematically examined across the health-neurological disease continuum. The purpose of this systematic scoping review with meta-analyses was to determine the effects and potential moderators of exercise training on morphological and neuromuscular muscle quality (MMQ, NMQ) in healthy older individuals. In addition and in the form of a scoping review, we examined the effects of exercise training on NMQ and MMQ in individuals with neurological conditions. METHODS: A systematic literature search was performed in the electronic databases Medline, Embase, and Web of Science. Randomized controlled trials were included that examined the effects of exercise training on muscle quality (MQ) in older individuals with and without neurological conditions. Risk of bias and study quality were assessed (Cochrane Risk of Bias Tool 2.0). We performed random-effects models using robust variance estimation and tested moderators using the approximate Hotelling-Zhang test. RESULTS: Thirty studies (n = 1494, 34% females) in healthy older individuals and no studies in individuals with neurological conditions were eligible for inclusion. Exercise training had small effects on MMQ (g = 0.21, 95% confidence interval [CI]: 0.03-0.40, p = 0.029). Heterogeneity was low (median I2 = 16%). Training and demographic variables did not moderate the effects of exercise on MMQ. There was no association between changes in MMQ and changes in functional outcomes. Exercise training improved NMQ (g = 0.68, 95% CI 0.35-1.01, p < 0.000) across all studies, in particular in higher-functioning older individuals (g = 0.72, 95% CI 0.38-1.06, p < 0.001), in lower extremity muscles (g = 0.74, 95% CI 0.35-1.13, p = 0.001), and after resistance training (g = 0.91; 95% CI 0.42-1.41, p = 0.001). Heterogeneity was very high (median I2 = 79%). Of the training and demographic variables, only resistance training moderated the exercise-effects on NMQ. High- versus low-intensity exercise moderated the exercise-effects on NMQ, but these effects were considered unreliable due to a low number of studies at high intensity. There was no association between changes in NMQ and changes in functional outcomes. CONCLUSION: Exercise training has small effects on MMQ and medium-large effects on NMQ in healthy older individuals. There was no association between improvements in MQ and increases in muscle strength, mobility, and balance. Information on dose-response relations following training is currently lacking. There is a critical gap in muscle quality data for older individuals with lower function and neurological conditions after exercise training. Health practitioners should use resistance training to improve muscle function in older individuals. Well-designed studies are needed to examine the relevance of exercise training-induced changes in MQ in daily function in older individuals, especially to those with lower function and neurological conditions.
Center for Human Movement Sciences University of Groningen Medical Center Groningen The Netherlands
Department of Kinesiology Hungarian University of Sports Science Budapest Hungary
Department of Physical Therapy University of Pittsburgh Pittsburgh PA USA
Exercise Medicine Research Institute Edith Cowan University Joondalup Australia
Faculty of Human Kinetics CIPER University of Lisboa Cruz Quebrada Dafundo Portugal
Faculty of Physical Education and Sport Charles University Prague Czech Republic
Institute of Sport Research Sports University of Tirana Tirana Albania
Institute of Sport Sciences and Physical Education University of Pécs Pecs Hungary
School of Medical and Health Sciences Edith Cowan University Joondalup WA Australia
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Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyere O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48(4):601. doi: 10.1093/ageing/afz046. PubMed DOI PMC
Frontera WR, Hughes VA, Fielding RA, Fiatarone MA, Evans WJ, Roubenoff R. Aging of skeletal muscle: a 12-yr longitudinal study. J Appl Physiol (1985) 2000;88(4):1321–1326. doi: 10.1152/jappl.2000.88.4.1321. PubMed DOI
Wolfe RR. The underappreciated role of muscle in health and disease. Am J Clin Nutr. 2006;84(3):475–482. doi: 10.1093/ajcn/84.3.475. PubMed DOI
Faulkner JA, Larkin LM, Claflin DR, Brooks SV. Age-related changes in the structure and function of skeletal muscles. Clin Exp Pharmacol Physiol. 2007;34(11):1091–1096. doi: 10.1111/j.1440-1681.2007.04752.x. PubMed DOI
Deschenes MR. Effects of aging on muscle fibre type and size. Sports Med. 2004;34(12):809–824. doi: 10.2165/00007256-200434120-00002. PubMed DOI
Suetta C, Haddock B, Alcazar J, Noerst T, Hansen OM, Ludvig H, et al. The Copenhagen Sarcopenia Study: lean mass, strength, power, and physical function in a Danish cohort aged 20–93 years. J Cachexia Sarcopenia Muscle. 2019;10(6):1316–1329. doi: 10.1002/jcsm.12477. PubMed DOI PMC
Janssen I, Heymsfield SB, Wang ZM, Ross R. Skeletal muscle mass and distribution in 468 men and women aged 18–88 yr. J Appl Physiol (1985) 2000;89(1):81–88. doi: 10.1152/jappl.2000.89.1.81. PubMed DOI
