Skip to main content
Top
Published in: Journal of the International Society of Sports Nutrition 1/2013

Open Access 01-12-2013 | Review

The effect of protein timing on muscle strength and hypertrophy: a meta-analysis

Authors: Brad Jon Schoenfeld, Alan Albert Aragon, James W Krieger

Published in: Journal of the International Society of Sports Nutrition | Issue 1/2013

Login to get access

Abstract

Protein timing is a popular dietary strategy designed to optimize the adaptive response to exercise. The strategy involves consuming protein in and around a training session in an effort to facilitate muscular repair and remodeling, and thereby enhance post-exercise strength- and hypertrophy-related adaptations. Despite the apparent biological plausibility of the strategy, however, the effectiveness of protein timing in chronic training studies has been decidedly mixed. The purpose of this paper therefore was to conduct a multi-level meta-regression of randomized controlled trials to determine whether protein timing is a viable strategy for enhancing post-exercise muscular adaptations. The strength analysis comprised 478 subjects and 96 ESs, nested within 41 treatment or control groups and 20 studies. The hypertrophy analysis comprised 525 subjects and 132 ESs, nested with 47 treatment or control groups and 23 studies. A simple pooled analysis of protein timing without controlling for covariates showed a small to moderate effect on muscle hypertrophy with no significant effect found on muscle strength. In the full meta-regression model controlling for all covariates, however, no significant differences were found between treatment and control for strength or hypertrophy. The reduced model was not significantly different from the full model for either strength or hypertrophy. With respect to hypertrophy, total protein intake was the strongest predictor of ES magnitude. These results refute the commonly held belief that the timing of protein intake in and around a training session is critical to muscular adaptations and indicate that consuming adequate protein in combination with resistance exercise is the key factor for maximizing muscle protein accretion.
Appendix
Available only for authorised users
Literature
1.
go back to reference Phillips SM, Van Loon LJ: Dietary protein for athletes: from requirements to optimum adaptation. J Sports Sci. 2011, 29 ((Suppl 1)): S29-38.CrossRefPubMed Phillips SM, Van Loon LJ: Dietary protein for athletes: from requirements to optimum adaptation. J Sports Sci. 2011, 29 ((Suppl 1)): S29-38.CrossRefPubMed
2.
go back to reference Kerksick C, Harvey T, Stout J, Campbell B, Wilborn C, Kreider R: International society of sports nutrition position stand: nutrient timing. J Int Soc Sports Nutr. 2008 Oct 3, 5: 17-PubMedCentralCrossRefPubMed Kerksick C, Harvey T, Stout J, Campbell B, Wilborn C, Kreider R: International society of sports nutrition position stand: nutrient timing. J Int Soc Sports Nutr. 2008 Oct 3, 5: 17-PubMedCentralCrossRefPubMed
3.
go back to reference Lemon PW, Berardi JM, Noreen EE: The role of protein and amino acid supplements in the athlete's diet: does type or timing of ingestion matter?. Curr Sports Med Rep. 2002 Aug, 1 (4): 214-221.CrossRefPubMed Lemon PW, Berardi JM, Noreen EE: The role of protein and amino acid supplements in the athlete's diet: does type or timing of ingestion matter?. Curr Sports Med Rep. 2002 Aug, 1 (4): 214-221.CrossRefPubMed
4.
go back to reference Ivy J, Portman R: Nutrient timing: The future of sports nutrition. 2004, North Bergen, NJ: Basic Health Publications Ivy J, Portman R: Nutrient timing: The future of sports nutrition. 2004, North Bergen, NJ: Basic Health Publications
5.
go back to reference Candow DG, Chilibeck PD: Timing of creatine or protein supplementation and resistance training in the elderly. Appl Physiol Nutr Metab. 2008 Feb, 33 (1): 184-190.CrossRefPubMed Candow DG, Chilibeck PD: Timing of creatine or protein supplementation and resistance training in the elderly. Appl Physiol Nutr Metab. 2008 Feb, 33 (1): 184-190.CrossRefPubMed
6.
go back to reference Tipton KD, Elliott TA, Cree MG, Wolf SE, Sanford AP, Wolfe RR: Ingestion of casein and whey proteins result in muscle anabolism after resistance exercise. Med Sci Sports Exerc. 2004 Dec, 36 (12): 2073-2081.CrossRefPubMed Tipton KD, Elliott TA, Cree MG, Wolf SE, Sanford AP, Wolfe RR: Ingestion of casein and whey proteins result in muscle anabolism after resistance exercise. Med Sci Sports Exerc. 2004 Dec, 36 (12): 2073-2081.CrossRefPubMed
7.
