Dietary protein considerations to support active aging

Wall, Benjamin T.; Cermak, Naomi M.; van Loon, Luc J. C.

doi:10.1007/s40279-014-0258-7

Cited by 56Muscle metabolism and nutritionNutrition and Health in AgingMuscle Physiology and Disorders

Dietary protein considerations to support active aging

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Wall, Benjamin T., Cermak, Naomi M., van Loon, Luc J. C.·2014·Sports Medicine

DOI 10.1007/s40279-014-0258-7PMC PMC4213379

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Abstract

Given our rapidly aging world-wide population, the loss of skeletal muscle mass with healthy aging (sarcopenia) represents an important societal and public health concern. Maintaining or adopting an active lifestyle alleviates age-related muscle loss to a certain extent. Over time, even small losses of muscle tissue can hinder the ability to maintain an active lifestyle and, as such, contribute to the development of frailty and metabolic disease. Considerable research focus has addressed the application of dietary protein supplementation to support exercise-induced gains in muscle mass in younger individuals. In contrast, the role of dietary protein in supporting the maintenance (or gain) of skeletal muscle mass in active older persons has received less attention. Older individuals display a blunted muscle protein synthetic response to dietary protein ingestion. However, this reduced anabolic response can largely be overcome when physical activity is performed in close temporal proximity to protein consumption. Moreover, recent evidence has helped elucidate the optimal type and amount of dietary protein that should be ingested by the older adult throughout the day in order to maximize the skeletal muscle adaptive response to physical activity. Evidence demonstrates that when these principles are adhered to, muscle maintenance or hypertrophy over prolonged periods can be further augmented in active older persons. The present review outlines the current understanding of the role that dietary protein occupies in the lifestyle of active older adults as a means to increase skeletal muscle mass, strength and function, and thus support healthier aging.

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Creatine, citrulline, and leucine-rich feedings are best interpreted as compounds that help maintain a permissive metabolic and signalling environment in which mechanical loading can drive nucleolar expansion.
“Creatine [166,167], citrulline [168,169], and leucine-rich feedings [111,162] are best interpreted as compounds that help maintain a permissive metabolic and signalling environment in which mechanical loading can drive nucleolar expansion.”
From Ribosome Biogenesis as a Putative Bottleneck to Skeletal Muscle Hypertrophy: Mechanisms, Human Evidence, and Practical Modulators (2026) · cites this paper as [162]
The Type and Amount of Dietary Protein section reports that leucine-enriched protein can amplify the post-meal anabolic response in elderly men. The Nutritional Regulation section identifies leucine as relevant to mTOR signalling. These passages support a role for leucine-rich feedings in muscle protein synthesis, but the paper does not link them to mechanical loading driving nucleolar expansion; it says their relevance after exercise needs further study. (LLM, conf=0.86)
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Leucine-rich feedings can amplify the stimulation of MPS, particularly in older adults or in contexts of anabolic resistance.