Kennis E, Verschueren S, Van Roie E, Thomis M, Lefevre J, Delecluse C. Longitudinal impact of aging on muscle quality in middle-aged men. Age (Dordr) 2014;36(4):9689. doi: 10.1007/s11357-014-9689-1. PubMed DOI PMC
Abe T, Thiebaud RS, Loenneke JP. Age-related change in handgrip strength in men and women: is muscle quality a contributing factor? Age (Dordr) 2016;38(1):28. doi: 10.1007/s11357-016-9891-4. PubMed DOI PMC
Goodpaster BH, Chomentowski P, Ward BK, Rossi A, Glynn NW, Delmonico MJ, et al. Effects of physical activity on strength and skeletal muscle fat infiltration in older adults: a randomized controlled trial. J Appl Physiol (1985) 2008;105(5):1498–1503. doi: 10.1152/japplphysiol.90425.2008. PubMed DOI PMC
Granacher U, Gruber M, Gollhofer A. Force production capacity and functional reflex activity in young and elderly men. Aging Clin Exp Res. 2010;22(5–6):374–382. doi: 10.1007/BF03337733. PubMed DOI
Manini TM, Clark BC. Dynapenia and aging: an update. J Gerontol A Biol Sci Med Sci. 2012;67(1):28–40. doi: 10.1093/gerona/glr010. PubMed DOI PMC
Ferrucci L, de Cabo R, Knuth ND, Studenski S. Of Greek heroes, wiggling worms, mighty mice, and old body builders. J Gerontol A Biol Sci Med Sci. 2012;67(1):13–16. doi: 10.1093/gerona/glr046. PubMed DOI PMC
Zanker J, Blackwell T, Patel S, Duchowny K, Brennan-Olsen S, Cummings SR, et al. Factor analysis to determine relative contributions of strength, physical performance, body composition and muscle mass to disability and mobility disability outcomes in older men. Exp Gerontol. 2022;161:111714. doi: 10.1016/j.exger.2022.111714. PubMed DOI PMC
Custodio Martins P, de Lima TR, Silva AM, Santos Silva DA. Association of phase angle with muscle strength and aerobic fitness in different populations: a systematic review. Nutrition. 2022;93:111489. doi: 10.1016/j.nut.2021.111489. PubMed DOI
Kato T, Ikezoe T, Tabara Y, Matsuda F, Tsuboyama T, Ichihashi N. Differences in lower limb muscle strength and balance ability between sarcopenia stages depend on sex in community-dwelling older adults. Aging Clin Exp Res. 2022;34(3):527–534. doi: 10.1007/s40520-021-01952-6. PubMed DOI
Son JS, Chae SA, Testroet ED, Du M, Jun HP. Exercise-induced myokines: a brief review of controversial issues of this decade. Expert Rev Endocrinol Metab. 2018;13(1):51–58. doi: 10.1080/17446651.2018.1416290. PubMed DOI
Yu JH, Kim REY, Jung JM, Park SY, Lee DY, Cho HJ, et al. Sarcopenia is associated with decreased gray matter volume in the parietal lobe: a longitudinal cohort study. BMC Geriatr. 2021;21(1):622. doi: 10.1186/s12877-021-02581-4. PubMed DOI PMC
Wang J, Cao L, Xu S. Sarcopenia affects clinical efficacy of immune checkpoint inhibitors in non-small cell lung cancer patients: a systematic review and meta-analysis. Int Immunopharmacol. 2020;88:106907. doi: 10.1016/j.intimp.2020.106907. PubMed DOI
Manrique-Espinoza B, Salinas-Rodriguez A, Rosas-Carrasco O, Gutierrez-Robledo LM, Avila-Funes JA. Sarcopenia is associated with physical and mental components of health-related quality of life in older adults. J Am Med Dir Assoc. 2017;18(7):636. doi: 10.1016/j.jamda.2017.04.005. PubMed DOI
Verlaan S, Aspray TJ, Bauer JM, Cederholm T, Hemsworth J, Hill TR, et al. Nutritional status, body composition, and quality of life in community-dwelling sarcopenic and non-sarcopenic older adults: a case-control study. Clin Nutr. 2017;36(1):267–274. doi: 10.1016/j.clnu.2015.11.013. PubMed DOI
Oztorun HS, Bahsi R, Turgut T, Surmeli DM, Cosarderelioglu C, Atmis V, et al. The relationship between sarcopenia and central hemodynamics in older adults with falls: a cross-sectional study. Blood Press Monit. 2022;27(2):87–97. doi: 10.1097/MBP.0000000000000569. PubMed DOI
Rodrigues F, Domingos C, Monteiro D, Morouco P. A review on aging, sarcopenia, falls, and resistance training in community-dwelling older adults. Int J Environ Res Public Health. 2022;19(2):874. doi: 10.3390/ijerph19020874. PubMed DOI PMC
Lim SK, Kong S. Prevalence, physical characteristics, and fall risk in older adults with and without possible sarcopenia. Aging Clin Exp Res. 2022;34(6):1365–1371. doi: 10.1007/s40520-022-02078-z. PubMed DOI
Köller M. Sarcopenia-a geriatric pandemic: a narrative review. Wien Med Wochenschr. 2022. PubMed
Xu J, Wan CS, Ktoris K, Reijnierse EM, Maier AB. Sarcopenia is associated with mortality in adults: a systematic review and meta-analysis. Gerontology. 2022;68(4):361–376. doi: 10.1159/000517099. PubMed DOI
Lopez P, Radaelli R, Taaffe DR, Newton RU, Galvao DA, Trajano GS, et al. Resistance training load effects on muscle hypertrophy and strength gain: systematic review and network meta-analysis. Med Sci Sports Exerc. 2021;53(6):1206–1216. doi: 10.1249/MSS.0000000000002585. PubMed DOI PMC
Radaelli R, Taaffe DR, Newton RU, Galvao DA, Lopez P. Exercise effects on muscle quality in older adults: a systematic review and meta-analysis. Sci Rep. 2021;11(1):21085. doi: 10.1038/s41598-021-00600-3. PubMed DOI PMC