go back to reference Rasmussen BB, Tipton KD, Miller SL, Wolf SE, Wolfe RR: An oral essential amino acid-carbohydrate supplement enhances muscle protein anabolism after resistance exercise. J Appl Physiol. 2000 Feb, 88 (2): 386-392.PubMed Rasmussen BB, Tipton KD, Miller SL, Wolf SE, Wolfe RR: An oral essential amino acid-carbohydrate supplement enhances muscle protein anabolism after resistance exercise. J Appl Physiol. 2000 Feb, 88 (2): 386-392.PubMed
8.
go back to reference Tipton KD, Elliott TA, Ferrando AA, Aarsland AA, Wolfe RR: Stimulation of muscle anabolism by resistance exercise and ingestion of leucine plus protein. Appl Physiol Nutr Metab. 2009 Apr, 34 (2): 151-161.CrossRefPubMed Tipton KD, Elliott TA, Ferrando AA, Aarsland AA, Wolfe RR: Stimulation of muscle anabolism by resistance exercise and ingestion of leucine plus protein. Appl Physiol Nutr Metab. 2009 Apr, 34 (2): 151-161.CrossRefPubMed
9.
go back to reference Tipton KD, Ferrando AA, Phillips SM, Doyle D, Wolfe RR: Postexercise net protein synthesis in human muscle from orally administered amino acids. Am J Physiol. 1999 Apr, 276 (4 Pt 1): E628-E634.PubMed Tipton KD, Ferrando AA, Phillips SM, Doyle D, Wolfe RR: Postexercise net protein synthesis in human muscle from orally administered amino acids. Am J Physiol. 1999 Apr, 276 (4 Pt 1): E628-E634.PubMed
10.
go back to reference Borsheim E, Tipton KD, Wolf SE, Wolfe RR: Essential amino acids and muscle protein recovery from resistance exercise. Am J Physiol Endocrinol Metab. 2002 Oct, 283 (4): E648-E657.CrossRefPubMed Borsheim E, Tipton KD, Wolf SE, Wolfe RR: Essential amino acids and muscle protein recovery from resistance exercise. Am J Physiol Endocrinol Metab. 2002 Oct, 283 (4): E648-E657.CrossRefPubMed
11.
go back to reference Tipton KD, Gurkin BE, Matin S, Wolfe RR: Nonessential amino acids are not necessary to stimulate net muscle protein synthesis in healthy volunteers. J Nutr Biochem. 1999 Feb, 10 (2): 89-95.CrossRefPubMed Tipton KD, Gurkin BE, Matin S, Wolfe RR: Nonessential amino acids are not necessary to stimulate net muscle protein synthesis in healthy volunteers. J Nutr Biochem. 1999 Feb, 10 (2): 89-95.CrossRefPubMed
12.
go back to reference Miller SL, Tipton KD, Chinkes DL, Wolf SE, Wolfe RR: Independent and combined effects of amino acids and glucose after resistance exercise. Med Sci Sports Exerc. 2003 Mar, 35 (3): 449-455.CrossRefPubMed Miller SL, Tipton KD, Chinkes DL, Wolf SE, Wolfe RR: Independent and combined effects of amino acids and glucose after resistance exercise. Med Sci Sports Exerc. 2003 Mar, 35 (3): 449-455.CrossRefPubMed
13.
go back to reference Koopman R, Beelen M, Stellingwerff T, Pennings B, Saris WH, Kies AK: Coingestion of carbohydrate with protein does not further augment postexercise muscle protein synthesis. Am J Physiol Endocrinol Metab. 2007 Sep, 293 (3): E833-E842.CrossRefPubMed Koopman R, Beelen M, Stellingwerff T, Pennings B, Saris WH, Kies AK: Coingestion of carbohydrate with protein does not further augment postexercise muscle protein synthesis. Am J Physiol Endocrinol Metab. 2007 Sep, 293 (3): E833-E842.CrossRefPubMed
14.
go back to reference Staples AW, Burd NA, West DW, Currie KD, Atherton PJ, Moore DR: Carbohydrate does not augment exercise-induced protein accretion versus protein alone. Med Sci Sports Exerc. 2011 Jul, 43 (7): 1154-1161.CrossRefPubMed Staples AW, Burd NA, West DW, Currie KD, Atherton PJ, Moore DR: Carbohydrate does not augment exercise-induced protein accretion versus protein alone. Med Sci Sports Exerc. 2011 Jul, 43 (7): 1154-1161.CrossRefPubMed
15.