“leucine-rich feedings can amplify the stimulation of MPS, particularly in older adults or in contexts of anabolic resistance [111,162]”
From Ribosome Biogenesis as a Putative Bottleneck to Skeletal Muscle Hypertrophy: Mechanisms, Human Evidence, and Practical Modulators (2026) · cites this paper as [162]

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Dickinson, J. M., Fry, C. S., Drummond, M. J., Gundermann, D. M., Walker, D. K., Glynn, E. L., Timmerman, K. L., Dhanani, S., Volpi, E., & Rasmussen, B. B. (2011) · The Journal of Nutrition · doi:10.3945/jn.111.139485 · Cited by 282 · see citing works
Myofibrillar protein synthesis in young and old men
Welle, S. L., Thornton, C. A., Józefowicz, R. F., & Statt, M. (1993) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1993.264.5.e693 · Cited by 280 · see citing works
Fish-oil supplementation enhances the effects of strength training in elderly women
Rodacki, C. L., Rodacki, A. L., Pereira, G., Naliwaiko, K., Coelho, I., Pequito, D., & Fernandes, L. C. (2012) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.111.021915 · Cited by 274 · see citing works
Myofibrillar and collagen protein synthesis in human skeletal muscle in young men after maximal shortening and lengthening contractions
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Rapid aminoacidemia enhances myofibrillar protein synthesis and anabolic intramuscular signaling responses after resistance exercise
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Protein supplementation before and after exercise does not further augment skeletal muscle hypertrophy after resistance training in elderly men
Verdijk, L. B., Jonkers, R. A., Gleeson, B. G., Beelen, M., Meijer, K., Savelberg, H. H., Wodzig, W. K., Dendale, P., & van Loon, L. J. (2009) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.2008.26626 · Cited by 253 · see citing works
Protein requirements and muscle mass/strength changes during intensive training in novice bodybuilders
Lemon, P. W., Tarnopolsky, M. A., MacDougall, J. D., & Atkinson, S. A. (1992) · Journal of Applied Physiology · doi:10.1152/jappl.1992.73.2.767 · Cited by 241 · see citing works
Creatine supplementation during resistance training in older adults - a meta-analysis
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Milk ingestion stimulates net muscle protein synthesis following resistance exercise
ELLIOT, T. A., CREE, M. G., SANFORD, A. P., WOLFE, R. R., & TIPTON, K. D. (2006) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000210190.64458.25 · Cited by 237 · see citing works
Nonessential amino acids are not necessary to stimulate net muscle protein synthesis in healthy volunteers
Tipton, K. (1999) · The Journal of Nutritional Biochemistry · doi:10.1016/s0955-2863(98)00087-4 · Cited by 231 · see citing works
An increase in essential amino acid availability upregulates amino acid transporter expression in human skeletal muscle.
Drummond, M., Glynn, E., Fry, C., Timmerman, K., Volpi, E., & Rasmussen, B. (2010) · American Journal of Physiology. Endocrinology and Metabolism · doi:10.1152/ajpendo.00690.2009 · Cited by 231 · see citing works
Effect of carbohydrate intake on net muscle protein synthesis during recovery from resistance exercise
Børsheim, E., Cree‐Green, M., Tipton, K. D., Elliott, T. A., Aarsland, A. A., & Wolfe, R. R. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00333.2003 · Cited by 230 · see citing works
The effect of resistance training combined with timed ingestion of protein on muscle fiber size and muscle strength
Andersen, L. L., Tufekovic, G., Zebis, M. K., Crameri, R. M., Verlaan, G., Kjær, M., Suetta, C., Magnusson, P., & Aagaard, P. (2005) · Metabolism · doi:10.1016/j.metabol.2004.07.012 · Cited by 228 · see citing works
Effects of resistance training and protein plus amino acid supplementation on muscle anabolism, mass, and strength
Willoughby, D. S., Stout, J. R., & Wilborn, C. D. (2007) · Amino Acids · doi:10.1007/s00726-006-0398-7 · Cited by 227 · see citing works
Protein Ingestion before Sleep Improves Postexercise Overnight Recovery
RES, P. T., GROEN, B., PENNINGS, B., BEELEN, M., WALLIS, G. A., GIJSEN, A. P., SENDEN, J. M. G., & VAN LOON, L. J. C. (2012) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e31824cc363 · Cited by 226 · see citing works
Resistance exercise training increases mixed muscle protein synthesis rate in frail women and men ≥76 yr old
