Protein Supplementation Increases Muscle Mass Gain During Prolonged Resistance-Type Exercise Training in Frail Elderly People: A Randomized, Double-Blind, Placebo-Controlled Trial

Tieland, Michael; Dirks, Marlou L.; van der Zwaluw, Nikita; Verdijk, Lex B.; van de Rest, Ondine; de Groot, Lisette C.P.G.M.; van Loon, Luc J.C.

doi:10.1016/j.jamda.2012.05.020

Cited by 556Muscle metabolism and nutritionNutrition and Health in AgingMuscle Physiology and Disorders

Protein Supplementation Increases Muscle Mass Gain During Prolonged Resistance-Type Exercise Training in Frail Elderly People: A Randomized, Double-Blind, Placebo-Controlled Trial

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Tieland, Michael, Dirks, Marlou L., van der Zwaluw, Nikita, Verdijk, Lex B., van de Rest, Ondine, de Groot, Lisette C.P.G.M., van Loon, Luc J.C.·2012·Journal of the American Medical Directors Association

DOI 10.1016/j.jamda.2012.05.020

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Abstract

Objectives Protein supplementation has been proposed as an effective dietary strategy to augment the skeletal muscle adaptive response to prolonged resistance-type exercise training in elderly people. Our objective was to assess the impact of protein supplementation on muscle mass, strength, and physical performance during prolonged resistance-type exercise training in frail elderly men and women. Design/setting/participants A randomized, double-blind, placebo-controlled trial with 2 arms in parallel among 62 frail elderly subjects (78 ± 1 year). These elderly subjects participated in a progressive resistance-type exercise training program (2 sessions per week for 24 weeks) during which they were supplemented twice daily with either protein (2 * 15 g) or a placebo. Measurements Lean body mass (DXA), strength (1-RM), and physical performance (SPPB) were assessed at baseline, and after 12 and 24 weeks of intervention. Results Lean body mass increased from 47.2 kg (95% CI, 43.5-50.9) to 48.5 kg (95% CI, 44.8-52.1) in the protein group and did not change in the placebo group (from 45.7 kg, 95% CI, 42.1-49.2 to 45.4 kg, 95% CI, 41.8-48.9) following the intervention (P value for treatment × time interaction = .006). Strength and physical performance improved significantly in both groups (P = .000) with no interaction effect of dietary protein supplementation. Conclusions Prolonged resistance-type exercise training represents an effective strategy to improve strength and physical performance in frail elderly people. Dietary protein supplementation is required to allow muscle mass gain during exercise training in frail elderly people. Trial registration clinicaltrials.gov identifier: NCT01110369.

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In a clinical study, frail older people who engaged in resistance training and consumed supplemental dietary protein for 24 weeks showed significant muscle hypertrophy, together with increases in muscle strength and performance; researchers concluded that protein intake was necessary for training-associated gains in muscle mass.
“In a clinical study, frail older people who engaged in resistance training and consumed supplemental dietary protein for 24 weeks showed significant muscle hypertrophy, together with increases in muscle strength and performance; study researchers concluded that protein intake was necessary for training-associated gains in muscle mass.142”
From Evidence-Based Recommendations for Optimal Dietary Protein Intake in Older People: A Position Paper From the PROT-AGE Study Group (2013) · cites this paper as [142]

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Sousa‐Santos, A. R., & do Amaral, T. F. (2017) · BMC Geriatrics · doi:10.1186/s12877-017-0625-y · Cited by 273 · see citing works
Protein and healthy aging.
Paddon-Jones, D., Campbell, W., Jacques, P., Kritchevsky, S., Moore, L., Rodriguez, N., & van Loon, L. V. (2015) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.114.084061 · Cited by 255 · see citing works
SARC-F for Screening of Sarcopenia Among Older Adults: A Meta-analysis of Screening Test Accuracy
Ida, S., Kaneko, R., & Murata, K. (2018) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2018.04.001 · Cited by 265 · see citing works
The role of dietary protein and vitamin D in maintaining musculoskeletal health in postmenopausal women: A consensus statement from the European Society for Clinical and Economic Aspects of Osteoporosis and Osteoarthritis (ESCEO)
Rizzoli, R., Stevenson, J. C., Bauer, J. M., van Loon, L. J. C., Walrand, S., Kanis, J. A., Cooper, C., Brandi, M.-L., Diez-Perez, A., & Reginster, J.-Y. (2014) · Maturitas · doi:10.1016/j.maturitas.2014.07.005 · Cited by 291 · see citing works
“Exercise and protein supplementation n frail elderly people can lead to an increase in muscle mass and n increase in strength [75].”