go back to reference Glynn EL, Fry CS, Timmerman KL, Drummond MJ, Volpi E, Rasmussen BB: Addition of carbohydrate or alanine to an essential amino acid mixture does not enhance human skeletal muscle protein anabolism. J Nutr. 2013 Mar, 143 (3): 307-314.PubMedCentralCrossRefPubMed Glynn EL, Fry CS, Timmerman KL, Drummond MJ, Volpi E, Rasmussen BB: Addition of carbohydrate or alanine to an essential amino acid mixture does not enhance human skeletal muscle protein anabolism. J Nutr. 2013 Mar, 143 (3): 307-314.PubMedCentralCrossRefPubMed
16.
go back to reference Cribb PJ, Hayes A: Effects of supplement timing and resistance exercise on skeletal muscle hypertrophy. Med Sci Sports Exerc. 2006 Nov, 38 (11): 1918-1925.CrossRefPubMed Cribb PJ, Hayes A: Effects of supplement timing and resistance exercise on skeletal muscle hypertrophy. Med Sci Sports Exerc. 2006 Nov, 38 (11): 1918-1925.CrossRefPubMed
17.
go back to reference Willoughby DS, Stout JR, Wilborn CD: Effects of resistance training and protein plus amino acid supplementation on muscle anabolism, mass, and strength. Amino Acids. 2007, 32 (4): 467-477.CrossRefPubMed Willoughby DS, Stout JR, Wilborn CD: Effects of resistance training and protein plus amino acid supplementation on muscle anabolism, mass, and strength. Amino Acids. 2007, 32 (4): 467-477.CrossRefPubMed
18.
go back to reference Hulmi JJ, Kovanen V, Selanne H, Kraemer WJ, Hakkinen K, Mero AA: Acute and long-term effects of resistance exercise with or without protein ingestion on muscle hypertrophy and gene expression. Amino Acids. 2009 Jul, 37 (2): 297-308.CrossRefPubMed Hulmi JJ, Kovanen V, Selanne H, Kraemer WJ, Hakkinen K, Mero AA: Acute and long-term effects of resistance exercise with or without protein ingestion on muscle hypertrophy and gene expression. Amino Acids. 2009 Jul, 37 (2): 297-308.CrossRefPubMed
19.
go back to reference Burk A, Timpmann S, Medijainen L, Vahi M, Oopik V: Time-divided ingestion pattern of casein-based protein supplement stimulates an increase in fat-free body mass during resistance training in young untrained men. Nutr Res. 2009 Jun, 29 (6): 405-413.CrossRefPubMed Burk A, Timpmann S, Medijainen L, Vahi M, Oopik V: Time-divided ingestion pattern of casein-based protein supplement stimulates an increase in fat-free body mass during resistance training in young untrained men. Nutr Res. 2009 Jun, 29 (6): 405-413.CrossRefPubMed
20.
go back to reference Hoffman JR, Ratamess NA, Tranchina CP, Rashti SL, Kang J, Faigenbaum AD: Effect of protein-supplement timing on strength, power, and body-composition changes in resistance-trained men. Int J Sport Nutr Exerc Metab. 2009 Apr, 19 (2): 172-185.PubMed Hoffman JR, Ratamess NA, Tranchina CP, Rashti SL, Kang J, Faigenbaum AD: Effect of protein-supplement timing on strength, power, and body-composition changes in resistance-trained men. Int J Sport Nutr Exerc Metab. 2009 Apr, 19 (2): 172-185.PubMed
21.
go back to reference Verdijk LB, Jonkers RA, Gleeson BG, Beelen M, Meijer K, Savelberg HH: Protein supplementation before and after exercise does not further augment skeletal muscle hypertrophy after resistance training in elderly men. Am J Clin Nutr. 2009 Feb, 89 (2): 608-616.CrossRefPubMed Verdijk LB, Jonkers RA, Gleeson BG, Beelen M, Meijer K, Savelberg HH: Protein supplementation before and after exercise does not further augment skeletal muscle hypertrophy after resistance training in elderly men. Am J Clin Nutr. 2009 Feb, 89 (2): 608-616.CrossRefPubMed
22.
go back to reference Wycherley TP, Noakes M, Clifton PM, Cleanthous X, Keogh JB, Brinkworth GD: Timing of protein ingestion relative to resistance exercise training does not influence body composition, energy expenditure, glycaemic control or cardiometabolic risk factors in a hypocaloric, high protein diet in patients with type 2 diabetes. Diab Obes Metab. 2010 Dec, 12 (12): 1097-1105.CrossRef Wycherley TP, Noakes M, Clifton PM, Cleanthous X, Keogh JB, Brinkworth GD: Timing of protein ingestion relative to resistance exercise training does not influence body composition, energy expenditure, glycaemic control or cardiometabolic risk factors in a hypocaloric, high protein diet in patients with type 2 diabetes. Diab Obes Metab. 2010 Dec, 12 (12): 1097-1105.CrossRef
23.