Yarasheski, K. E., Pak-Loduca, J., Hasten, D. L., Obert, K. A., Brown, M. B., & Sinacore, D. R. (1999) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1999.277.1.e118 · Cited by 226 · see citing works
Leucine co-ingestion improves post-prandial muscle protein accretion in elderly men
Wall, B. T., Hamer, H. M., de Lange, A., Kiskini, A., Groen, B. B. L., Senden, J. M. G., Gijsen, A. P., Verdijk, L. B., & van Loon, L. J. C. (2013) · Clinical Nutrition · doi:10.1016/j.clnu.2012.09.002 · Cited by 220 · see citing works
Self-citation
Blunting of insulin inhibition of proteolysis in legs of older subjects may contribute to age-related sarcopenia
Wilkes, E. A., Selby, A. L., Atherton, P. J., Patel, R., Rankin, D., Smith, K., & Rennie, M. J. (2009) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.2009.27543 · Cited by 204 · see citing works
The Effect of Whey Protein Supplementation with and Without Creatine Monohydrate Combined with Resistance Training on Lean Tissue Mass and Muscle Strength
Burke, D. G., Chilibeck, P. D., Davison, K. S., Candow, D. C., Farthing, J., & Smith-Palmer, T. (2001) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.11.3.349 · Cited by 193 · see citing works
Myofibrillar protein synthesis in young and old human subjects after three months of resistance training
Welle, S. L., Thornton, C. A., & Statt, M. (1995) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1995.268.3.e422 · Cited by 190 · 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
Body Composition and Strength Changes in Women with Milk and Resistance Exercise
JOSSE, A. R., TANG, J. E., TARNOPOLSKY, M. A., & PHILLIPS, S. M. (2010) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3181c854f6 · Cited by 181 · see citing works
Effect of Whey and Soy Protein Supplementation Combined with Resistance Training in Young Adults
Candow, D. G., Burke, N. C., Smith-Palmer, T., & Burke, D. G. (2006) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.16.3.233 · Cited by 180 · see citing works
Insulin Stimulates Human Skeletal Muscle Protein Synthesis via an Indirect Mechanism Involving Endothelial-Dependent Vasodilation and Mammalian Target of Rapamycin Complex 1 Signaling
Timmerman, K. L., Lee, J. L., Dreyer, H. C., Dhanani, S., Glynn, E. L., Fry, C. S., Drummond, M. J., Sheffield‐Moore, M., Rasmussen, B. B., & Volpi, E. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-2696 · Cited by 180 · see citing works
Disuse Impairs the Muscle Protein Synthetic Response to Protein Ingestion in Healthy Men
Wall, B. T., Snijders, T., Senden, J. M., Ottenbros, C. L. P., Gijsen, A. P., Verdijk, L. B., & van Loon, L. J. C. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-2098 · Cited by 178 · see citing works
Self-citation
Does dietary creatine supplementation play a role in skeletal muscle metabolism and performance?
Casey, A. E., & Greenhaff, P. L. (2000) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/72.2.607s · Cited by 173 · see citing works
Resistance training alters the response of fed state mixed muscle protein synthesis in young men
Tang, J. E., Perco, J. G., Moore, D. R., Wilkinson, S. B., & Phillips, S. M. (2007) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00636.2007 · Cited by 172 · see citing works
Effect of glucose supplement timing on protein metabolism after resistance training
Roy, B. D., Tarnopolsky, M. A., MacDOUGALL, J. D., Fowles, J. R., & Yarasheski, K. E. (1997) · Journal of Applied Physiology · doi:10.1152/jappl.1997.82.6.1882 · Cited by 171 · see citing works
Dietary Protein Digestion and Absorption Rates and the Subsequent Postprandial Muscle Protein Synthetic Response Do Not Differ between Young and Elderly Men ,
Koopman, R., Walrand, S., Beelen, M., Gijsen, A. P., Kies, A. K., Boirie, Y., Saris, W. H. M., & van Loon, L. J. C. (2009) · The Journal of Nutrition · doi:10.3945/jn.109.109173 · Cited by 167 · see citing works
Minced beef is more rapidly digested and absorbed than beef steak, resulting in greater postprandial protein retention in older men
Pennings, B., Groen, B. B., van Dijk, J.-W., de Lange, A., Kiskini, A., Kuklinski, M., Senden, J. M., & van Loon, L. J. (2013) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.112.051201 · Cited by 167 · cited 1× · see citing works
“As discussed, protein is the fundamentally anabolic macronutrient, hence studies have attempted to define the optimal amount [83, 88–90] and type [91–94] of dietary protein to maximize muscle protein synthesis rates.”