Background
Exercise as a remedy for sarcopenia
Landi, F., Marzetti, E., Martone, A. M., Bernabei, R., & Onder, G. (2013) · Current Opinion in Clinical Nutrition and Metabolic Care · doi:10.1097/mco.0000000000000018 · Cited by 255 · see citing works
“[28,29] reported the results of two trials on the effects of protein supplementation with and without exercise on muscle mass and physical performance in frail older people.”
Background
Protein Requirements and Recommendations for Older People: A Review
Nowson, C., & O'Connell, S. (2015) · Nutrients · doi:10.3390/nu7085311 · Cited by 243 · see citing works
“The three studies without energy restriction published after this do not alter the overall conclusion from the meta-analysis, with one finding an improvement in lean mass [64] and the others no improvement [65,66] (Table 1).”
BackgroundResultInfluential
A high whey protein-, leucine-, and vitamin D–enriched supplement preserves muscle mass during intentional weight loss in obese older adults: a double-blind randomized controlled trial
Verreijen, A. M., Verlaan, S., Engberink, M. F., Swinkels, S., de Vogel-van den Bosch, J., & Weijs, P. J. (2015) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.114.090290 · Cited by 237 · see citing works
“(30) showed in their randomized controlled trial that protein supplementation in (pre)frail elderly increased muscle mass during resistance-type exercise without increasing physical functioning.”
Pharmacologic Options for the Treatment of Sarcopenia
Morley, J. E. (2016) · Calcified Tissue International · doi:10.1007/s00223-015-0022-5 · Cited by 225 · see citing works
Effectiveness of Nutritional Supplementation on Muscle Mass in Treatment of Sarcopenia in Old Age: A Systematic Review
Malafarina, V., Úriz‐Otano, F., Iniesta, R. R., & Gil‐Guerrero, L. (2012) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2012.08.001 · Cited by 231 · see citing works
Elderly men and women benefit equally from prolonged resistance-type exercise training
Leenders, M., Verdijk, L. B., van der Hoeven, L., van Kranenburg, J., Nilwik, R., & van Loon, L. J. C. (2013) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/gls241 · Cited by 226 · see citing works
Self-citation
Protein Intake and Muscle Health in Old Age: From Biological Plausibility to Clinical Evidence
Landi, F., Calvani, R., Tosato, M., Martone, A., Ortolani, E., Savera, G., D’Angelo, E., Sisto, A., & Marzetti, E. (2016) · Nutrients · doi:10.3390/nu8050295 · Cited by 218 · see citing works
“Tieland and colleagues [43,44] reported the findings of two trials on the effect of protein supplementation on muscle mass and physical performance in frail older participants.”
Background
Exercise and nutrition strategies to counteract sarcopenic obesity
Trouwborst, I., Verreijen, A., Memelink, R., Massanet, P., Boirie, Y., Weijs, P., & Tieland, M. (2018) · Nutrients · doi:10.3390/nu10050605 · Cited by 210 · see citing works
Self-citation
Mechanisms of mechanical overload-induced skeletal muscle hypertrophy: current understanding and future directions
Roberts, M. D., McCarthy, J. J., Hornberger, T. A., Phillips, S. M., Mackey, A. L., Nader, G. A., Boppart, M. D., Kavazis, A. N., Reidy, P. T., Ogasawara, R., et al. (2023) · Physiological Reviews · doi:10.1152/physrev.00039.2022 · Cited by 214 · see citing works
Age-related changes in skeletal muscle: changes to life-style as a therapy
McCormick, R., & Vasilaki, A. (2018) · Biogerontology · doi:10.1007/s10522-018-9775-3 · Cited by 210 · see citing works
Implications of ICD-10 for Sarcopenia Clinical Practice and Clinical Trials: Report by the International Conference on Frailty and Sarcopenia Research Task Force
Vellas, B. J., Fielding, R. A., Bens, C., Bernabei, R., Cawthon, P. M., Cederholm, T., Cruz-Jentoft, A. J., Signore, S. D., Donahue, S., Morley, J. E., et al. (2018) · The Journal of Frailty & Aging · doi:10.14283/jfa.2017.30 · Cited by 195 · see citing works
“As described in Table 1, nutritional supplementation (alone or in combination with exercise) is a widely-studied treatment strategy (13, 14, 18-21).”