go back to reference Aragon AA, Schoenfeld BJ: Nutrient timing revisited: is there a post-exercise anabolic window?. J Int Soc Sports Nutr. 2013 Jan 29, 10 (1): 10-15. 5,2783CrossRef Aragon AA, Schoenfeld BJ: Nutrient timing revisited: is there a post-exercise anabolic window?. J Int Soc Sports Nutr. 2013 Jan 29, 10 (1): 10-15. 5,2783CrossRef
24.
go back to reference Cermak NM, Res PT, de Groot LC, Saris WH, van Loon LJ: Protein supplementation augments the adaptive response of skeletal muscle to resistance-type exercise training: a meta-analysis. Am J Clin Nutr. 2012 Dec, 96 (6): 1454-1464.CrossRefPubMed Cermak NM, Res PT, de Groot LC, Saris WH, van Loon LJ: Protein supplementation augments the adaptive response of skeletal muscle to resistance-type exercise training: a meta-analysis. Am J Clin Nutr. 2012 Dec, 96 (6): 1454-1464.CrossRefPubMed
25.
go back to reference Greenhalgh T, Peacock R: Effectiveness and efficiency of search methods in systematic reviews of complex evidence: audit of primary sources. BMJ. 2005 Nov 5, 331 (7524): 1064-1065.PubMedCentralCrossRefPubMed Greenhalgh T, Peacock R: Effectiveness and efficiency of search methods in systematic reviews of complex evidence: audit of primary sources. BMJ. 2005 Nov 5, 331 (7524): 1064-1065.PubMedCentralCrossRefPubMed
26.
go back to reference Elkins MR, Herbert RD, Moseley AM, Sherrington C, Maher C: Rating the quality of trials in systematic reviews of physical therapy interventions. Cardiopulm Phys Ther J. 2010 Sep, 21 (3): 20-26.PubMedCentralPubMed Elkins MR, Herbert RD, Moseley AM, Sherrington C, Maher C: Rating the quality of trials in systematic reviews of physical therapy interventions. Cardiopulm Phys Ther J. 2010 Sep, 21 (3): 20-26.PubMedCentralPubMed
27.
go back to reference Moseley AM, Herbert RD, Sherrington C, Maher CG: Evidence for physiotherapy practice: a survey of the physiotherapy evidence database (PEDro). Aust J Physiother. 2002, 48 (1): 43-49.CrossRefPubMed Moseley AM, Herbert RD, Sherrington C, Maher CG: Evidence for physiotherapy practice: a survey of the physiotherapy evidence database (PEDro). Aust J Physiother. 2002, 48 (1): 43-49.CrossRefPubMed
28.
go back to reference Esmarck B, Andersen JL, Olsen S, Richter EA, Mizuno M, Kjaer M: Timing of postexercise protein intake is important for muscle hypertrophy with resistance training in elderly humans. J Physiol. 2001 Aug 15, 535 (Pt 1): 301-311.PubMedCentralCrossRefPubMed Esmarck B, Andersen JL, Olsen S, Richter EA, Mizuno M, Kjaer M: Timing of postexercise protein intake is important for muscle hypertrophy with resistance training in elderly humans. J Physiol. 2001 Aug 15, 535 (Pt 1): 301-311.PubMedCentralCrossRefPubMed
29.
go back to reference Holm L, Olesen JL, Matsumoto K, Doi T, Mizuno M, Alsted TJ: Protein-containing nutrient supplementation following strength training enhances the effect on muscle mass, strength, and bone formation in postmenopausal women. J Appl Physiol. 2008 Jul, 105 (1): 274-281.CrossRefPubMed Holm L, Olesen JL, Matsumoto K, Doi T, Mizuno M, Alsted TJ: Protein-containing nutrient supplementation following strength training enhances the effect on muscle mass, strength, and bone formation in postmenopausal women. J Appl Physiol. 2008 Jul, 105 (1): 274-281.CrossRefPubMed
30.
go back to reference White KM, Bauer SJ, Hartz KK, Baldridge M: Changes in body composition with yogurt consumption during resistance training in women. Int J Sport Nutr Exerc Metab. 2009 Feb, 19 (1): 18-33.PubMed White KM, Bauer SJ, Hartz KK, Baldridge M: Changes in body composition with yogurt consumption during resistance training in women. Int J Sport Nutr Exerc Metab. 2009 Feb, 19 (1): 18-33.PubMed
31.
