Protein supplementation augments the adaptive response of skeletal muscle to resistance-type exercise training: a meta-analysis

Cermak, Naomi M; Res, Peter T; de Groot, Lisette CPGM; Saris, Wim HM; van Loon, Luc JC

doi:10.3945/ajcn.112.037556

Cited by 827Muscle metabolism and nutritionSports Performance and TrainingMuscle Physiology and Disorders

Protein supplementation augments the adaptive response of skeletal muscle to resistance-type exercise training: a meta-analysis

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Cermak, Naomi M, Res, Peter T, de Groot, Lisette CPGM, Saris, Wim HM, van Loon, Luc JC·2012·The American Journal of Clinical Nutrition

DOI 10.3945/ajcn.112.037556

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Abstract

Background Protein ingestion after a single bout of resistance-type exercise stimulates net muscle protein accretion during acute postexercise recovery. Consequently, it is generally accepted that protein supplementation is required to maximize the adaptive response of the skeletal muscle to prolonged resistance-type exercise training. However, there is much discrepancy in the literature regarding the proposed benefits of protein supplementation during prolonged resistance-type exercise training in younger and older populations.Objective The objective of the study was to define the efficacy of protein supplementation to augment the adaptive response of the skeletal muscle to prolonged resistance-type exercise training in younger and older populations.Design A systematic review of interventional evidence was performed through the use of a random-effects meta-analysis model. Data from the outcome variables fat-free mass (FFM), fat mass, type I and II muscle fiber cross-sectional area, and 1 repetition maximum (1-RM) leg press strength were collected from randomized controlled trials (RCTs) investigating the effect of dietary protein supplementation during prolonged (>6 wk) resistance-type exercise training.Results Data were included from 22 RCTs that included 680 subjects. Protein supplementation showed a positive effect for FFM (weighted mean difference: 0.69 kg; 95% CI: 0.47, 0.91 kg; P < 0.00001) and 1-RM leg press strength (weighted mean difference: 13.5 kg; 95% CI: 6.4, 20.7 kg; P < 0.005) compared with a placebo after prolonged resistance-type exercise training in younger and older subjects.Conclusion Protein supplementation increases muscle mass and strength gains during prolonged resistance-type exercise training in both younger and older subjects.

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The insertion of clinical trials testing multi-ingredient supplements, including energy-restricted weight-loss diets, or using different cut-off points for age sub-groups likely explains differences in main effects and conclusions when comparing studies.
“The insertion of clinical trials testing multi‐ingredient supplements, 106 including energy‐restricted weight‐loss diets, 13 or using different cut‐off points for age sub‐groups likely explain the differences in main effects and conclusions when comparing studies. 14 , 21 , 22 , 23”
From Systematic review and meta-analysis of protein intake to support muscle mass and function in healthy adults (2022) · cites this paper as [23]
The Sensitivity analysis section reports that changing the older-adult cutoff from 50 to 60 years produced findings similar to the primary analysis; it concludes that the overall fat-free-mass outcome was not dependent on the age cutoff or protein source. That runs contrary to the attributed explanation that different cutoffs likely account for differences in conclusions. The Study eligibility and data extraction section also says supplements combined with other muscle-growth-promoting ingredients, such as creatine, were excluded; it does not establish the claim about energy-restricted weight-loss diets. (LLM, conf=0.84)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measured
Protein supplementation rarely substantially affects strength outcomes, which highlights that the extra LBM gain stimulated by protein supplementation may not be muscle, or at least not sufficient muscle that is contributing to increases in strength.
“This question is relevant as protein supplementation rarely substantially affects strength outcomes, 14 , 21 , 22 , 23 which highlights that the extra LBM gain stimulated by protein supplementation may not be muscle, 111 or at least not sufficient muscle that is contributing to increases in strength.”