Zhang H, Lin S, Gao T, Zhong F, Cai J, Sun Y, et al. Association between sarcopenia and metabolic syndrome in middle-aged and older non-obese adults: a systematic review and meta-analysis. Nutrients. 2018;10(3):364. doi: 10.3390/nu10030364. PubMed DOI PMC
Gao Q, Hu K, Gao J, Shang Y, Mei F, Zhao L, et al. Prevalence and prognostic value of sarcopenic obesity in patients with cancer: a systematic review and meta-analysis. Nutrition. 2022;101:111704. doi: 10.1016/j.nut.2022.111704. PubMed DOI
Jogiat UM, Sasewich H, Turner SR, Baracos V, Eurich DT, Filafilo H, et al. Sarcopenia determined by skeletal muscle index predicts overall survival, disease-free survival, and postoperative complications in resectable esophageal cancer: a systematic review and meta-analysis. Ann Surg. 2022;276:e311. doi: 10.1097/SLA.0000000000005452. PubMed DOI
Meyer HJ, Strobel A, Wienke A, Surov A. Prognostic role of low-skeletal muscle mass on staging computed tomography in metastasized colorectal cancer: a systematic review and meta-analysis. Clin Colorectal Cancer. 2022. PubMed
Heo JE, Shim JS, Song BM, Bae HY, Lee HJ, Lee E, et al. Association between appendicular skeletal muscle mass and depressive symptoms: review of the cardiovascular and metabolic diseases etiology research center cohort. J Affect Disord. 2018;238:8–15. doi: 10.1016/j.jad.2018.05.012. PubMed DOI
Salinas-Rodriguez A, Palazuelos-Gonzalez R, Rivera-Almaraz A, Manrique-Espinoza B. Longitudinal association of sarcopenia and mild cognitive impairment among older Mexican adults. J Cachexia Sarcopenia Muscle. 2021;12(6):1848–1859. doi: 10.1002/jcsm.12787. PubMed DOI PMC
Orwoll ES, Blackwell T, Cummings SR, Cauley JA, Lane NE, Hoffman AR, et al. CT muscle density, D3Cr muscle mass, and body fat associations with physical performance, mobility outcomes, and mortality risk in older Men. J Gerontol A Biol Sci Med Sci. 2022;77(4):790–799. doi: 10.1093/gerona/glab266. PubMed DOI PMC
Smith C, Woessner MN, Sim M, Levinger I. Sarcopenia definition: does it really matter? Implications for resistance training. Ageing Res Rev. 2022;78:101617. doi: 10.1016/j.arr.2022.101617. PubMed DOI
Arango-Lopera VE, Arroyo P, Gutierrez-Robledo LM, Perez-Zepeda MU, Cesari M. Mortality as an adverse outcome of sarcopenia. J Nutr Health Aging. 2013;17(3):259–262. doi: 10.1007/s12603-012-0434-0. PubMed DOI PMC
Li CI, Liu CS, Lin CH, Yang SY, Li TC, Lin CC. Independent and joint associations of skeletal muscle mass and physical performance with all-cause mortality among older adults: a 12-year prospective cohort study. BMC Geriatr. 2022;22(1):597. doi: 10.1186/s12877-022-03292-0. PubMed DOI PMC
Lynch DH, Spangler HB, Franz JR, Krupenevich RL, Kim H, Nissman D, et al. Multimodal diagnostic approaches to advance precision medicine in sarcopenia and frailty. Nutrients. 2022;14(7):1384. doi: 10.3390/nu14071384. PubMed DOI PMC
Kim JH, Cho JJ, Park YS. Relationship between sarcopenic obesity and cardiovascular disease risk as estimated by the Framingham risk score. J Korean Med Sci. 2015;30(3):264–271. doi: 10.3346/jkms.2015.30.3.264. PubMed DOI PMC
Longobucco Y, Krumpoch S, Lauretani F, Angileri V, Sieber C, Marzetti E, et al. Gait characteristics in community-dwelling older persons with low skeletal muscle mass and low physical performance. Aging Clin Exp Res. 2022;34(7):1563–1571. doi: 10.1007/s40520-021-02061-0. PubMed DOI PMC
Gianoudis J, Bailey CA, Daly RM. Associations between sedentary behaviour and body composition, muscle function and sarcopenia in community-dwelling older adults. Osteoporos Int. 2015;26(2):571–579. doi: 10.1007/s00198-014-2895-y. PubMed DOI
Cao L, Morley JE. Sarcopenia is recognized as an independent condition by an international classification of disease, tenth revision, clinical modification (ICD-10-CM) code. J Am Med Dir Assoc. 2016;17(8):675–677. doi: 10.1016/j.jamda.2016.06.001. PubMed DOI
Fragala MS, Kenny AM, Kuchel GA. Muscle quality in aging: a multi-dimensional approach to muscle functioning with applications for treatment. Sports Med. 2015;45(5):641–658. doi: 10.1007/s40279-015-0305-z. PubMed DOI
Correa-de-Araujo R, Addison O, Miljkovic I, Goodpaster BH, Bergman BC, Clark RV, et al. Myosteatosis in the context of skeletal muscle function deficit: an interdisciplinary workshop at the national institute on aging. Front Physiol. 2020;11:963. doi: 10.3389/fphys.2020.00963. PubMed DOI PMC
Barbat-Artigas S, Rolland Y, Zamboni M, Aubertin-Leheudre M. How to assess functional status: a new muscle quality index. J Nutr Health Aging. 2012;16(1):67–77. doi: 10.1007/s12603-012-0004-5. PubMed DOI
Lynch NA, Metter EJ, Lindle RS, Fozard JL, Tobin JD, Roy TA, et al. Muscle quality. I. Age-associated differences between arm and leg muscle groups. J Appl Physiol (1985) 1999;86(1):188–194. doi: 10.1152/jappl.1999.86.1.188. PubMed DOI
Tracy BL, Ivey FM, Hurlbut D, Martel GF, Lemmer JT, Siegel EL, et al. Muscle quality. II. Effects of strength training in 65- to 75-yr-old men and women. J Appl Physiol (1985) 1999;86(1):195–201. doi: 10.1152/jappl.1999.86.1.195. PubMed DOI