go back to reference Kerksick CM, Rasmussen CJ, Lancaster SL, Magu B, Smith P, Melton C: The effects of protein and amino acid supplementation on performance and training adaptations during ten weeks of resistance training. J Strength Cond Res. 2006 Aug, 20 (3): 643-653.PubMed Kerksick CM, Rasmussen CJ, Lancaster SL, Magu B, Smith P, Melton C: The effects of protein and amino acid supplementation on performance and training adaptations during ten weeks of resistance training. J Strength Cond Res. 2006 Aug, 20 (3): 643-653.PubMed
32.
go back to reference Bemben MG, Witten MS, Carter JM, Eliot KA, Knehans AW, Bemben DA: The effects of supplementation with creatine and protein on muscle strength following a traditional resistance training program in middle-aged and older men. J Nutr Health Aging. 2010 Feb, 14 (2): 155-159.CrossRefPubMed Bemben MG, Witten MS, Carter JM, Eliot KA, Knehans AW, Bemben DA: The effects of supplementation with creatine and protein on muscle strength following a traditional resistance training program in middle-aged and older men. J Nutr Health Aging. 2010 Feb, 14 (2): 155-159.CrossRefPubMed
33.
go back to reference Antonio J, Sanders MS, Ehler LA, Uelmen J, Raether JB, Stout JR: Effects of exercise training and amino-acid supplementation on body composition and physical performance in untrained women. Nutrition. 2000 Nov-Dec, 16 (11-12): 1043-1046.CrossRefPubMed Antonio J, Sanders MS, Ehler LA, Uelmen J, Raether JB, Stout JR: Effects of exercise training and amino-acid supplementation on body composition and physical performance in untrained women. Nutrition. 2000 Nov-Dec, 16 (11-12): 1043-1046.CrossRefPubMed
34.
go back to reference Godard MP, Williamson DL, Trappe SW: Oral amino-acid provision does not affect muscle strength or size gains in older men. Med Sci Sports Exerc. 2002 Jul, 34 (7): 1126-1131.CrossRefPubMed Godard MP, Williamson DL, Trappe SW: Oral amino-acid provision does not affect muscle strength or size gains in older men. Med Sci Sports Exerc. 2002 Jul, 34 (7): 1126-1131.CrossRefPubMed
35.
go back to reference Rankin JW, Goldman LP, Puglisi MJ, Nickols-Richardson SM, Earthman CP, Gwazdauskas FC: Effect of post-exercise supplement consumption on adaptations to resistance training. J Am Coll Nutr. 2004 Aug, 23 (4): 322-330.CrossRefPubMed Rankin JW, Goldman LP, Puglisi MJ, Nickols-Richardson SM, Earthman CP, Gwazdauskas FC: Effect of post-exercise supplement consumption on adaptations to resistance training. J Am Coll Nutr. 2004 Aug, 23 (4): 322-330.CrossRefPubMed
36.
go back to reference Andersen LL, Tufekovic G, Zebis MK, Crameri RM, Verlaan G, Kjaer M: The effect of resistance training combined with timed ingestion of protein on muscle fiber size and muscle strength. Metabolism. 2005 Feb, 54 (2): 151-156.CrossRefPubMed Andersen LL, Tufekovic G, Zebis MK, Crameri RM, Verlaan G, Kjaer M: The effect of resistance training combined with timed ingestion of protein on muscle fiber size and muscle strength. Metabolism. 2005 Feb, 54 (2): 151-156.CrossRefPubMed
37.
go back to reference Bird SP, Tarpenning KM, Marino FE: Independent and combined effects of liquid carbohydrate/essential amino acid ingestion on hormonal and muscular adaptations following resistance training in untrained men. Eur J Appl Physiol. 2006 May, 97 (2): 225-238.CrossRefPubMed Bird SP, Tarpenning KM, Marino FE: Independent and combined effects of liquid carbohydrate/essential amino acid ingestion on hormonal and muscular adaptations following resistance training in untrained men. Eur J Appl Physiol. 2006 May, 97 (2): 225-238.CrossRefPubMed
38.
go back to reference Coburn JW, Housh DJ, Housh TJ, Malek MH, Beck TW, Cramer JT: Effects of leucine and whey protein supplementation during eight weeks of unilateral resistance training. J Strength Cond Res. 2006 May, 20 (2): 284-291.PubMed Coburn JW, Housh DJ, Housh TJ, Malek MH, Beck TW, Cramer JT: Effects of leucine and whey protein supplementation during eight weeks of unilateral resistance training. J Strength Cond Res. 2006 May, 20 (2): 284-291.PubMed
39.
go back to reference Candow DG, Burke NC, Smith-Palmer T, Burke DG: Effect of whey and soy protein supplementation combined with resistance training in young adults. Int J Sport Nutr Exerc Metab. 2006 Jun, 16 (3): 233-244.PubMed Candow DG, Burke NC, Smith-Palmer T, Burke DG: Effect of whey and soy protein supplementation combined with resistance training in young adults. Int J Sport Nutr Exerc Metab. 2006 Jun, 16 (3): 233-244.PubMed
40.