From Systematic review and meta-analysis of protein intake to support muscle mass and function in healthy adults (2022) · cites this paper as [23]
Split into 2 atoms — 0 confirmed, 0 partially supported, 2 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measured
Higher amounts of protein are needed by exercising individuals to optimize exercise training adaptations.
“A growing body of literature is available that suggests higher amounts of protein are needed by exercising individuals to optimize exercise training adaptations [11, 83, 211, 226].”
From ISSN exercise & sports nutrition review update: research & recommendations (2018) · cites this paper as [211]
The Discussion concludes that protein supplementation augments skeletal-muscle adaptations to prolonged resistance-type training in healthy younger and older adults. The citing sentence extends that finding to exercising individuals and exercise-training adaptations generally; this paper does not establish that broader claim. (LLM, conf=0.85)
Experimental — accuracy not yet measured
The anabolic effects of insulin and amino acids on protein synthesis are enhanced by physical activity and some nutrients (omega-3 fatty acids, vitamin D) and are impaired by sedentary lifestyle, bed rest, or immobilization.
“The anabolic effects of insulin and amino acids on protein synthesis are enhanced by physical activity and some nutrients (omega-3 fatty acids, vitamin D) and are impaired by sedentary lifestyle, bed rest, or immobilization (Figure 2).53,120,121”
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 [53]
The Introduction and Discussion (page not specified) state that protein or amino acids after resistance exercise stimulate muscle protein synthesis, supporting the physical-activity portion of the claim. Our copy does not support the claimed effects of insulin, omega-3 fatty acids, vitamin D, bed rest, or immobilization on protein synthesis; its mention of sedentary lifestyle concerns age-related muscle loss instead. (LLM, conf=0.88)
Experimental — accuracy not yet measured
Pooled results of multiple studies using meta-analytic and other systematic approaches consistently indicate that protein supplementation (15 to 25 g over 4 to 21 weeks) exerts a positive impact on performance.
“Pooled results of multiple studies using meta-analytic and other systematic approaches consistently indicate that protein supplementation (15 to 25 g over 4 to 21 weeks) exerts a positive impact on performance.”
From International Society of Sports Nutrition Position Stand: protein and exercise (2017) · cites this paper as [35]
The Discussion reports that pooled results found greater gains in muscle mass and leg-press strength with protein supplementation during resistance training. However, the Protein supplementation characteristics section gives a dose range of 6–106 g, not 15–25 g, and the Resistance-type exercise training characteristics section gives a duration of 6–24 weeks, not 4–21 weeks. The analysis assessed strength, not performance broadly; page numbers were not supplied. (LLM, conf=0.90)
Experimental — accuracy not yet measured

The lack of agreement on the efficacy of protein supplementation is likely due to divergent study inclusion criteria and inclusion of subjects with differing ages, training statuses, total protein intakes, protein sources and protein doses.
“This lack of agreement on the efficacy of protein supplementation6–12 is likely due to the use of divergent study inclusion criteria and inclusion of subjects with differing: ages, training statuses, total protein intakes, protein sources and protein doses.”
From A systematic review, meta-analysis and meta-regression of the effect of protein supplementation on resistance training-induced gains in muscle mass and strength in healthy adults (2018) · cites this paper as [7]
The Introduction (page not provided) attributes conflicting findings to differences in participants’ ages and training status and in the amount and type of protein supplementation. It does not identify divergent study inclusion criteria or differences in total protein intake as reasons for that disagreement; the amount of a supplement is not necessarily total protein intake. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Previous data from our group 14 and Cermak et al. 23 showed very small but significant effect of additional protein ingestion on strength, mainly lower body strength data when selecting RE studies.
“Previous data from our group 14 and Cermak et al. 23 showed very small but significant effect of additional protein ingestion on strength, mainly lower body strength data when selecting RE studies.”