Background
The role of dietary protein intake in the prevention of sarcopenia of aging
Beasley, J. M., Shikany, J., & Thomson, C. (2013) · Nutrition in clinical practice · doi:10.1177/0884533613507607 · Cited by 183 · see citing works
The Role of Muscle Mass Gain Following Protein Supplementation Plus Exercise Therapy in Older Adults with Sarcopenia and Frailty Risks: A Systematic Review and Meta-Regression Analysis of Randomized Trials
Liao, C.-D., Chen, H.-C., Huang, S.-W., & Liou, T.-H. (2019) · Nutrients · doi:10.3390/nu11081713 · Cited by 189 · see citing works
“The treatment effect of PS + MSE on physical function was assessed using several mobility tests, including walking capability by 18 RCTs (23 comparisons) [31,37–39,41,43,44,47,48,51,52], chair-rise test by seven RCTs (13 comparisons) [37–39,41,48,51,52], timed up-and-go by two RCTs (three comparisons) [38,48], stair-c…”
MethodInfluential
Effects of protein supplementation in older adults undergoing resistance training: a systematic review and meta-analysis
Finger, D., Goltz, F. R., Umpierre, D., Meyer, E., Rosa, L. H. T., & Schneider, C. D. (2015) · Sports Medicine · doi:10.1007/s40279-014-0269-4 · Cited by 185 · see citing works
“[20], also showed positive effects for the cointervention of exercise plus supplementation.”
BackgroundResultInfluential
Effects of exercise and nutrition supplementation in community-dwelling older Chinese people with sarcopenia: a randomized controlled trial
Zhu, L.-Y., Chan, R., Kwok, T., Cheng, K. C.-C., Ha, A., & Woo, J. (2019) · Age and Ageing · doi:10.1093/ageing/afy179 · Cited by 179 · see citing works
A High Whey Protein, Vitamin D and E Supplement Preserves Muscle Mass, Strength, and Quality of Life in Sarcopenic Older Adults: A Double-Blind Randomized Controlled Trial
Bo, Y., Liu, C., Ji, Z., Yang, R., An, Q., Zhang, X., You, J., Duan, D., Sun, Y., Zhu, Y., et al. (2019) · Clinical Nutrition · doi:10.1016/j.clnu.2017.12.020 · Cited by 184 · see citing works
The Effects of Lifestyle and Diet on Gut Microbiota Composition, Inflammation and Muscle Performance in Our Aging Society
Strasser, B., Wolters, M., Weyh, C., Krüger, K., & Ticinesi, A. (2021) · Nutrients · doi:10.3390/nu13062045 · Cited by 181 · see citing works
Effects of an Oral Nutritional Supplementation Plus Physical Exercise Intervention on the Physical Function, Nutritional Status, and Quality of Life in Frail Institutionalized Older Adults: The ACTIVNES Study
Abizanda, P., López, M. D., García, V. P., Estrella, J. D. D., González, Á. D. S., Vilardell, N. B., & Torres, K. A. (2015) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2015.02.005 · Cited by 172 · see citing works
Muscle fibre capillarization is a critical factor in muscle fibre hypertrophy during resistance exercise training in older men
Snijders, T., Nederveen, J. P., Joanisse, S., Leenders, M., Verdijk, L. B., van Loon, L. J. C., & Parise, G. (2016) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12137 · Cited by 170 · see citing works
Self-citation
Individualized home-based exercise and nutrition interventions improve frailty in older adults: a randomized controlled trial
Hsieh, T.-J., Su, S.-C., Chen, C.-W., Kang, Y.-W., Hu, M., Hsu, L., Wu, S.-Y., Chen, L., Chang, H., Chuang, S., et al. (2019) · International Journal of Behavioral Nutrition and Physical Activity · doi:10.1186/s12966-019-0855-9 · Cited by 169 · see citing works
Sarcopenic obesity and complex interventions with nutrition and exercise in community-dwelling older persons &ndash; a narrative review
Freiberger, E., Goisser, S., Porzel, S., Volkert, D., Kemmler, W., Sieber, C., & Bollheimer, C. (2015) · Clinical Interventions in Aging · doi:10.2147/cia.s82454 · Cited by 162 · see citing works
“27,66,69,81 86 Vitamin D deficiency is reported to be a common problem in older persons.”