go back to reference Candow DG, Chilibeck PD, Facci M, Abeysekara S, Zello GA: Protein supplementation before and after resistance training in older men. Eur J Appl Physiol. 2006 Jul, 97 (5): 548-556.CrossRefPubMed Candow DG, Chilibeck PD, Facci M, Abeysekara S, Zello GA: Protein supplementation before and after resistance training in older men. Eur J Appl Physiol. 2006 Jul, 97 (5): 548-556.CrossRefPubMed
41.
go back to reference Hartman JW, Tang JE, Wilkinson SB, Tarnopolsky MA, Lawrence RL, Fullerton AV: Consumption of fat-free fluid milk after resistance exercise promotes greater lean mass accretion than does consumption of soy or carbohydrate in young, novice, male weightlifters. Am J Clin Nutr. 2007 Aug, 86 (2): 373-381.PubMed Hartman JW, Tang JE, Wilkinson SB, Tarnopolsky MA, Lawrence RL, Fullerton AV: Consumption of fat-free fluid milk after resistance exercise promotes greater lean mass accretion than does consumption of soy or carbohydrate in young, novice, male weightlifters. Am J Clin Nutr. 2007 Aug, 86 (2): 373-381.PubMed
42.
go back to reference Hoffman JR, Ratamess NA, Kang J, Falvo MJ, Faigenbaum AD: Effects of protein supplementation on muscular performance and resting hormonal changes in college football players. J Sports Sci Med. 2007, 6: 85-92.PubMedCentralPubMed Hoffman JR, Ratamess NA, Kang J, Falvo MJ, Faigenbaum AD: Effects of protein supplementation on muscular performance and resting hormonal changes in college football players. J Sports Sci Med. 2007, 6: 85-92.PubMedCentralPubMed
43.
go back to reference Eliot KA, Knehans AW, Bemben DA, Witten MS, Carter J, Bemben MG: The effects of creatine and whey protein supplementation on body composition in men aged 48 to 72 years during resistance training. J Nutr Health Aging. 2008 Mar, 12 (3): 208-212.CrossRefPubMed Eliot KA, Knehans AW, Bemben DA, Witten MS, Carter J, Bemben MG: The effects of creatine and whey protein supplementation on body composition in men aged 48 to 72 years during resistance training. J Nutr Health Aging. 2008 Mar, 12 (3): 208-212.CrossRefPubMed
44.
go back to reference Mielke M, Housh TJ, Malek MH, Beck T, Schmidt RJ, Johnson GO: The effects of whey protein and leucine supplementation on strength, muscular endurance, and body composition during resistance training. J Exerc Physiol Online. 2009, 12: 39-50. Mielke M, Housh TJ, Malek MH, Beck T, Schmidt RJ, Johnson GO: The effects of whey protein and leucine supplementation on strength, muscular endurance, and body composition during resistance training. J Exerc Physiol Online. 2009, 12: 39-50.
45.
go back to reference Josse AR, Tang JE, Tarnopolsky MA, Phillips SM: Body composition and strength changes in women with milk and resistance exercise. Med Sci Sports Exerc. 2010 Jun, 42 (6): 1122-1130.PubMed Josse AR, Tang JE, Tarnopolsky MA, Phillips SM: Body composition and strength changes in women with milk and resistance exercise. Med Sci Sports Exerc. 2010 Jun, 42 (6): 1122-1130.PubMed
46.
go back to reference Walker TB, Smith J, Herrera M, Lebegue B, Pinchak A, Fischer J: The influence of 8 weeks of whey-protein and leucine supplementation on physical and cognitive performance. Int J Sport Nutr Exerc Metab. 2010 Oct, 20 (5): 409-417.PubMed Walker TB, Smith J, Herrera M, Lebegue B, Pinchak A, Fischer J: The influence of 8 weeks of whey-protein and leucine supplementation on physical and cognitive performance. Int J Sport Nutr Exerc Metab. 2010 Oct, 20 (5): 409-417.PubMed
47.
go back to reference Vieillevoye S, Poortmans JR, Duchateau J, Carpentier A: Effects of a combined essential amino acids/carbohydrate supplementation on muscle mass, architecture and maximal strength following heavy-load training. Eur J Appl Physiol. 2010 Oct, 110 (3): 479-488.CrossRefPubMed Vieillevoye S, Poortmans JR, Duchateau J, Carpentier A: Effects of a combined essential amino acids/carbohydrate supplementation on muscle mass, architecture and maximal strength following heavy-load training. Eur J Appl Physiol. 2010 Oct, 110 (3): 479-488.CrossRefPubMed
48.