From Systematic review and meta-analysis of protein intake to support muscle mass and function in healthy adults (2022) · cites this paper as [23]
The 1-RM strength section reports a significant additional gain in leg-press strength with protein supplementation during resistance-type exercise training. The Publication bias and heterogeneity section says leg-extension and bench-press results were too heterogeneous to pool, supporting the lower-body emphasis. The paper does not characterize the strength effect as “very small”; it reports a 13.5 kg pooled difference. (LLM, conf=0.83)
Experimental — accuracy not yet measured
According to previous meta-analyses, the effects of increasing daily protein ingestion on muscle strength are highly variable.
“According to previous meta‐analyses from our group and others, the effects of increasing daily protein ingestion on muscle strength are highly variable. 14 , 21 , 22 , 23”
From Systematic review and meta-analysis of protein intake to support muscle mass and function in healthy adults (2022) · cites this paper as [23]
The Introduction and Discussion describe conflicting findings on whether protein supplementation improves muscle strength, supporting the claim that reported effects vary. The paper addresses supplementation during prolonged resistance-type exercise training, however, not the effects of increasing daily protein intake on strength generally. Page numbers are unavailable in our copy. (LLM, conf=0.85)
Experimental — accuracy not yet measured
The amount of CAS supplementation used in this study is relatively low compared with those used in previous studies (10-63 g/d or 0.3 g/kg/d).
“On the other hand, amount of CAS supplementation used in this study is relatively low in comparison with those used in the previous studies (10–63 g/d or 0.3 g/kg/d) (10,11).”
From Modulation of Neural and Muscular Adaptation Processes During Resistance Training by Fish Protein Ingestions in Older Adults (2020) · cites this paper as [10]
The Subject characteristics table lists previous studies using 10 g/d and 63 g/d, so the paper supports those doses as examples. But Protein supplementation characteristics gives the overall range as 6–106 g on training days, not 10–63 g/d, and the retrieved passages do not report a 0.3 g/kg/d dose. The paper also cannot establish the comparison with the citing study’s dose. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Protein supplementation mainly induces muscular adaptations such as muscle hypertrophy.
“Because protein supplementation mainly induces muscular adaptations such as muscle hypertrophy, contributions of neural and muscular factors to training-induced adaptation would not be coincidence between resistance training interventions with and without protein supplementation.”
From Modulation of Neural and Muscular Adaptation Processes During Resistance Training by Fish Protein Ingestions in Older Adults (2020) · cites this paper as [10]
The Discussion reports greater muscle-fiber cross-sectional area with protein supplementation during resistance training, supporting the hypertrophy example. It also reports greater strength gains, but does not assess neural adaptations or establish that supplementation acts mainly through muscular rather than neural changes. (LLM, conf=0.83)
Experimental — accuracy not yet measured
Protein supplementation increases muscle mass and strength gains during prolonged resistance-type exercise training in both younger and older subjects.
“Cermak 2012 53 Protein supplementation increases muscle mass and strength gains during prolonged resistance-type exercise training in both younger and older subjects”
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 Cermak 2012 53
The present meta-analysis includes more than double the number of studies and participants than the largest published comprehensive meta-analysis on protein supplementation during RET to date.
“The present meta-analysis includes more than double the number of studies and participants than the largest published comprehensive meta-analysis on protein supplementation during RET to date.7ST1”
From A systematic review, meta-analysis and meta-regression of the effect of protein supplementation on resistance training-induced gains in muscle mass and strength in healthy adults (2018) · cites this paper as [7]
Most meta-analyses have reported consistently positive results regarding the effect of additional protein ingestion on RE training-induced increases in LBM.
“Most meta‐analyses have reported consistently positive results regarding the effect of additional protein ingestion on RE training‐induced increases in LBM. 13 , 14 , 21 , 23”
From Systematic review and meta-analysis of protein intake to support muscle mass and function in healthy adults (2022) · cites this paper as [23]
An abundance of evidence is available to indicate that ingestion of high-quality protein sources can heighten adaptations to resistance training.