Correa-de-Araujo R, Harris-Love MO, Miljkovic I, Fragala MS, Anthony BW, Manini TM. The need for standardized assessment of muscle quality in skeletal muscle function deficit and other aging-related muscle dysfunctions: a symposium report. Front Physiol. 2017;8:87. doi: 10.3389/fphys.2017.00087. PubMed DOI PMC
Garatachea N, Pareja-Galeano H, Sanchis-Gomar F, Santos-Lozano A, Fiuza-Luces C, Moran M, et al. Exercise attenuates the major hallmarks of aging. Rejuvenation Res. 2015;18(1):57–89. doi: 10.1089/rej.2014.1623. PubMed DOI PMC
Mende E, Moeinnia N, Schaller N, Weiss M, Haller B, Halle M, et al. Progressive machine-based resistance training for prevention and treatment of sarcopenia in the oldest old: a systematic review and meta-analysis. Exp Gerontol. 2022;163:111767. doi: 10.1016/j.exger.2022.111767. PubMed DOI
Zhang Y, Zou L, Chen ST, Bae JH, Kim DY, Liu X, et al. Effects and moderators of exercise on sarcopenic components in sarcopenic elderly: a systematic review and meta-analysis. Front Med (Lausanne) 2021;8:649748. doi: 10.3389/fmed.2021.649748. PubMed DOI PMC
Teodoro JL, Izquierdo M, da Silva LXN, Baroni BM, Grazioli R, Lopez P, et al. Effects of long-term concurrent training to failure or not in muscle power output, muscle quality and cardiometabolic risk factors in older men: a secondary analysis of a randomized clinical trial. Exp Gerontol. 2020;139:111023. doi: 10.1016/j.exger.2020.111023. PubMed DOI
Lopez P, Crosby BJ, Robetti BP, Turella DJP, Weber TAS, de Oliveira ML, et al. Effects of an 8-week resistance training intervention on plantar flexor muscle quality and functional capacity in older women: a randomised controlled trial. Exp Gerontol. 2020;138:111003. doi: 10.1016/j.exger.2020.111003. PubMed DOI
Radaelli R, Brusco CM, Lopez P, Rech A, Machado CLF, Grazioli R, et al. Muscle quality and functionality in older women improve similarly with muscle power training using one or three sets. Exp Gerontol. 2019;128:110745. doi: 10.1016/j.exger.2019.110745. PubMed DOI
Barichella M, Pinelli G, Iorio L, Cassani E, Valentino A, Pusani C, et al. Sarcopenia and dynapenia in patients with parkinsonism. J Am Med Dir Assoc. 2016;17(7):640–646. doi: 10.1016/j.jamda.2016.03.016. PubMed DOI
Do Nascimento TG, Paes-Silva RP, Da Luz MCL, Cabral PC, De Araujo Bezerra GK, Gomes ACB. Phase angle, muscle mass, and functionality in patients with Parkinson's disease. Neurol Sci. 2022;43(7):4203–4209. doi: 10.1007/s10072-022-05975-3. PubMed DOI
Vetrano DL, Pisciotta MS, Laudisio A, Lo Monaco MR, Onder G, Brandi V, et al. Sarcopenia in Parkinson disease: comparison of different criteria and association with disease severity. J Am Med Dir Assoc. 2018;19(6):523–527. doi: 10.1016/j.jamda.2017.12.005. PubMed DOI
Diechmann MD, Campbell E, Coulter E, Paul L, Dalgas U, Hvid LG. Effects of exercise training on neurotrophic factors and subsequent neuroprotection in persons with multiple sclerosis-a systematic review and meta-analysis. Brain Sci. 2021;11(11):1499. doi: 10.3390/brainsci11111499. PubMed DOI PMC
Portilla-Cueto K, Medina-Perez C, Romero-Perez EM, Nunez-Othon G, Horta-Gim MA, de Paz JA. Muscle quality of knee extensors based on several types of force in multiple sclerosis patients with varying degrees of disability. Medicina (Kaunas) 2022;58(2):316. doi: 10.3390/medicina58020316. PubMed DOI PMC
Wens I, Dalgas U, Vandenabeele F, Grevendonk L, Verboven K, Hansen D, et al. High intensity exercise in multiple sclerosis: effects on muscle contractile characteristics and exercise capacity, a randomised controlled trial. PLoS ONE. 2015;10(9):e0133697. doi: 10.1371/journal.pone.0133697. PubMed DOI PMC
Dalgas U, Stenager E, Jakobsen J, Petersen T, Overgaard K, Ingemann-Hansen T. Muscle fiber size increases following resistance training in multiple sclerosis. Mult Scler. 2010;16(11):1367–1376. doi: 10.1177/1352458510377222. PubMed DOI
Kjolhede T, Vissing K, de Place L, Pedersen BG, Ringgaard S, Stenager E, et al. Neuromuscular adaptations to long-term progressive resistance training translates to improved functional capacity for people with multiple sclerosis and is maintained at follow-up. Mult Scler. 2015;21(5):599–611. doi: 10.1177/1352458514549402. PubMed DOI
Fernandez-Gonzalo R, Fernandez-Gonzalo S, Turon M, Prieto C, Tesch PA, Garcia-Carreira MC. Muscle, functional and cognitive adaptations after flywheel resistance training in stroke patients: a pilot randomized controlled trial. J Neuroeng Rehabil. 2016;13:37. doi: 10.1186/s12984-016-0144-7. PubMed DOI PMC
Akazawa N, Harada K, Okawa N, Kishi M, Tamura K, Moriyama H. Changes in quadriceps thickness and echo intensity in chronic stroke survivors: a 3-year longitudinal study. J Stroke Cerebrovasc Dis. 2021;30(3):105543. doi: 10.1016/j.jstrokecerebrovasdis.2020.105543. PubMed DOI
Feng D, Zhao C, Chen D, He X, Lu X, Gao W. Preventive effect of rehabilitation training therapy on muscle quality in patients with stroke. Retrosp Study Aging Pathobiol Ther. 2021;3(4):136–138.