Background
Resistance exercise with whey protein ingestion affects mTOR signaling pathway and myostatin in men
Hulmi, J. J., Tannerstedt, J., Selänne, H., Kainulainen, H., Kovanen, V., & Mero, A. A. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00087.2009 · Cited by 163 · see citing works
Carbohydrate Does Not Augment Exercise-Induced Protein Accretion versus Protein Alone
STAPLES, A. W., BURD, N. A., WEST, D. W. D., CURRIE, K. D., ATHERTON, P. J., MOORE, D. R., RENNIE, M. J., MACDONALD, M. J., BAKER, S. K., & PHILLIPS, S. M. (2011) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e31820751cb · Cited by 162 · see citing works
Aging Affects the Transcriptional Regulation of Human Skeletal Muscle Disuse Atrophy
Suetta, C., Frandsen, U., Jensen, L., Jensen, M. M., Jespersen, J. G., Hvid, L. G., Bayer, M. L., Petersson, S. J., Schrøder, H. D., Andersen, J. L., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0051238 · Cited by 160 · see citing works
THE EFFECTS OF PROTEIN AND AMINO ACID SUPPLEMENTATION ON PERFORMANCE AND TRAINING ADAPTATIONS DURING TEN WEEKS OF RESISTANCE TRAINING
KERKSICK, C. M., RASMUSSEN, C. J., LANCASTER, S. L., MAGU, B., SMITH, P., MELTON, C., GREENWOOD, M., ALMADA, A. L., EARNEST, C. P., & KREIDER, R. B. (2006) · Journal of Strength and Conditioning Research · doi:10.1519/00124278-200608000-00028 · Cited by 156 · see citing works
Impact of protein pulse feeding on lean mass in malnourished and at-risk hospitalized elderly patients: a randomized controlled trial
Bouillanne, O., Curis, E., Hamon-Vilcot, B., Nicolis, I., Chrétien, P., Schauer, N., Vincent, J.-P., Cynober, L., & Aussel, C. (2013) · Clinical Nutrition · doi:10.1016/j.clnu.2012.08.015 · Cited by 152 · cited 1× · see citing works
“Interestingly, when extreme skewed diets are employed (*80 % of daily protein intake [*80–85 g] consumed in a single meal with the rest spread across the remaining meals), favourable effects on nitrogen retention, whole body protein balance and/or lean mass have been reported compared with a more spread feeding approa…”
Background
Pharmacological Vasodilation Improves Insulin-Stimulated Muscle Protein Anabolism but Not Glucose Utilization in Older Adults
Timmerman, K. L., Lee, J. L., Fujita, S., Dhanani, S., Dreyer, H. C., Fry, C. S., Drummond, M. J., Sheffield-Moore, M., Rasmussen, B. B., & Volpi, E. (2010) · Diabetes · doi:10.2337/db10-0415 · Cited by 149 · see citing works
Combined ingestion of protein and carbohydrate improves protein balance during ultra-endurance exercise
Koopman, R., Pannemans, D. L. E., Jeukendrup, A. E., Gijsen, A. P., Senden, J. M. G., Halliday, D., Saris, W. H. M., van Loon, L. J. C., & Wagenmakers, A. J. M. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00543.2003 · Cited by 147 · see citing works
Is there a maximal anabolic response to protein intake with a meal?
Deutz, N. E., & Wolfe, R. R. (2013) · Clinical Nutrition · doi:10.1016/j.clnu.2012.11.018 · Cited by 144 · see citing works
Skeletal muscle disuse atrophy is not attenuated by dietary protein supplementation in healthy older men
Dirks, M. L., Wall, B. T., Nilwik, R., Weerts, D. H. J. M., Verdijk, L. B., & van Loon, L. J. C. (2014) · The Journal of Nutrition · doi:10.3945/jn.114.194217 · Cited by 137 · see citing works
Self-citation
Carbohydrate coingestion delays dietary protein digestion and absorption but does not modulate postprandial muscle protein accretion.