go back to reference Erskine RM, Fletcher G, Hanson B, Folland JP: Whey protein does not enhance the adaptations to elbow flexor resistance training. Med Sci Sports Exerc. 2012 Sep, 44 (9): 1791-1800.CrossRefPubMed Erskine RM, Fletcher G, Hanson B, Folland JP: Whey protein does not enhance the adaptations to elbow flexor resistance training. Med Sci Sports Exerc. 2012 Sep, 44 (9): 1791-1800.CrossRefPubMed
49.
go back to reference Weisgarber KD, Candow DG, Vogt ESM: Whey protein before and during resistance exercise has no effect on muscle mass and strength in untrained young adults. Int J Sport Nutr Exerc Metab. 2012 Jul, 4: Weisgarber KD, Candow DG, Vogt ESM: Whey protein before and during resistance exercise has no effect on muscle mass and strength in untrained young adults. Int J Sport Nutr Exerc Metab. 2012 Jul, 4:
50.
go back to reference Cooper H, Hedges L, Valentine J: The handbook of research synthesis and meta-analysis. 2009, New York: Russell Sage Foundation, 2 Cooper H, Hedges L, Valentine J: The handbook of research synthesis and meta-analysis. 2009, New York: Russell Sage Foundation, 2
51.
go back to reference Morris SB, DeShon RP: Combining effect size estimates in meta-analysis with repeated measures and independent-groups designs. Psychol Methods. 2002 Mar, 7 (1): 105-125.CrossRefPubMed Morris SB, DeShon RP: Combining effect size estimates in meta-analysis with repeated measures and independent-groups designs. Psychol Methods. 2002 Mar, 7 (1): 105-125.CrossRefPubMed
53.
go back to reference Hox JJ, de Leeuw ED, Hox JJ, de Leeuw ED: Multilevel models for meta-analysis. Reise SP, Duan N, editors. Multilevel modeling. Methodological advances, issues, and applications. Edited by: Duan N. 2003, Mahway, NJ: Lawrence Erlbaum Associates, 90-111. Hox JJ, de Leeuw ED, Hox JJ, de Leeuw ED: Multilevel models for meta-analysis. Reise SP, Duan N, editors. Multilevel modeling. Methodological advances, issues, and applications. Edited by: Duan N. 2003, Mahway, NJ: Lawrence Erlbaum Associates, 90-111.
54.
go back to reference Burnham KP, Anderson DR: Model selection and inference: A practical information-theoretic approach. 2002, New York: Springer-Verlag Burnham KP, Anderson DR: Model selection and inference: A practical information-theoretic approach. 2002, New York: Springer-Verlag
55.
go back to reference Hurvich CM, Tsai CL: Regression and time series model selection in small samples. Biometrika. 1989, 76: 297-307.CrossRef Hurvich CM, Tsai CL: Regression and time series model selection in small samples. Biometrika. 1989, 76: 297-307.CrossRef
56.
go back to reference Thompson SG, Sharp SJ: Explaining heterogeneity in meta-analysis: a comparison of methods. Stat Med. 1999 Oct 30, 18 (20): 2693-2708.CrossRefPubMed Thompson SG, Sharp SJ: Explaining heterogeneity in meta-analysis: a comparison of methods. Stat Med. 1999 Oct 30, 18 (20): 2693-2708.CrossRefPubMed
57.
go back to reference Berkey CS, Hoaglin DC, Mosteller F, Colditz GA: A random-effects regression model for meta-analysis. Stat Med. 1995 Feb 28, 14 (4): 395-411.CrossRefPubMed Berkey CS, Hoaglin DC, Mosteller F, Colditz GA: A random-effects regression model for meta-analysis. Stat Med. 1995 Feb 28, 14 (4): 395-411.CrossRefPubMed
58.
go back to reference Edwards D, Berry JJ: The efficiency of simulation-based multiple comparisons. Biometrics. 1987 Dec, 43 (4): 913-928.CrossRefPubMed Edwards D, Berry JJ: The efficiency of simulation-based multiple comparisons. Biometrics. 1987 Dec, 43 (4): 913-928.CrossRefPubMed
59.
go back to reference Campbell B, Kreider RB, Ziegenfuss T, La Bounty P, Roberts M, Burke D: International society of sports nutrition position stand: protein and exercise. J Int Soc Sports Nutr. 2007 Sep 26, 4: 8-PubMedCentralCrossRefPubMed Campbell B, Kreider RB, Ziegenfuss T, La Bounty P, Roberts M, Burke D: International society of sports nutrition position stand: protein and exercise. J Int Soc Sports Nutr. 2007 Sep 26, 4: 8-PubMedCentralCrossRefPubMed
60.