Honaga K, Mori N, Akimoto T, Tsujikawa M, Kawakami M, Okamoto T, et al. Investigation of the effect of nutritional supplementation with whey protein and vitamin D on muscle mass and muscle quality in subacute post-stroke rehabilitation patients: a randomized, single-blinded, placebo-controlled trial. Nutrients. 2022;14(3):685. doi: 10.3390/nu14030685. PubMed DOI PMC
Mas MF, Gonzalez J, Frontera WR. Stroke and sarcopenia. Curr Phys Med Rehabil Rep. 2020;8(4):452–460. doi: 10.1007/s40141-020-00284-2. PubMed DOI PMC
Ryan AS, Ivey FM, Prior S, Li G, Hafer-Macko C. Skeletal muscle hypertrophy and muscle myostatin reduction after resistive training in stroke survivors. Stroke. 2011;42(2):416–420. doi: 10.1161/STROKEAHA.110.602441. PubMed DOI PMC
Suzuki K, Ito T, Okada Y, Hiraoka T, Hanayama K, Tsubahara A. Preventive effects of repetitive peripheral magnetic stimulation on muscle atrophy in the paretic lower limb of acute stroke patients: a pilot study. Prog Rehabil Med. 2020;5:20200008. doi: 10.2490/prm.20200008. PubMed DOI PMC
Tanaka S, Ito D, Kimura Y, Ishiyama D, Suzuki M, Koyama S, et al. Relationship between longitudinal changes in skeletal muscle characteristics over time and functional recovery during intensive rehabilitation of patients with subacute stroke. Top Stroke Rehabil. 2022;29(5):356–365. doi: 10.1080/10749357.2021.1940724. PubMed DOI
Dalise S, Azzollini V, Chisari C. Brain and muscle: how central nervous system disorders can modify the skeletal muscle. Diagnostics (Basel) 2020;10(12):1047. doi: 10.3390/diagnostics10121047. PubMed DOI PMC
Harbo T, Brincks J, Andersen H. Maximal isokinetic and isometric muscle strength of major muscle groups related to age, body mass, height, and sex in 178 healthy subjects. Eur J Appl Physiol. 2012;112(1):267–275. doi: 10.1007/s00421-011-1975-3. PubMed DOI
Phillipe de Lucena Alves C, Camara M, Dantas Macedo GA, Freire YA, de Melo Silva R, Paulo-Pereira R, et al. Agreement between upper and lower limb measures to identify older adults with low skeletal muscle strength, muscle mass and muscle quality. PLoS ONE. 2022;17(1):e0262732. PubMed PMC
Candow DG, Chilibeck PD. Differences in size, strength, and power of upper and lower body muscle groups in young and older men. J Gerontol A Biol Sci Med Sci. 2005;60(2):148–156. doi: 10.1093/gerona/60.2.148. PubMed DOI
Bergamin M, Ermolao A, Tolomio S, Berton L, Sergi G, Zaccaria M. Water- versus land-based exercise in elderly subjects: effects on physical performance and body composition. Clin Interv Aging. 2013;8:1109–1117. doi: 10.2147/CIA.S44198. PubMed DOI PMC
Cunha PM, Nunes JP, Tomeleri CM, Nascimento MA, Schoenfeld BJ, Antunes M, et al. Resistance training performed with single and multiple sets induces similar improvements in muscular strength, muscle mass, muscle quality, and IGF-1 in older women: a randomized controlled trial. J Strength Cond Res. 2020;34(4):1008–1016. doi: 10.1519/JSC.0000000000002847. PubMed DOI
Cunha PM, Tomeleri CM, Nascimento MAD, Nunes JP, Antunes M, Nabuco HCG, et al. Improvement of cellular health indicators and muscle quality in older women with different resistance training volumes. J Sports Sci. 2018;36(24):2843–2848. doi: 10.1080/02640414.2018.1479103. PubMed DOI
Herda AA, Nabavizadeh O. Short-term resistance training in older adults improves muscle quality: a randomized control trial. Exp Gerontol. 2021;145:111195. doi: 10.1016/j.exger.2020.111195. PubMed DOI
Hofmann M, Schober-Halper B, Oesen S, Franzke B, Tschan H, Bachl N, et al. Effects of elastic band resistance training and nutritional supplementation on muscle quality and circulating muscle growth and degradation factors of institutionalized elderly women: the Vienna Active Ageing Study (VAAS) Eur J Appl Physiol. 2016;116(5):885–897. doi: 10.1007/s00421-016-3344-8. PubMed DOI PMC
Yamada M, Kimura Y, Ishiyama D, Nishio N, Otobe Y, Tanaka T, et al. Synergistic effect of bodyweight resistance exercise and protein supplementation on skeletal muscle in sarcopenic or dynapenic older adults. Geriatr Gerontol Int. 2019;19(5):429–437. doi: 10.1111/ggi.13643. PubMed DOI
Beaudart C, Dawson A, Shaw SC, Harvey NC, Kanis JA, Binkley N, et al. Nutrition and physical activity in the prevention and treatment of sarcopenia: systematic review. Osteoporos Int. 2017;28(6):1817–1833. doi: 10.1007/s00198-017-3980-9. PubMed DOI PMC
Englund DA, Kirn DR, Koochek A, Zhu H, Travison TG, Reid KF, et al. Nutritional supplementation with physical activity improves muscle composition in mobility-limited older adults, the VIVE2 study: a randomized, double-blind, placebo-controlled trial. J Gerontol A Biol Sci Med Sci. 2017;73(1):95–101. doi: 10.1093/gerona/glx141. PubMed DOI PMC
Strasser EM, Hofmann M, Franzke B, Schober-Halper B, Oesen S, Jandrasits W, et al. Strength training increases skeletal muscle quality but not muscle mass in old institutionalized adults: a randomized, multi-arm parallel and controlled intervention study. Eur J Phys Rehabil Med. 2018;54(6):921–933. PubMed