Protein and exercise in the prevention of sarcopenia and aging
Naseeb, M. A., & Volpe, S. L. (2017) · Nutrition Research · doi:10.1016/j.nutres.2017.01.001 · Cited by 160 · see citing works
Evidence-Based Recommendations for Addressing Malnutrition in Health Care: An Updated Strategy From the feedM.E. Global Study Group
Correia, M. I. T. D., Hegazi, R. A. F., Higashiguchi, T., Michel, J., Reddy, B. R., Tappenden, K. A., Uyar, M., & Muscaritoli, M. (2014) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2014.05.011 · Cited by 157 · see citing works
Nutritional Supplementation With Physical Activity Improves Muscle Composition in Mobility-Limited Older Adults, The VIVE2 Study: A Randomized, Double-Blind, Placebo-Controlled Trial
Englund, D. A., Kirn, D. R., Koochek, A., Zhu, H., Travison, T. G., Reid, K. F., von Berens, Å., Melin, M., Cederholm, T., Gustafsson, T., et al. (2018) · The Journals of Gerontology: Series A · doi:10.1093/gerona/glx141 · Cited by 151 · see citing works
Health promotion interventions for community-dwelling older people with mild or pre-frailty: a systematic review and meta-analysis
Frost, R., Belk, C., Jovicić, A., Ricciardi, F., Kharicha, K., Gardner, B., Iliffe, S., Goodman, C. M., Manthorpe, J., Drennan, V. M., et al. (2017) · BMC Geriatrics · doi:10.1186/s12877-017-0547-8 · Cited by 156 · see citing works
Effects of protein supplementation on lean body mass, muscle strength, and physical performance in nonfrail community-dwelling older adults: a systematic review and meta-analysis
ten Haaf, D. S. M., Nuijten, M. A. H., Maessen, M. F. H., Horstman, A. M. H., Eijsvogels, T. M. H., & Hopman, M. T. (2018) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqy192 · Cited by 152 · see citing works
Therapeutic Interventions for Frail Elderly Patients: Part I. Published Randomized Trials
Bibas, L., Levi, M., Bendayan, M., Mullie, L., Forman, D. E., & Afilalo, J. (2014) · Progress in Cardiovascular Diseases · doi:10.1016/j.pcad.2014.07.004 · Cited by 150 · see citing works
l-Carnitine Supplementation in Recovery after Exercise
Fielding, R. A., Riede, L., Lugo, J. P., & Bellamine, A. (2018) · Nutrients · doi:10.3390/nu10030349 · Cited by 146 · see citing works
“Moreover, supplemental protein intake can increase muscle mass and strength in elderly [82,83] and improve their physical performance [84].”
Background
Nutritional Supplements in Support of Resistance Exercise to Counter Age-Related Sarcopenia
Phillips, S. M. (2015) · Advances in Nutrition · doi:10.3945/an.115.008367 · Cited by 144 · see citing works
“This thesis is supported by findings of no increase in muscle mass when RT was performed without protein supplementation compared with protein supplementation (30 g of protein: 15 g, twice daily) in frail elderly individuals (49).”
Background
Relation between mealtime distribution of protein intake and lean mass loss in free-living older adults of the NuAge study
Farsijani, S., Morais, J. A., Payette, H., Gaudreau, P., Shatenstein, B., Gray-Donald, K., & Chevalier, S. (2016) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.116.130716 · Cited by 136 · see citing works
The effectiveness of leucine on muscle protein synthesis, lean body mass and leg lean mass accretion in older people: a systematic review and meta-analysis
Xu, Z.-R., Tan, Z.-J., Zhang, Q., Gui, Q.-F., & Yang, Y.-M. (2015) · British Journal of Nutrition · doi:10.1017/s0007114514002475 · Cited by 136 · see citing works
Exercise and Protein Intake: A Synergistic Approach against Sarcopenia
Martone, A. M., Marzetti, E., Calvani, R., Picca, A., Tosato, M., Santoro, L., Giorgio, A. D., Nesci, A., Sisto, A., Santoliquido, A., et al. (2017) · BioMed Research International · doi:10.1155/2017/2672435 · Cited by 136 · see citing works
“[42] showed that 24-week protein supplementation combined with resistance training increased muscle mass, strength, and physical performance in frail elderly participants.”
Background
Nutritional Interventions for Elderly and Considerations for the Development of Geriatric Foods
Kaur, D., Rasane, P., Singh, J., Kaur, S., Kumar, V., Mahato, D. K., Dey, A., Dhawan, K., & Kumar, S. (2019) · Current Aging Science · doi:10.2174/1874609812666190521110548 · Cited by 134 · see citing works
Creatine supplementation in the aging population: effects on skeletal muscle, bone and brain
Gualano, B., Rawson, E. S., Candow, D. G., & Chilibeck, P. D. (2016) · Amino Acids · doi:10.1007/s00726-016-2239-7 · Cited by 133 · see citing works
“Moreover, there is strong evidence pointing out the efficacy of specific dietary interventions in adding to the well-known beneficial effects of training to older individuals, with proteins, amino acids and creatine being the most studied nutrients in this context (Gualano et al. 2014; Tieland et al. 2012).”