“An abundance of evidence is available, however, to indicate that ingestion of high-quality protein sources can heighten adaptations to resistance training [211].”
From ISSN exercise & sports nutrition review update: research & recommendations (2018) · cites this paper as [211]
A meta-analysis of 22 RCTs involving 680 young and old subjects demonstrated that prolonged resistance training (>6 weeks) combined with cotemporal protein supplement consumption led to significant muscle mass gains, which were associated with significant strength gains.
“Results of a meta-analysis of 22 RCTs involving 680 young and old subjects demonstrated that prolonged resistance training (>6 weeks) combined with cotemporal protein supplement consumption led to significant muscle mass gains, which were associated with significant strength gains. 53”
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 [53]
Protein supplementation during a resistance-training program results in a mean increase in fat-free mass of 0.69 kg (95% CI 0.47-0.91 kg) compared to placebo.
“a meta-analysis by Cermak and colleagues [35] reported a mean increase in fat-free mass of 0.69 kg (95% Confidence Interval: 0.47–0.91 kg) when protein supplementation was provided versus a placebo during a resistance-training program.”
From International Society of Sports Nutrition Position Stand: protein and exercise (2017) · cites this paper as [35]
Narrative reviews and meta-analyses yield conflicting results as to the effectiveness of protein supplementation to enhance RET-mediated gains in muscle mass and strength.
“Despite a large volume of work in this area, narrative reviews1–5 and even meta-analyses6–12 yield conflicting results as to the actual effectiveness of protein supplementation to enhance RET-mediated gains in muscle mass and strength.”
From A systematic review, meta-analysis and meta-regression of the effect of protein supplementation on resistance training-induced gains in muscle mass and strength in healthy adults (2018) · cites this paper as [7]
Cermak et al. 23 showed a significant main effect for protein supplementation on muscle mass in young and old subjects during resistance exercise-like training.
“Cermak et al. 23 showed a significant main effect for protein supplementation in muscle mass in young and old subjects during resistance exercise‐like training.”
From Systematic review and meta-analysis of protein intake to support muscle mass and function in healthy adults (2022) · cites this paper as [23]
Increases in muscle mass and strength following resistance training are elicited by protein supplementation in older adults.
“There has been growing recognition that increases in muscle mass and strength following resistance training is elicited by protein supplementation in older adults (10,11).”
From Modulation of Neural and Muscular Adaptation Processes During Resistance Training by Fish Protein Ingestions in Older Adults (2020) · cites this paper as [10]
In most previous studies, casein, whey, and/or milk protein have been used as protein supplementations to test the effect of their combination with resistance training.
“In most of the previous studies, casein, whey, and/or milk protein have been used as protein supplementations to test the effect of its combination with resistance training (10,11)”
From Modulation of Neural and Muscular Adaptation Processes During Resistance Training by Fish Protein Ingestions in Older Adults (2020) · cites this paper as [10]
The inability of the group that delayed supplementation but still completed the resistance training program to experience any measurable increase in muscle cross-sectional area has led some to question the outcomes resulting from the Esmarck et al. study.
“While interesting, the inability of the group that delayed supplementation but still completed the resistance training program to experience any measurable increase in muscle cross-sectional area has led some to question the outcomes resulting from this study [5, 123].”
From International society of sports nutrition position stand: nutrient timing (2017) · cites this paper as [5]
Split into 2 atoms — 0 confirmed, 0 partially supported, 0 disputed, 0 misattributed, 2 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measured
Nutrition and exercise interventions are two of the most promising strategies in the management of sarcopenic obesity.
“Nutrition and exercise interventions are the two of the most promising strategies in the management of sarcopenic obesity.17–19”
From Nutritional and exercise interventions in individuals with sarcopenic obesity around retirement age: a systematic review and meta-analysis (2023) · cites this paper as [19]
Nutrition can play a critical role in augmenting the adaptive stimulus that comes from resistance exercise.