Ribeiro AS, Picoloto A, Nunes JP, Bezerra ES, Schoenfeld BJ, Cyrino ES. Effects of different resistance training loads on the muscle quality index in older women. J Strength Cond Res. 2022;36(5):1445–1449. doi: 10.1519/JSC.0000000000003667. PubMed DOI
Middleton A, Fritz SL, Lusardi M. Walking speed: the functional vital sign. J Aging Phys Act. 2015;23(2):314–322. doi: 10.1123/japa.2013-0236. PubMed DOI PMC
Bernabei R, Landi F, Calvani R, Cesari M, Del Signore S, Anker SD, et al. Multicomponent intervention to prevent mobility disability in frail older adults: randomised controlled trial (SPRINTT project) BMJ. 2022;377:e068788. doi: 10.1136/bmj-2021-068788. PubMed DOI PMC
Kraemer WJ, Adams K, Cafarelli E, Dudley GA, Dooly C, Feigenbaum MS, et al. American College of Sports Medicine position stand. Progression models in resistance training for healthy adults. Med Sci Sports Exerc. 2002;34(2):364–380. doi: 10.1097/00005768-200202000-00027. PubMed DOI
Ratamess NA, Alvar BA, Evetoch TK, Housh TJ, Kibler WB, Kraemer WJ. Progression models in resistance training for healthy adults. Med Sci Sports Exerc. 2009;41(3):687–708. doi: 10.1249/MSS.0b013e3181915670. PubMed DOI
Borde R, Hortobagyi T, Granacher U. Dose-response relationships of resistance training in healthy old adults: a systematic review and meta-analysis. Sports Med. 2015;45(12):1693–1720. doi: 10.1007/s40279-015-0385-9. PubMed DOI PMC
Ainsworth BE, Haskell WL, Whitt MC, Irwin ML, Swartz AM, Strath SJ, et al. Compendium of physical activities: an update of activity codes and MET intensities. Med Sci Sports Exerc. 2000;32(9 Suppl):S498–504. doi: 10.1097/00005768-200009001-00009. PubMed DOI
Garber CE, Blissmer B, Deschenes MR, Franklin BA, Lamonte MJ, Lee IM, et al. American College of Sports Medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Med Sci Sports Exerc. 2011;43(7):1334–1359. doi: 10.1249/MSS.0b013e318213fefb. PubMed DOI
Sterne JAC, Savovic J, Page MJ, Elbers RG, Blencowe NS, Boutron I, et al. RoB 2: a revised tool for assessing risk of bias in randomised trials. BMJ. 2019;366:l4898. doi: 10.1136/bmj.l4898. PubMed DOI
Hedges LV, Tipton E, Johnson MC. Robust variance estimation in meta-regression with dependent effect size estimates. Res Synth Meth. 2010;1:39–65. doi: 10.1002/jrsm.5. PubMed DOI
Tipton E. Small sample adjustments for robust variance estimation with meta-regression. Psych Meth. 2015;20:375–393. doi: 10.1037/met0000011. PubMed DOI
Viechtbauer W, Cheung MW. Outlier and influence diagnostics for meta-analysis. Res Synth Methods. 2010;1(2):112–125. doi: 10.1002/jrsm.11. PubMed DOI
Sterne JA, Egger M. Regression methods to detect publication and other bias in meta-analysis. In: Rothstein HR, Sutton AJ, Borenstein M, editors. Publication bias in meta-analysis: prevention, assessment and adjustments. West Sussex: John Wiley & Sons Ltd; 2005. pp. 99–110.
Brydges CR. Effect size guidelines, sample size calculations, and statistical power in gerontology. Innov Aging. 2019;3(4):igz036. doi: 10.1093/geroni/igz036. PubMed DOI PMC
Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–560. doi: 10.1136/bmj.327.7414.557. PubMed DOI PMC
Falck RS, Davis JC, Best JR, Crockett RA, Liu-Ambrose T. Impact of exercise training on physical and cognitive function among older adults: a systematic review and meta-analysis. Neurobiol Aging. 2019;79:119–130. doi: 10.1016/j.neurobiolaging.2019.03.007. PubMed DOI
Brightwell CR, Markofski MM, Moro T, Fry CS, Porter C, Volpi E, et al. Moderate-intensity aerobic exercise improves skeletal muscle quality in older adults. Transl Sports Med. 2019;2(3):109–119. doi: 10.1002/tsm2.70. PubMed DOI PMC
Cadore EL, Casas-Herrero A, Zambom-Ferraresi F, Idoate F, Millor N, Gomez M, et al. Multicomponent exercises including muscle power training enhance muscle mass, power output, and functional outcomes in institutionalized frail nonagenarians. Age (Dordr) 2014;36(2):773–785. doi: 10.1007/s11357-013-9586-z. PubMed DOI PMC
Coelho-Junior HJ, de Oliveira GI, Sampaio RAC, Sewo Sampaio PY, Cadore EL, Izquierdo M, et al. Periodized and non-periodized resistance training programs on body composition and physical function of older women. Exp Gerontol. 2019;121:10–18. doi: 10.1016/j.exger.2019.03.001. PubMed DOI
de Azevedo BS, Radaelli R, Beck Schemes M, Neske R, Garbelotto C, Roschel H, et al. Can supplemental protein to low-protein containing meals superimpose on resistance-training muscle adaptations in older adults? A randomized clinical trial. Exp Gerontol. 2022;162:111760. doi: 10.1016/j.exger.2022.111760. PubMed DOI
Flor-Rufino C, Barrachina-Igual J, Perez-Ros P, Pablos-Monzo A, Sanz-Requena R, Martinez-Arnau FM. Fat infiltration and muscle hydration improve after high-intensity resistance training in women with sarcopenia A randomized clinical trial. Maturitas. 2023;168:29–36. doi: 10.1016/j.maturitas.2022.09.001. PubMed DOI