Background
Healthy Aging—Nutrition Matters: Start Early and Screen Often
Roberts, S. B., Silver, R. E., Das, S. K., Fielding, R. A., Gilhooly, C. H., Jacques, P. F., Kelly, J. M., Mason, J. B., McKeown, N. M., Reardon, M. A., et al. (2021) · Advances in Nutrition · doi:10.1093/advances/nmab032 · Cited by 133 · see citing works
Let thy food be thy medicine….when possible
Witkamp, R. F., & van Norren, K. (2018) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2018.06.026 · Cited by 130 · see citing works
Effect of whey protein supplementation combined with resistance training on body composition, muscular strength, functional capacity, and plasma-metabolism biomarkers in older women with sarcopenic obesity: a randomized, double-blind, placebo-controlled trial
Nabuco, H. C. G., Tomeleri, C. M., Fernandes, R. R., Sugihara Junior, P., Cavalcante, E. F., Cunha, P. M., Antunes, M., Nunes, J. P., Venturini, D., Barbosa, D. S., et al. (2019) · Clinical Nutrition ESPEN · doi:10.1016/j.clnesp.2019.04.007 · Cited by 125 · see citing works
Does the muscle protein synthetic response to exercise and amino acid-based nutrition diminish with advancing age? A systematic review.
Shad, B. J., Thompson, J. L., & Breen, L. (2016) · American Journal of Physiology. Endocrinology and Metabolism · doi:10.1152/ajpendo.00213.2016 · Cited by 125 · see citing works
“Chronically, protein supplementation enhances resistance training-induced muscle hypertrophy and strength increases in young and older individuals (22, 94, 112).”
Background
Frailty and sarcopenia in elderly
Morley, J. E. (2016) · Wiener klinische Wochenschrift · doi:10.1007/s00508-016-1087-5 · Cited by 127 · see citing works
Biomarker-Calibrated Protein Intake and Physical Function in the Women’s Health Initiative
Beasley, J. M., Wertheim, B., Lacroix, A. Z., Prentice, R., Neuhouser, M., Tinker, L., Kritchevsky, S., Shikany, J., Eaton, C., Chen, Z., et al. (2013) · Journal of The American Geriatrics Society · doi:10.1111/jgs.12503 · Cited by 114 · see citing works
“Two randomized controlled trials of protein supplementation (30 g/d) and protein supplementation (30 g/d) plus exercise found an approximately 1-point increase in SPPB after 24 intervention weeks, compared with no changes in the placebo group.(18,19) These data support the hypothesis that greater protein intake as per…”
Result
Dietary Protein Intake in Dutch Elderly People: A Focus on Protein Sources
Tieland, M., den Berg, K. J. B.-V., van Loon, L. V., & de Groot, L. (2015) · Nutrients · doi:10.3390/nu7125496 · Cited by 116 · see citing works
“Increasing protein intake at breakfast and lunch during exercise stimulated muscle protein synthesis [28,29] and augmented muscle mass gain in frail elderly people [16].”
BackgroundSelf-citation
The impact of dietary protein or amino acid supplementation on muscle mass and strength in elderly people: Individual participant data and meta-analysis of RCT's
Tieland, M., Franssen, R., Dullemeijer, C., van Dronkelaar, C., Kim, H. K., Ispoglou, T., Zhu, K., Prince, R. L., van Loon, L. J. C., & de Groot, L. C. P. G. M. (2017) · The Journal of nutrition, health and aging · doi:10.1007/s12603-017-0896-1 · Cited by 123 · see citing works
Self-citation
Frailty, Sarcopenia, and Hormones
Morley, J. E., & Malmstrom, T. K. (2013) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2013.02.006 · Cited by 122 · see citing works
Associations of sarcopenia and sarcopenic obesity with metabolic syndrome considering both muscle mass and muscle strength
Lee, J., Hong, Y.-P., Shin, H. J., & Lee, W. (2015) · Journal of Preventive Medicine and Public Health · doi:10.3961/jpmph.15.055 · Cited by 119 · see citing works
“It has been proven that exercise and protein supplements are effective in managing sarcopenia [40].”
Background
Comparative effectiveness study of low versus high-intensity aerobic training with resistance training in community-dwelling older men with post-COVID 19 sarcopenia: A randomized controlled trial
Nambi, G. S., Abdelbasset, W. K., Alrawaili, S. M., ELSAYED, S. H., Verma, A., Vellaiyan, A., Marwa Mahmoud, E. I. D., Aldhafian, O. R., Nwihadh, N. B., & Saleh, A. K. (2021) · Clinical Rehabilitation · doi:10.1177/02692155211036956 · Cited by 118 · see citing works
Nutrition in chronic pancreatitis.