Gorissen, S., Burd, N., Hamer, H., Gijsen, A., Groen, B. B. L., & van Loon, L. V. (2014) · Journal of Clinical Endocrinology and Metabolism · doi:10.1210/jc.2013-3970 · Cited by 135 · see citing works
The impact of supplemental N-3 long chain polyunsaturated fatty acids and dietary antioxidants on physical performance in postmenopausal women
Hutchins-Wiese, H., Kleppinger, A., Annis, K., Liva, E., Lammi‐Keefe, C. J., Durham, H. A., & Kenny, R. A. (2012) · The journal of nutrition health & aging · doi:10.1007/s12603-012-0415-3 · Cited by 133 · see citing works
Effects of creatine loading and prolonged creatine supplementation on body composition, fuel selection, sprint and endurance performance in humans
LOON, L. J. C. V., OOSTERLAAR, A. M., HARTGENS, F., HESSELINK, M. K. C., SNOW, R. J., & WAGENMAKERS, A. J. M. (2003) · Clinical Science · doi:10.1042/cs1040153 · Cited by 128 · see citing works
Facts, noise and wishful thinking: muscle protein turnover in aging and human disuse atrophy
Rennie, M. J., Selby, A., Atherton, P. J., Smith, K., Kumar, V., Glover, E. L., & Philips, S. M. (2010) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.2009.00967.x · Cited by 121 · see citing works
Intragastric protein administration stimulates overnight muscle protein synthesis in elderly men
Groen, B. B. L., Res, P. T., Pennings, B., Hertle, E., Senden, J. M. G., Saris, W. H. M., & van Loon, L. J. C. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00321.2011 · Cited by 117 · see citing works
Isolated bovine retinal pigment epithelial cells express delayed rectifier type and M-type K+ currents
Takahira, M., & Hughes, B. A. (1997) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1997.273.3.c790 · Cited by 115 · 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
Dose-dependent responses of myofibrillar protein synthesis with beef ingestion are enhanced with resistance exercise in middle-aged men
Robinson, M. J., Burd, N. A., Breen, L., Rerecich, T., Yang, Y., Hector, A. J., Baker, S. K., & Phillips, S. M. (2013) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2012-0092 · Cited by 109 · see citing works
Co-ingestion of leucine with protein does not further augment post-exercise muscle protein synthesis rates in elderly men
Koopman, R., Verdijk, L. B., Beelen, M., Gorselink, M., Kruseman, A. N., Wagenmakers, A. J. M., Kuipers, H., & van Loon, L. J. C. (2008) · British Journal Of Nutrition · doi:10.1017/s0007114507812013 · Cited by 104 · see citing works
Prevalence of sarcopenia among healthy ambulatory subjects: the sarcopenia begins from 45 years
Cherin, P., Voronska, E., Fraoucene, N., & de Jaeger, C. (2013) · Aging Clinical and Experimental Research · doi:10.1007/s40520-013-0132-8 · Cited by 99 · see citing works
Omega-3 fatty acids and protein metabolism
Girolamo, F. G. D., Situlin, R., Mazzucco, S., Valentini, R., Toigo, G., & Biolo, G. (2014) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0000000000000032 · Cited by 97 · see citing works
Protein coingestion stimulates muscle protein synthesis during resistance-type exercise
Beelen, M., Koopman, R., Gijsen, A. P., Vandereyt, H., Kies, A. K., Kuipers, H., Saris, W. H. M., & van Loon, L. J. C. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00774.2007 · Cited by 94 · see citing works
Effect of Post-Exercise Supplement Consumption on Adaptations to Resistance Training
Rankin, J. W., Goldman, L. P., Puglisi, M. J., Nickols-Richardson, S. M., Earthman, C. P., & Gwazdauskas, F. C. (2004) · Journal of the American College of Nutrition · doi:10.1080/07315724.2004.10719375 · Cited by 90 · see citing works
Aging differentially affects human skeletal muscle amino acid transporter expression when essential amino acids are ingested after exercise
Dickinson, J. M., Drummond, M. J., Coben, J. R., Volpi, E., & Rasmussen, B. B. (2012) · Clinical Nutrition · doi:10.1016/j.clnu.2012.07.009 · Cited by 86 · see citing works
Effect of a 10-Week strength training program and recovery drink on body composition, muscular strength and endurance, and anaerobic power and capacity
Chromiak, J. A., Smedley, B., Carpenter, W., Brown, R., Koh, Y., Lamberth, J., Joe, L. A., Abadie, B. R., & Altorfer, G. (2004) · Nutrition · doi:10.1016/j.nut.2004.01.005 · Cited by 86 · see citing works
The science of muscle hypertrophy: making dietary protein count
Phillips, S. M. (2011) · Proceedings of the Nutrition Society · doi:10.1017/s002966511000399x · Cited by 81 · see citing works
Effects of high-calorie supplements on body composition and muscular strength following resistance training.