Fragala MS, Jajtner AR, Beyer KS, Townsend JR, Emerson NS, Scanlon TC, et al. Biomarkers of muscle quality: N-terminal propeptide of type III procollagen and C-terminal agrin fragment responses to resistance exercise training in older adults. J Cachexia Sarcopenia Muscle. 2014;5(2):139–148. doi: 10.1007/s13539-013-0120-z. PubMed DOI PMC
Ghasemikaram M, Engelke K, Kohl M, von Stengel S, Kemmler W. Detraining effects on muscle quality in older men with osteosarcopenia. Follow-up of the randomized controlled franconian osteopenia and sarcopenia trial (FrOST) Nutrients. 2021;13(5):1528. doi: 10.3390/nu13051528. PubMed DOI PMC
Kargaran A, Abedinpour A, Saadatmehr Z, Yaali R, Amani-Shalamzari S, Gahreman D. Effects of dual-task training with blood flow restriction on cognitive functions, muscle quality, and circulatory biomarkers in elderly women. Physiol Behav. 2021;239:113500. doi: 10.1016/j.physbeh.2021.113500. PubMed DOI
Kennis E, Verschueren SM, Bogaerts A, Coudyzer W, Boonen S, Delecluse C. Effects of fitness and vibration training on muscle quality: a 1-year postintervention follow-up in older men. Arch Phys Med Rehabil. 2013;94(5):910–918. doi: 10.1016/j.apmr.2012.12.005. PubMed DOI
Liao CD, Tsauo JY, Huang SW, Ku JW, Hsiao DJ, Liou TH. Effects of elastic band exercise on lean mass and physical capacity in older women with sarcopenic obesity: a randomized controlled trial. Sci Rep. 2018;8(1):2317. doi: 10.1038/s41598-018-20677-7. PubMed DOI PMC
Markofski MM, Jennings K, Timmerman KL, Dickinson JM, Fry CS, Borack MS, et al. Effect of aerobic exercise training and essential amino acid supplementation for 24 weeks on physical function, body composition, and muscle metabolism in healthy, independent older adults: a randomized clinical trial. J Gerontol A Biol Sci Med Sci. 2019;74(10):1598–1604. doi: 10.1093/gerona/gly109. PubMed DOI PMC
Oh SL, Kim HJ, Woo S, Cho BL, Song M, Park YH, et al. Effects of an integrated health education and elastic band resistance training program on physical function and muscle strength in community-dwelling elderly women: healthy aging and happy aging II study. Geriatr Gerontol Int. 2017;17(5):825–833. doi: 10.1111/ggi.12795. PubMed DOI
Osuka Y, Kojima N, Nishihara K, Sasai H, Wakaba K, Tanaka K, et al. Beta-hydroxy-beta-methylbutyrate supplementation may not enhance additional effects of exercise on muscle quality in older women. Med Sci Sports Exerc. 2022;54(4):543–550. doi: 10.1249/MSS.0000000000002836. PubMed DOI
Pinto RS, Correa CS, Radaelli R, Cadore EL, Brown LE, Bottaro M. Short-term strength training improves muscle quality and functional capacity of elderly women. Age (Dordr) 2014;36(1):365–372. doi: 10.1007/s11357-013-9567-2. PubMed DOI PMC
Scanlon TC, Fragala MS, Stout JR, Emerson NS, Beyer KS, Oliveira LP, et al. Muscle architecture and strength: adaptations to short-term resistance training in older adults. Muscle Nerve. 2014;49(4):584–592. doi: 10.1002/mus.23969. PubMed DOI
Sipila S, Suominen H. Effects of strength and endurance training on thigh and leg muscle mass and composition in elderly women. J Appl Physiol (1985) 1995;78(1):334–340. doi: 10.1152/jappl.1995.78.1.334. PubMed DOI
Vojciechowski AS, Silva CTS, Rodrigues EV, Gallo LH, Melo Filho J, Gomes ARS. Does physical dance training with virtual games change muscle quality of community-dwelling older women? Games Health J. 2021;10(6):391–399. doi: 10.1089/g4h.2020.0223. PubMed DOI
Wei M, Meng D, Guo H, He S, Tian Z, Wang Z, et al. Hybrid exercise program for sarcopenia in older adults: the effectiveness of explainable artificial intelligence-based clinical assistance in assessing skeletal muscle area. Int J Environ Res Public Health. 2022;19(16):9952. doi: 10.3390/ijerph19169952. PubMed DOI PMC
Wilhelm EN, Rech A, Minozzo F, Botton CE, Radaelli R, Teixeira BC, et al. Concurrent strength and endurance training exercise sequence does not affect neuromuscular adaptations in older men. Exp Gerontol. 2014;60:207–214. doi: 10.1016/j.exger.2014.11.007. PubMed DOI
Hortobágyi T, Granacher U, Fernandez-Del-Olmo M, Howatson G, Manca A, Deriu F, et al. Functional relevance of resistance training-induced neuroplasticity in health and disease. Neurosci Biobehav Rev. 2021;122:79–91. doi: 10.1016/j.neubiorev.2020.12.019. PubMed DOI
Azzollini V, Dalise S, Chisari C. How does stroke affect skeletal muscle? State of the art and rehabilitation perspective. Front Neurol. 2021;12:797559. doi: 10.3389/fneur.2021.797559. PubMed DOI PMC
Engelke K, Ghasemikaram M, Chaudry O, Uder M, Nagel AM, Jakob F, et al. The effect of ageing on fat infiltration of thigh and paraspinal muscles in men. Aging Clin Exp Res. 2022;34(9):2089–2098. doi: 10.1007/s40520-022-02149-1. PubMed DOI PMC