Rasmussen, H., Irtun, Ø., Olesen, S. S., Drewes, A., & Holst, M. (2013) · World Journal of Gastroenterology · doi:10.3748/wjg.v19.i42.7267 · Cited by 107 · see citing works
Lack of knowledge and availability of diagnostic equipment could hinder the diagnosis of sarcopenia and its management
Reijnierse, E. M., de van der Schueren, M. A. E., Trappenburg, M. C., Doves, M., Meskers, C. G. M., & Maier, A. B. (2017) · PLoS ONE · doi:10.1371/journal.pone.0185837 · Cited by 116 · see citing works
Combining nutrition and exercise to optimize survival and recovery from critical illness: Conceptual and methodological issues
Heyland, D. K., Stapleton, R. D., Mourtzakis, M., Hough, C. L., Morris, P. E., Deutz, N. E. P., Colantuoni, E., Day, A. G., Prado, C. M. M., & Needham, D. M. (2015) · Clinical Nutrition · doi:10.1016/j.clnu.2015.07.003 · Cited by 114 · see citing works
Low vitamin D status is associated with reduced muscle mass and impaired physical performance in frail elderly people
Tieland, M., Brouwer-Brolsma, E. M., Nienaber‐Rousseau, C., van Loon, L. J. C., & de Groot, C. P. G. M. (2013) · European Journal of Clinical Nutrition · doi:10.1038/ejcn.2013.144 · Cited by 110 · see citing works
Self-citation
Influence of Amino Acids, Dietary Protein, and Physical Activity on Muscle Mass Development in Humans
Dideriksen, K., Reitelseder, S., & Holm, L. (2013) · Nutrients · doi:10.3390/nu5030852 · Cited by 110 · see citing works
“supplementation (15 g milk protein concentrate twice daily) had additive effects to exercise only in the group of frail elderly [136,137].”
Background
Development of a Japanese version of the SARC-F for diabetic patients: an examination of reliability and validity
Ida, S., Murata, K., Nakadachi, D., Ishihara, Y., Imataka, K., Uchida, A., Monguchi, K., Kaneko, R., Fujiwara, R., & Takahashi, H. (2016) · Aging Clinical and Experimental Research · doi:10.1007/s40520-016-0668-5 · Cited by 110 · see citing works
Protein supplementation does not significantly augment the effects of resistance exercise training in older adults: a systematic review
Thomas, D. K., Quinn, M. A., Saunders, D. H., & Greig, C. A. (2016) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2016.07.002 · Cited by 108 · see citing works
The skeletal muscle satellite cell response to a single bout of resistance-type exercise is delayed with aging in men
Snijders, T., Verdijk, L. B., Smeets, J. S. J., McKay, B. R., Senden, J. M., Hartgens, F., Parise, G., Greenhaff, P. L., & van Loon, L. J. C. (2014) · AGE · doi:10.1007/s11357-014-9699-z · Cited by 106 · see citing works
Self-citation
Effects of physical activity interventions in frail and prefrail community-dwelling people on frailty status, muscle strength, physical performance and muscle mass—a narrative review
Haider, S., Grabovac, I., & Dorner, T. E. (2019) · Wiener klinische Wochenschrift · doi:10.1007/s00508-019-1484-7 · Cited by 106 · see citing works
Four-Month Course of Soluble Milk Proteins Interacts With Exercise to Improve Muscle Strength and Delay Fatigue in Elderly Participants
Gryson, C., Ratel, S., Rance, M., Penando, S., Bonhomme, C., Ruyet, P. L., Duclos, M., Boirie‌, Y., & Walrand, S. (2014) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2014.09.011 · Cited by 105 · see citing works
Impact of resistance training on sarcopenia in nursing care facilities: A pilot study
Hassan, B. H., Hewitt, J., Keogh, J., Bermeo, S., Duque, G., & Henwood, T. R. (2015) · Geriatric Nursing · doi:10.1016/j.gerinurse.2015.11.001 · Cited by 102 · see citing works
Effect of resistance-type exercise training with or without protein supplementation on cognitive functioning in frail and pre-frail elderly: Secondary analysis of a randomized, double-blind, placebo-controlled trial
van de Rest, O., van der Zwaluw, N. L., Tieland, M., Adam, J. J., Hiddink, G. J., van Loon, L. J. C., & de Groot, C. P. G. M. (2014) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2013.12.005 · Cited by 100 · see citing works
Self-citation
The Muscle Metabolome Differs between Healthy and Frail Older Adults
Fazelzadeh, P., Hangelbroek, R., Tieland, M., de Groot, C. P. G. M., Verdijk, L. B., van Loon, L. J. C., Smilde, A. K., Alves, R. D. A. M., Vervoort, J. J. M., Müller, M. M., et al. (2016) · Journal of Proteome Research · doi:10.1021/acs.jproteome.5b00840 · Cited by 94 · see citing works
Self-citation
Nutrition and protein energy homeostasis in elderly