Rozenek, R., Ward, P., Long, S., & Garhammer, J. (2002) · PubMed · Cited by 80 · see citing works
A Creatine-Protein-Carbohydrate Supplement Enhances Responses to Resistance Training
Cribb, P. J., Williams, A. D., & Hayes, A. (2007) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e31814fb52a · Cited by 76 · see citing works
EFFECTS OF LEUCINE AND WHEY PROTEIN SUPPLEMENTATION DURING EIGHT WEEKS OF UNILATERAL RESISTANCE TRAINING
Coburn, J. W., Housh, D. J., Housh, T. J., Malek, M. H., Beck, T. W., Cramer, J. T., Johnson, G. O., & Donlin, P. E. (2006) · The Journal of Strength and Conditioning Research · doi:10.1519/r-17925.1 · Cited by 75 · see citing works
Basic concepts about genes, inactivity and aging
Booth, F. W., & Zwetsloot, K. A. (2010) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.2009.00972.x · Cited by 74 · see citing works
Adequacy and change in nutrient and food intakes with aging in a seven-year cohort study in elderly women
Zhu, K., Devine, A., Suleska, A., Tan, C. Y. L., Toh, C. Z. J., Kerr, D. A., & Prince, R. L. (2010) · The journal of nutrition health & aging · doi:10.1007/s12603-010-0324-2 · Cited by 67 · see citing works
Plasma characteristics at off-axis high pressure magnetron YBa2Cu3O7−δ sputtering
Marchenko, V. A., Znamenskii, A. G., & Helmersson, U. (1997) · Journal of Applied Physics · doi:10.1063/1.365993 · Cited by 53 · see citing works
The curious case of anabolic resistance: old wives' tales or new fables?
Burd, N. A., Wall, B. T., & van Loon, L. J. C. (2011) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01343.2011 · Cited by 52 · see citing works
Self-citation
Effects of a combined essential amino acids/carbohydrate supplementation on muscle mass, architecture and maximal strength following heavy-load training
Vieillevoye, S., POORTMANS, J. R., Duchateau, J., & Carpentier, A. (2010) · European Journal of Applied Physiology · doi:10.1007/s00421-010-1520-9 · Cited by 49 · see citing works
The Influence of 8 Weeks of Whey-Protein and Leucine Supplementation on Physical and Cognitive Performance
Walker, T. B., Smith, J. K., Herrera, M. B., Lebegue, B., Pinchak, A., & FISCHER, J. R. (2010) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.20.5.409 · Cited by 47 · see citing works
Carbohydrate co-ingestion with protein does not further augment post-prandial muscle protein accretion in older men
Hamer, H. M., Wall, B. T., Kiskini, A., de Lange, A., Groen, B. B. L., Bakker, J. A., Gijsen, A. P., Verdijk, L. B., & van Loon, L. J. C. (2013) · Nutrition & Metabolism · doi:10.1186/1743-7075-10-15 · Cited by 44 · see citing works
Self-citation
Maintenance of the musculoskeletal mass by control of protein turnover: the concept of anabolic resistance and its relevance to the transplant recipient.