“As with endurance exercise, nutrition can play a critical role in augmenting the adaptive stimulus that comes from resistance exercise [84].”
From New strategies in sport nutrition to increase exercise performance (2016) · cites this paper as [84]
Supplementation of protein during a program of resistance training enhances lean mass/muscle gains.
“Furthermore supplementation of protein during a program of resistance training is well proven to enhance lean mass/muscle gains [84].”
From New strategies in sport nutrition to increase exercise performance (2016) · cites this paper as [84]

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Effect of Post-Exercise Supplement Consumption on Adaptations to Resistance Training
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Effect of a 10-Week strength training program and recovery drink on body composition, muscular strength and endurance, and anaerobic power and capacity
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[3]3. Tipton KD, Ferrando AA, Phillips SM, Doyle D, Jr, Wolfe RR. Post- exercise net protein synthesis in human muscle from orally adminis- tered amino acids. 1999;276:E628-34.

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Evidence-Based Recommendations for Optimal Dietary Protein Intake in Older People: A Position Paper From the PROT-AGE Study Group
Bauer, J., Biolo, G., Cederholm, T., Cesari, M., Cruz-Jentoft, A. J., Morley, J. E., Phillips, S., Sieber, C., Stehle, P., Teta, D., et al. (2013) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2013.05.021 · Cited by 2,553 · see citing works
Skeletal muscle: A brief review of structure and function
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A systematic review, meta-analysis and meta-regression of the effect of protein supplementation on resistance training-induced gains in muscle mass and strength in healthy adults
Morton, R. W., Murphy, K. T., McKellar, S. R., Schoenfeld, B. J., Henselmans, M., Helms, E., Aragon, A. A., Devries, M. C., Banfield, L., Krieger, J. W., et al. (2018) · British Journal of Sports Medicine · doi:10.1136/bjsports-2017-097608 · Cited by 1,154 · see citing works
IOC Consensus Statement: Dietary Supplements and the High-performance Athlete
Maughan, R. J., Burke, L. M., Dvorak, J., Larson-Meyer, D. E., Peeling, P., Phillips, S. M., Rawson, E. S., Walsh, N. P., Garthe, I., Geyer, H., et al. (2018) · British Journal of Sports Medicine · doi:10.1136/bjsports-2018-099027 · Cited by 1,004 · see citing works
Self-citation
ISSN exercise & sports nutrition review update: research & recommendations
Kerksick, C. M., Wilborn, C. D., Roberts, M. D., Smith-Ryan, A., Kleiner, S. M., Jäger, R., Collins, R., Cooke, M., Davis, J. N., Galvan, E., et al. (2018) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-018-0242-y · Cited by 945 · see citing works
International Society of Sports Nutrition Position Stand: protein and exercise
Jäger, R., Kerksick, C. M., Campbell, B. I., Cribb, P. J., Wells, S. D., Skwiat, T. M., Purpura, M., Ziegenfuss, T. N., Ferrando, A. A., Arent, S. M., et al. (2017) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-017-0177-8 · Cited by 873 · see citing works
“Cermak and colleagues [35] pooled the outcomes from 22 separate clinical trials to yield 680 subjects in their statistical analysis and found that protein supplementation with resistance training resulted in a 13.”
Background
The Skeletal Muscle Anabolic Response to Plant- versus Animal-Based Protein Consumption
van Vliet, S., Burd, N. A., & van Loon, L. J. (2015) · The Journal of Nutrition · doi:10.3945/jn.114.204305 · Cited by 651 · see citing works
Self-citation
International society of sports nutrition position stand: nutrient timing
Kerksick, C. M., Arent, S., Schoenfeld, B. J., Stout, J. R., Campbell, B., Wilborn, C. D., Taylor, L., Kalman, D., Smith-Ryan, A. E., Kreider, R. B., et al. (2017) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-017-0189-4 · Cited by 622 · see citing works
“While strategies surrounding carbohydrates were the first to be explored, there has been a growing body of research over the last several years that has examined the effect of protein and amino acids, with and without carbohydrates, as a nutrient timing strategy [1, 5].”