Boirie, Y., Morio, B., Caumon, E., & Cano, N. J. (2014) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2014.01.008 · Cited by 94 · see citing works
Effects of Protein Supplementation Combined with Exercise Intervention on Frailty Indices, Body Composition, and Physical Function in Frail Older Adults
Liao, C.-D., Lee, P.-H., Hsiao, D.-J., Huang, S.-W., Tsauo, J.-Y., Chen, H.-C., & Liou, T.-H. (2018) · Nutrients · doi:10.3390/nu10121916 · Cited by 94 · see citing works
“The treatment effect of PS plus exercise training on physical function was assessed using several mobility tests, namely chair rise time by eight RCTs [41,43,45,48,50,56,58,59], timed up-and-go by four RCTs [52,54,55,59], and short physical performance battery by three RCTs [46,48,58], as well as ADL by five RCTs [42,…”
BackgroundMethodInfluential
Rapid Geriatric Assessment
Morley, J. E., & Adams, E. V. (2015) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2015.08.004 · Cited by 93 · see citing works
European Respiratory Society statement on frailty in adults with chronic lung disease
Osadnik, C. R., Brighton, L. J., Burtin, C., Cesari, M., Lahousse, L., Man, W. D., Marengoni, A., Šajnić, A., Singer, J. P., ter Beek, L., et al. (2023) · European Respiratory Journal · doi:10.1183/13993003.00442-2023 · Cited by 93 · see citing works
“The effect of resistance training on muscle mass is enhanced by adequate protein and energy intake, to ensure the protein required to enhance muscle development is not used as a source of energy [177 – 179].”
Background
Role of protein and amino acids in promoting lean mass accretion with resistance exercise and attenuating lean mass loss during energy deficit in humans
Churchward-Venne, T. A., Murphy, C. H., Longland, T. M., & Phillips, S. M. (2013) · Amino Acids · doi:10.1007/s00726-013-1506-0 · Cited by 90 · see citing works
Protein interventions augment the effect of resistance exercise on appendicular lean mass and handgrip strength in older adults: a systematic review and meta-analysis of randomized controlled trials
Kirwan, R., Mazidi, M., Rodríguez‐García, C., Lane, K. E., Jafari, A., Butler, T., de Heredia, F. P., & Davies, I. G. (2021) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqab355 · Cited by 93 · see citing works
Effect of Protein Supplementation Combined With Resistance Training on Muscle Mass, Strength and Function in the Elderly: A Systematic Review and Meta-Analysis
Hou, L., Lei, Y., Li, X., Huo, C., Jia, X.-M., Yang, J., Xu, R., & Wang, X. (2019) · The journal of nutrition health & aging · doi:10.1007/s12603-019-1181-2 · Cited by 88 · see citing works
The Role of Protein Intake and its Timing on Body Composition and Muscle Function in Healthy Adults: A Systematic Review and Meta-Analysis of Randomized Controlled Trials
Wirth, J., Hillesheim, E., & Brennan, L. (2020) · The Journal of Nutrition · doi:10.1093/jn/nxaa049 · Cited by 87 · see citing works
“Four studies were conducted with postmenopausal women (24–27) and 2 with frail elderly (28, 29).”
Background
Sarcopenia Associated with Chronic Obstructive Pulmonary Disease
Kim, S. H., Shin, M., Shin, Y. B., & Kim, K. U. (2019) · Journal of Bone Metabolism · doi:10.11005/jbm.2019.26.2.65 · Cited by 87 · see citing works
Frailty and heart disease
von Haehling, S., Anker, S. D., Doehner, W., Morley, J. E., & Vellas, B. J. (2013) · International Journal of Cardiology · doi:10.1016/j.ijcard.2013.07.068 · Cited by 88 · see citing works
Influence of combined resistance training and healthy diet on muscle mass in healthy elderly women: a randomized controlled trial
Strandberg, E., Edholm, P., Ponsot, E., Wåhlin‐Larsson, B., Hellmén, E., Nilsson, A. E., Engfeldt, P., Cederholm, T., Risérus, U., & Kadi, F. (2015) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00066.2015 · Cited by 89 · see citing works
Expression of protocadherin gamma in skeletal muscle tissue is associated with age and muscle weakness
Hangelbroek, R., Fazelzadeh, P., Tieland, M., Boekschoten, M. V., Hooiveld, G. J. E. J., van Duynhoven, J., Timmons, J. A., Verdijk, L. B., de Groot, C. P. G. M., van Loon, L. J. C., et al. (2016) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12099 · Cited by 82 · see citing works
“Biopsies from frail and pre-frail older subjects were collected from participants of two studies performed by Tieland et al.15,17 For these studies frail and pre-frail older subjects were selected based on the Fried criteria for frailty.2 These subjects will hereafter be referred to as frail older subjects.”