go back to reference American College of Sports Medicine, American Dietetic Association, Dietitians of Canada: Joint position statement: Nutrition and athletic performance. american college of sports medicine, american dietetic association, and dietitians of canada. Med Sci Sports Exerc. 2000 Dec, 32 (12): 2130-2145.CrossRef American College of Sports Medicine, American Dietetic Association, Dietitians of Canada: Joint position statement: Nutrition and athletic performance. american college of sports medicine, american dietetic association, and dietitians of canada. Med Sci Sports Exerc. 2000 Dec, 32 (12): 2130-2145.CrossRef
61.
go back to reference Lemon PW, Tarnopolsky MA, MacDougall JD, Atkinson SA: Protein requirements and muscle mass/strength changes during intensive training in novice bodybuilders. J Appl Physiol. 1992 Aug, 73 (2): 767-775.PubMed Lemon PW, Tarnopolsky MA, MacDougall JD, Atkinson SA: Protein requirements and muscle mass/strength changes during intensive training in novice bodybuilders. J Appl Physiol. 1992 Aug, 73 (2): 767-775.PubMed
62.
go back to reference Lemon PW: Beyond the zone: protein needs of active individuals. J Am Coll Nutr. 2000 Oct, 19 (5 Suppl): 513S-521S.CrossRefPubMed Lemon PW: Beyond the zone: protein needs of active individuals. J Am Coll Nutr. 2000 Oct, 19 (5 Suppl): 513S-521S.CrossRefPubMed
63.
go back to reference Moore DR, Del Bel NC, Nizi KI, Hartman JW, Tang JE, Armstrong D: Resistance training reduces fasted- and fed-state leucine turnover and increases dietary nitrogen retention in previously untrained young men. J Nutr. 2007 Apr, 137 (4): 985-991.PubMed Moore DR, Del Bel NC, Nizi KI, Hartman JW, Tang JE, Armstrong D: Resistance training reduces fasted- and fed-state leucine turnover and increases dietary nitrogen retention in previously untrained young men. J Nutr. 2007 Apr, 137 (4): 985-991.PubMed
64.
go back to reference van Houwelingen HC, Arends LR, Stijnen T: Advanced methods in meta-analysis: multivariate approach and meta-regression. Stat Med. 2002 Feb 28, 21 (4): 589-624.CrossRefPubMed van Houwelingen HC, Arends LR, Stijnen T: Advanced methods in meta-analysis: multivariate approach and meta-regression. Stat Med. 2002 Feb 28, 21 (4): 589-624.CrossRefPubMed
65.
go back to reference Peterson MD, Rhea MR, Alvar BA: Applications of the dose-response for muscular strength development: a review of meta-analytic efficacy and reliability for designing training prescription. J Strength Cond Res. 2005 Nov, 19 (4): 950-958.PubMed Peterson MD, Rhea MR, Alvar BA: Applications of the dose-response for muscular strength development: a review of meta-analytic efficacy and reliability for designing training prescription. J Strength Cond Res. 2005 Nov, 19 (4): 950-958.PubMed
66.
go back to reference Ogasawara R, Kobayashi K, Tsutaki A, Lee K, Abe T, Fujita S: mTOR signaling response to resistance exercise is altered by chronic resistance training and detraining in skeletal muscle. J Appl Physiol. 2013 Jan, 31: Ogasawara R, Kobayashi K, Tsutaki A, Lee K, Abe T, Fujita S: mTOR signaling response to resistance exercise is altered by chronic resistance training and detraining in skeletal muscle. J Appl Physiol. 2013 Jan, 31:
67.
go back to reference Coffey VG, Zhong Z, Shield A, Canny BJ, Chibalin AV, Zierath JR: Early signaling responses to divergent exercise stimuli in skeletal muscle from well-trained humans. FASEB J. 2006 Jan, 20 (1): 190-192.PubMed Coffey VG, Zhong Z, Shield A, Canny BJ, Chibalin AV, Zierath JR: Early signaling responses to divergent exercise stimuli in skeletal muscle from well-trained humans. FASEB J. 2006 Jan, 20 (1): 190-192.PubMed
Metadata
Title
The effect of protein timing on muscle strength and hypertrophy: a meta-analysis
Authors
Brad Jon Schoenfeld
Alan Albert Aragon
James W Krieger
Publication date
01-12-2013
Publisher
BioMed Central
DOI
https://doi.org/10.1186/1550-2783-10-53

Other articles of this Issue 1/2013

Journal of the International Society of Sports Nutrition 1/2013 Go to the issue