BackgroundResult
Nutrition and physical activity in the prevention and treatment of sarcopenia: systematic review.
the IOF-ESCEO Sarcopenia Working Group, Beaudart, C., Dawson, A., Shaw, S. C., Harvey, N. C., Kanis, J. A., Binkley, N., Reginster, J. Y., Chapurlat, R., Chan, D. C., et al. (2017) · Osteoporosis International · doi:10.1007/s00198-017-3980-9 · Cited by 602 · see citing works
IOC Consensus Statement: Dietary Supplements and the High-Performance Athlete
Maughan, R. J., Burke, L. M., Dvorak, J., Larson-Meyer, D. E., Peeling, P., Phillips, S. M., Rawson, E. S., Walsh, N. P., Garthe, I., Geyer, H., et al. (2018) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2018-0020 · Cited by 540 · see citing works
Self-citation
Does nutrition play a role in the prevention and management of sarcopenia?
Robinson, S. M., Reginster, J. Y., Rizzoli, R., Shaw, S. C., Kanis, J. A., Bautmans, I., Bischoff-Ferrari, H., Bruyère, O., Cesari, M., Dawson-Hughes, B., et al. (2018) · Clinical Nutrition · doi:10.1016/j.clnu.2017.08.016 · Cited by 491 · see citing works
Self-citation
Prevalence of dietary supplement use by athletes: Systematic review and meta-analysis
Knapik, J. J., Steelman, R. A., Hoedebecke, S. S., Austin, K. G., Farina, E. K., & Lieberman, H. R. (2016) · Sports Medicine · doi:10.1007/s40279-015-0387-7 · Cited by 452 · see citing works
Neither load nor systemic hormones determine resistance training-mediated hypertrophy or strength gains in resistance-trained young men
Morton, R. W., Oikawa, S. Y., Wavell, C. G., Mazara, N., McGlory, C., Quadrilatero, J., Baechler, B. L., Baker, S. K., & Phillips, S. M. (2016) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00154.2016 · Cited by 404 · see citing works
“Participants consumed 30 g of whey protein (BioPRO, 129 Davisco Foods International, Le Sueur, MN) twice per day: immediately following RT on 130 training days (8) and the other prior to sleep (39).”
Method
Resistance training-induced changes in integrated myofibrillar protein synthesis are related to hypertrophy only after attenuation of muscle damage
Damas, F., Phillips, S. M., Libardi, C. A., Vechin, F. C., Lixandrão, M. E., Jannig, P. R., Costa, L. A. R., Bacurau, A. V., Snijders, T., Parise, G., et al. (2016) · The Journal of Physiology · doi:10.1113/jp272472 · Cited by 353 · see citing works
Effects of protein supplementation combined with resistance exercise on body composition and physical function in older adults: a systematic review and meta-analysis
Liao, C.-D., Tsauo, J.-Y., Wu, Y.-T., Cheng, C.-P., Chen, H.-C., Huang, Y.-C., Chen, H.-C., & Liou, T.-H. (2017) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.116.143594 · Cited by 317 · see citing works
Effects of multi-domain interventions in (pre)frail elderly on frailty, functional, and cognitive status: a systematic review
Dedeyne, L., Deschodt, M., Verschueren, S., Tournoy, J., & Gielen, E. (2017) · Clinical Interventions in Aging · doi:10.2147/cia.s130794 · Cited by 315 · see citing works
International society of sports nutrition position stand: diets and body composition
Aragon, A. A., Schoenfeld, B. J., Wildman, R., Kleiner, S., VanDusseldorp, T., Taylor, L., Earnest, C. P., Arciero, P. J., Wilborn, C., Kalman, D. S., et al. (2017) · Journal of the International Society of Sports Nutrition · doi:10.1186/s12970-017-0174-y · Cited by 301 · see citing works
Systematic review and meta-analysis of protein intake to support muscle mass and function in healthy adults
Nunes, E. A., Colenso‐Semple, L., McKellar, S. R., Yau, T., Ali, M. U., Fitzpatrick‐Lewis, D., Sherifali, D., Gaudichon, C., Tomé, D., Atherton, P. J., et al. (2022) · Journal of Cachexia, Sarcopenia and Muscle · doi:10.1002/jcsm.12922 · Cited by 280 · see citing works