Rennie, M. J., & Wilkes, E. (2005) · PubMed · Cited by 43 · see citing works
EFFECTS OF A DRINK CONTAINING CREATINE,AMINO ACIDS, AND PROTEIN COMBINED WITH TEN WEEKS OF RESISTANCE TRAINING ON BODY COMPOSITION, STRENGTH, AND ANAEROBIC PERFORMANCE
Beck, T. W., Housh, T. J., Johnson, G. O., Coburn, J. W., Malek, M. H., & Cramer, J. T. (2007) · The Journal of Strength and Conditioning Research · doi:10.1519/r-18685.1 · Cited by 39 · see citing works
Muscle Performance, Size, and Safety Responses After Eight Weeks of Resistance Training and Protein Supplementation: A Randomized, Double-Blinded, Placebo-Controlled Clinical Trial
Herda, A. A., Herda, T. J., Costa, P. B., Ryan, E. D., Stout, J. R., & Cramer, J. T. (2013) · Journal of Strength and Conditioning Research · doi:10.1519/jsc.0b013e31828c289f · Cited by 39 · see citing works
Fish oil omega-3 fatty acids partially prevent lipid-induced insulin resistance in human skeletal muscle without limiting acylcarnitine accumulation
Stephens, F. B., Mendis, B., Shannon, C. E., Cooper, S., Ortori, C. A., Barrett, D. A., Mansell, P., & Tsintzas, K. (2014) · Clinical Science · doi:10.1042/cs20140031 · Cited by 35 · see citing works
Changes in Body Composition with Yogurt Consumption during Resistance Training in Women
White, K. M., Bauer, S. J., Hartz, K. K., & Baldridge, M. (2009) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.19.1.18 · Cited by 35 · see citing works
Serum Basal Hormone Concentrations, Nutrition and Physical Fitness During Strength and/or Endurance Training in 39–64-Year-Old Women
Sillanpää, E., HÄKKINEN, A. H., Laaksonen, D. E., Karavirta, L., Kraemer, W. J., & Häkkinen, K. (2009) · International Journal of Sports Medicine · doi:10.1055/s-0029-1242811 · Cited by 35 · see citing works
The role of glucose, long‐chain triglycerides and amino acids for promotion of amino acid balance across peripheral tissues in man
Svanberg, E., Möller‐Loswick, A., Matthews, D. E., Körner, U., Andersson, M., & Lundholm, K. (1999) · Clinical Physiology · doi:10.1046/j.1365-2281.1999.00183.x · Cited by 32 · see citing works
Response to Dr. Roger’s letter: further studies are necessary in order to conclude a causal association between the consumption of monosodium L-glutamate (MSG) and the prevalence of metabolic syndrome in the rural Thai population
Insawang, T., Selmi, C. F., Cha’on, U., Gershwin, M. E., Yongvanit, P., & Prasongwattana, V. (2013) · Nutrition & Metabolism · doi:10.1186/1743-7075-10-10 · Cited by 1 · see citing works

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Effects of multi-domain interventions in (pre)frail elderly on frailty, functional, and cognitive status: a systematic review
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Authors: Wall, B. T., Cermak, N. M., & van Loon, L. J. C.
Affiliations: Maastricht University (NL)
ORCID: Wall, Benjamin T.
Cermak, Naomi M.
Venue: Sports Medicine
Publisher: Springer Science and Business Media LLC
Published: 2014-10-30
Volume: 44
Issue: S2
Pages: 185-194
ISSN: 0112-1642 (ISSN-L)
1179-2035
DOI: 10.1007/s40279-014-0258-7
PMC: PMC4213379
OpenAlex: W1969627119
Cited by: 56
References: 141
Citations by year: 2026: 3 · 2025: 1 · 2024: 2 · 2023: 1 · 2022: 3 · 2021: 4 · 2020: 4 · 2019: 6 · 2018: 2 · 2017: 6 · 2016: 15 · 2015: 7 · 2014: 1 · 2012: 1
FWCI: 0.97
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0 (unspecified)
Locations: Sports Medicine (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Open Research Exeter (University of Exeter) (acceptedVersion, other-oa)
Research Bank (Australian Catholic University) (submittedVersion)
Figshare (submittedVersion)
Funders: PepsiCo
Gran Sasso Science Institute
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: dietary protein, sarcopenia, healthy aging, older adults, muscle protein synthesis, muscle hypertrophy, frailty, physical activity, protein timing, muscle strength, muscle function, active ageing
MeSH terms: Aged, Aging, Dietary Proteins, Humans, Muscle Proteins, Physical Education and Training, Exercise, Muscle, Skeletal

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