BackgroundMethodSelf-citation
Effect of nutritional supplementations on physical performance and muscle strength parameters in older people: A systematic review and meta-analysis
Veronese, N., Stubbs, B., Punzi, L., Soysal, P., Incalzi, R. A., Saller, A., & Maggi, S. (2019) · Ageing Research Reviews · doi:10.1016/j.arr.2019.02.005 · Cited by 85 · see citing works
The Effect of β-Hydroxy-β-Methylbutyrate (HMB) on Sarcopenia and Functional Frailty in Older Persons: A Systematic Review
Oktaviana, J., Zanker, J., Vogrin, S., & Duque, G. (2018) · The journal of nutrition health & aging · doi:10.1007/s12603-018-1153-y · Cited by 84 · see citing works
“Many strategies have been studied to reverse the ageassociated muscle loss, including resistance training (11, 12) and nutritional supplementation (13-15).”

From the October Issue of JAMDA
Eisenberg, J. S. (2012) · Caring for the Ages · doi:10.1016/j.carage.2012.10.005
Protein Supplementation Improves Physical Performance in Frail Elderly People: A Randomized, Double-Blind, Placebo-Controlled Trial
Tieland, M., van de Rest, O., Dirks, M. L., van der Zwaluw, N., Mensink, M., van Loon, L. J. C., & de Groot, L. C. P. G. M. (2012) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2012.07.005 · Cited by 446 · see citing works
Self-citation
Protein supplementation increases muscle mass gain during prolonged strength training in frail elderly people
Tieland, M., (18463707), L. D. G., & van Loon, L. J. C. (2024) · Figshare
Self-citation
Protein Supplementation during Resistance-Type Exercise Training in the Elderly
Leenders, M., Verdijk, L. B., van der Hoeven, L., van Kranenburg, J. M. X., Nilwik, R., Wodzig, W. K. W. H., Senden, J. M., KEIZER, H. A., & van Loon, L. J. C. (2013) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e318272fcdb · Cited by 129 · see citing works
Self-citation
Perspective: Exercise and Protein Supplementation in Frail Elders
Paddon‐Jones, D. (2012) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2012.09.028 · Cited by 17 · see citing works

Authors: Tieland, M., Dirks, M. L., van der Zwaluw, N., Verdijk, L. B., van de Rest, O., de Groot, L. C. P. G. M., & van Loon, L. J. C.
Affiliations: TiFN (NL)
Maastricht University Medical Centre (NL)
Corresponding author: Tieland, Michael
ORCID: Tieland, Michael
Dirks, Marlou L.
Verdijk, Lex B.
Venue: Journal of the American Medical Directors Association
Publisher: Elsevier BV
Published: 2012-10
Volume: 13
Issue: 8
Pages: 713-719
ISSN: 1525-8610 (ISSN-L)
DOI: 10.1016/j.jamda.2012.05.020
OpenAlex: W2054574324
Cited by: 556
References: 42
Citations by year: 2026: 21 · 2025: 35 · 2024: 17 · 2023: 26 · 2022: 24 · 2021: 42 · 2020: 44 · 2019: 42 · 2018: 57 · 2017: 64 · 2016: 52 · 2015: 41 · 2014: 39 · 2013: 33 · 2012: 16
FWCI: 19.56
Type: journal article
Language: en
Open access: green
figshare.com
Licence: cc-by
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Journal of the American Medical Directors Association (publishedVersion)
PubMed (publishedVersion)
Research Bank (Australian Catholic University) (submittedVersion)
Research Publications (Maastricht University) (submittedVersion)
Figshare (submittedVersion, cc-by)
Socio-Environmental Systems Modeling (submittedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion)
Funders: Wageningen University and Research
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
Health Sciences › Medicine › Physiology › Nutrition and Health in Aging
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Keywords: protein supplementation, frail elderly, muscle mass gain, lean body mass, muscle strength, physical performance, sarcopenia, older adults
MeSH terms: Aged, Dietary Proteins, Double-Blind Method, Exercise Therapy, Female, Humans, Male, Netherlands, Frail Elderly, Muscle, Skeletal, Dietary Supplements, Muscle Strength, Resistance Training

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Protein Supplementation Increases Muscle Mass Gain During Prolonged Resistance-Type Exercise Training in Frail Elderly People: A Randomized, Double-Blind, Placebo-Controlled Trial

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