“Most meta-analyses have reported consistently positive results regarding the effect of additional protein ingestion on RE training-induced increases in LBM.13,14,21,23 Cermak et al.23 showed a significant main effect for protein supplementation in muscle mass in young and old subjects during resistance exercise-like t…”
BackgroundResultInfluential
Higher compared with lower dietary protein during an energy deficit combined with intense exercise promotes greater lean mass gain and fat mass loss: a randomized trial
Longland, T. M., Oikawa, S. Y., Mitchell, C. J., Devries, M. C., & Phillips, S. M. (2016) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.115.119339 · Cited by 271 · see citing works
Recent Perspectives Regarding the Role of Dietary Protein for the Promotion of Muscle Hypertrophy with Resistance Exercise Training
Stokes, T., Hector, A., Morton, R., McGlory, C., & Phillips, S. (2018) · Nutrients · doi:10.3390/nu10020180 · Cited by 263 · see citing works
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
Creatine supplementation during resistance training in older adults - a meta-analysis
DEVRIES, M. C., & PHILLIPS, S. M. (2014) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000000220 · Cited by 239 · see citing works
Nutritional interventions to augment resistance training-induced skeletal muscle hypertrophy
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Age-related differences in lean mass, protein synthesis and skeletal muscle markers of proteolysis after bed rest and exercise rehabilitation
Tanner, R. E., Brunker, L. B., Agergaard, J., Barrows, K. M., Briggs, R. A., Kwon, O. S., Young, L. M., Hopkins, P. N., Volpi, E., Marcus, R. L., et al. (2015) · The Journal of Physiology · doi:10.1113/jp270699 · Cited by 223 · see citing works
New strategies in sport nutrition to increase exercise performance
Close, G. L., Hamilton, D. L., Philp, A., Burke, L. M., & Morton, J. P. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.01.016 · Cited by 221 · see citing works
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
Acute Post-Exercise Myofibrillar Protein Synthesis Is Not Correlated with Resistance Training-Induced Muscle Hypertrophy in Young Men
Mitchell, C. J., Churchward-Venne, T. A., Parise, G., Bellamy, L., Baker, S. K., Smith, K., Atherton, P. J., & Phillips, S. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0089431 · Cited by 212 · see citing works
The Effects of Protein Supplements on Muscle Mass, Strength, and Aerobic and Anaerobic Power in Healthy Adults: A Systematic Review
Pasiakos, S. M., McLellan, T. M., & Lieberman, H. R. (2015) · Sports Medicine · doi:10.1007/s40279-014-0242-2 · Cited by 202 · see citing works
The effect of protein timing on muscle strength and hypertrophy: a meta-analysis
Schoenfeld, B. J., Aragon, A. A., & Krieger, J. W. (2013) · Journal of the International Society of Sports Nutrition · doi:10.1186/1550-2783-10-53 · Cited by 201 · see citing works
Early resistance training-induced increases in muscle cross-sectional area are concomitant with edema-induced muscle swelling
Damas, F., Phillips, S. M., Lixandrão, M. E., Vechin, F. C., Libardi, C. A., Roschel, H., Tricoli, V., & Ugrinowitsch, C. (2016) · European Journal of Applied Physiology · doi:10.1007/s00421-015-3243-4 · Cited by 202 · 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
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Strategies to Prevent Sarcopenia in the Aging Process: Role of Protein Intake and Exercise
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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
Whey protein supplementation during resistance training augments lean body mass
Volek, J. S., Volk, B. M., Gómez, A. L., Kunces, L. J., Kupchak, B. R., Freidenreich, D. J., Aristizabal, J. C., Saenz, C., Dunn-Lewis, C., Ballard, K. D., et al. (2013) · Journal of the American College of Nutrition · doi:10.1080/07315724.2013.793580 · Cited by 181 · see citing works