Sardeli AV, Tomeleri CM, Cyrino ES, Fernhall B, Cavaglieri CR, Chacon-Mikahil MPT. Effect of resistance training on inflammatory markers of older adults: a meta-analysis. Exp Gerontol. 2018;111:188–196. doi: 10.1016/j.exger.2018.07.021. PubMed DOI
Curran-Everett D. Explorations in statistics: the analysis of ratios and normalized data. Adv Physiol Educ. 2013;37(3):213–219. doi: 10.1152/advan.00053.2013. PubMed DOI
Dibble LE, Hale TF, Marcus RL, Droge J, Gerber JP, LaStayo PC. High-intensity resistance training amplifies muscle hypertrophy and functional gains in persons with Parkinson's disease. Mov Disord. 2006;21(9):1444–1452. doi: 10.1002/mds.20997. PubMed DOI
Brahms CM, Hortobágyi T, Kressig RW, Granacher U. The interaction between mobility status and exercise specificity in older adults. Exerc Sport Sci Rev. 2021;49(1):15–22. doi: 10.1249/JES.0000000000000237. PubMed DOI
Choi M, Kim H, Bae J. Does the combination of resistance training and a nutritional intervention have a synergic effect on muscle mass, strength, and physical function in older adults? A systematic review and meta-analysis. BMC Geriatr. 2021;21(639):1–16. PubMed PMC
Antunes M, Kassiano W, Silva AM, Schoenfeld BJ, Ribeiro AS, Costa B, et al. Volume reduction: which dose is sufficient to retain resistance training adaptations in older women? Int J Sports Med. 2022;43(1):68–76. doi: 10.1055/a-1502-6361. PubMed DOI
Radaelli R, Botton CE, Wilhelm EN, Bottaro M, Brown LE, Lacerda F, et al. Time course of low- and high-volume strength training on neuromuscular adaptations and muscle quality in older women. Age (Dordr) 2014;36(2):881–892. doi: 10.1007/s11357-013-9611-2. PubMed DOI PMC
Sousa N, Mendes R, Abrantes C, Sampaio J. Differences in maximum upper and lower limb strength in older adults after a 12 week intense resistance training program. J Hum Kinet. 2011;30:183–188. doi: 10.2478/v10078-011-0086-x. PubMed DOI PMC
Kern DS, Semmler JG, Enoka RM. Long-term activity in upper- and lower-limb muscles of humans. J Appl Physiol (1985) 2001;91(5):2224–2232. doi: 10.1152/jappl.2001.91.5.2224. PubMed DOI
Cereda E, Cassani E, Barichella M, Spadafranca A, Caccialanza R, Bertoli S, et al. Low cardiometabolic risk in Parkinson's disease is independent of nutritional status, body composition and fat distribution. Clin Nutr. 2012;31(5):699–704. doi: 10.1016/j.clnu.2012.02.004. PubMed DOI
Martignon C, Ruzzante F, Giuriato G, Laginestra FG, Pedrinolla A, Di Vico IA, et al. The key role of physical activity against the neuromuscular deterioration in patients with Parkinson's disease. Acta Physiol (Oxf) 2021;231(4):e13630. doi: 10.1111/apha.13630. PubMed DOI
Kelly NA, Ford MP, Standaert DG, Watts RL, Bickel CS, Moellering DR, et al. Novel, high-intensity exercise prescription improves muscle mass, mitochondrial function, and physical capacity in individuals with Parkinson's disease. J Appl Physiol (1985) 2014;116(5):582–592. doi: 10.1152/japplphysiol.01277.2013. PubMed DOI PMC
Chiang PL, Chen YS, Lin AW. Altered body composition of psoas and thigh muscles in relation to frailty and severity of Parkinson's Disease. Int J Environ Res Public Health. 2019;16(19). PubMed PMC
Reich DS, Lucchinetti CF, Calabresi PA. Multiple sclerosis. N Engl J Med. 2018;378(2):169–180. doi: 10.1056/NEJMra1401483. PubMed DOI PMC
Kirmaci ZIK, Firat T, Ozkur HA, Neyal AM, Neyal A, Ergun N. Muscle architecture and its relationship with lower extremity muscle strength in multiple sclerosis. Acta Neurol Belg. 2021. PubMed
Carroll CC, Gallagher PM, Seidle ME, Trappe SW. Skeletal muscle characteristics of people with multiple sclerosis. Arch Phys Med Rehabil. 2005;86(2):224–229. doi: 10.1016/j.apmr.2004.03.035. PubMed DOI
Kent-Braun JA, Ng AV, Castro M, Weiner MW, Gelinas D, Dudley GA, et al. Strength, skeletal muscle composition, and enzyme activity in multiple sclerosis. J Appl Physiol (1985) 1997;83(6):1998–2004. doi: 10.1152/jappl.1997.83.6.1998. PubMed DOI
Ramsay JW, Barrance PJ, Buchanan TS, Higginson JS. Paretic muscle atrophy and non-contractile tissue content in individual muscles of the post-stroke lower extremity. J Biomech. 2011;44(16):2741–2746. doi: 10.1016/j.jbiomech.2011.09.001. PubMed DOI PMC
Taul-Madsen L, Connolly L, Dennett R, Freeman J, Dalgas U, Hvid LG. Is aerobic or resistance training the most effective exercise modality for improving lower extremity physical function and perceived fatigue in people with multiple sclerosis? A systematic review and meta-analysis. Arch Phys Med Rehabil. 2021;102(10):2032–2048. doi: 10.1016/j.apmr.2021.03.026. PubMed DOI
Lee J, Stone AJ. Combined aerobic and resistance training for cardiorespiratory fitness, muscle strength, and walking capacity after stroke: a systematic review and meta-analysis. J Stroke Cerebrovasc Dis. 2020;29(1):104498. doi: 10.1016/j.jstrokecerebrovasdis.2019.104498. PubMed DOI