Protein Ingestion before Sleep Increases Muscle Mass and Strength Gains during Prolonged Resistance-Type Exercise Training in Healthy Young MenNitrogen1–3
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The impact of protein quality on the promotion of resistance exercise-induced changes in muscle mass
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The anabolic response to plant-based protein ingestion
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Innate Immunity in the Persistent Inflammation, Immunosuppression, and Catabolism Syndrome and Its Implications for Therapy
Horiguchi, H., Loftus, T. J., Hawkins, R. B., Raymond, S. L., Stortz, J. A., Hollen, M. K., Weiss, B. P., Miller, E. S., Bihorac, A., Larson, S. D., et al. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00595 · Cited by 164 · see citing works
Sarcopenic obesity and complex interventions with nutrition and exercise in community-dwelling older persons &ndash; a narrative review
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Effects of leucine-rich protein supplements on anthropometric parameter and muscle strength in the elderly: A systematic review and meta-analysis
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Effect of a Protein Supplement on the Gut Microbiota of Endurance Athletes: A Randomized, Controlled, Double-Blind Pilot Study
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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
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Pea proteins oral supplementation promotes muscle thickness gains during resistance training: a double-blind, randomized, Placebo-controlled clinical trial vs. Whey protein
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Authors: Cermak, N. M., Res, P. T., de Groot, L. C., Saris, W. H., & van Loon, L. J.
Affiliations: Maastricht University Medical Centre (NL)
ORCID: Cermak, Naomi M
Saris, Wim HM
Venue: The American Journal of Clinical Nutrition
Publisher: Elsevier BV
Published: 2012-12
Volume: 96
Issue: 6
Pages: 1454-1464
ISSN: 0002-9165 (ISSN-L)
DOI: 10.3945/ajcn.112.037556
OpenAlex: W2113082753
Cited by: 827
References: 70
Citations by year: 2026: 39 · 2025: 50 · 2024: 33 · 2023: 49 · 2022: 52 · 2021: 68 · 2020: 65 · 2019: 82 · 2018: 93 · 2017: 83 · 2016: 65 · 2015: 70 · 2014: 47 · 2013: 27 · 2012: 2
FWCI: 4.30
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 3737 d)
Locations: American Journal of Clinical Nutrition (publishedVersion)
PubMed (publishedVersion)
Research Publications (Maastricht University) (publishedVersion, other-oa)
Socio-Environmental Systems Modeling (acceptedVersion)
Research Bank (Australian Catholic University) (submittedVersion)
VUBIR (Vrije Universiteit Brussel) (submittedVersion)
Research Publications (Maastricht University) (submittedVersion, other-oa)
Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Funders: Canadian Institutes of Health Research
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
Health Sciences › Medicine › Orthopedics and Sports Medicine › Sports Performance and Training
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
Keywords: protein supplementation, skeletal muscle adaptation, muscle protein accretion, fat-free mass, muscle strength, leg press strength, muscle fiber cross-sectional area, older adults, muscle hypertrophy
MeSH terms: Aging, Dietary Proteins, Humans, Randomized Controlled Trials as Topic, Muscle, Skeletal, Dietary Supplements, Muscle Development, Muscle Strength, Resistance Training

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Protein supplementation augments the adaptive response of skeletal muscle to resistance-type exercise training: a meta-analysis

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