Effects of protein supplementation combined with resistance exercise on body composition and physical function in older adults: A systematic review and meta-analysis

American Journal of Clinical Nutrition

Volumn 106, Issue 4, 2017, Pages 1078-1091

  Liao, Chun De ^a,b   Tsauo, Jau Yih ^a   Wu, Yen Tzu ^a   Cheng, Chin Pao ^e   Chen, Hui Chuen ^e   Huang, Yi Ching ^f   Chen, Hung Chou ^b,c,d   Liou, Tsan Hon ^b,d  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^e NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^f NATIONAL TAIPEI UNIVERSITY OF NURSING AND HEALTH SCIENCES   (Taiwan)

Author keywords

Body composition; Elderly people; Obesity; Protein supplementation; Resistance exercise

Indexed keywords

CASEIN; LEUCINE; MILK PROTEIN; PROTEIN; WHEY PROTEIN; PROTEIN INTAKE;

ARTICLE; BODY COMPOSITION; BODY MASS; COCHRANE LIBRARY; DIET SUPPLEMENTATION; EMBASE; HUMAN; LEG MUSCLE; MEDLINE; META ANALYSIS; MUSCLE MASS; MUSCLE STRENGTH; PEDRO; PHYSICAL MOBILITY; PROTEIN INTAKE; RANDOMIZED CONTROLLED TRIAL (TOPIC); RESISTANCE TRAINING; SARCOPENIC OBESITY; SYSTEMATIC REVIEW; AGED; DIETARY SUPPLEMENT; DRUG EFFECTS; FEMALE; FITNESS; MALE; METABOLISM; MIDDLE AGED; MUSCLE; OBESITY; PHARMACOLOGY; PHYSIOLOGY; SARCOPENIA; VERY ELDERLY;

AGED; AGED, 80 AND OVER; BODY COMPOSITION; DIETARY PROTEINS; DIETARY SUPPLEMENTS; FEMALE; HUMANS; MALE; MIDDLE AGED; MUSCLE STRENGTH; MUSCLES; OBESITY; PHYSICAL FITNESS; RESISTANCE TRAINING; SARCOPENIA;

EID: 85031665729     PISSN: 00029165     EISSN: 19383207     Source Type: Journal    
DOI: 10.3945/ajcn.116.143594     Document Type: Article

References (62)

1. Lechleitner M. The elderly as a target for obesity treatment. Expert Rev Endocrinol Metab 2015;10:375–80.
2. von Haehling S, Morley JE, Anker SD. From muscle wasting to sarcopenia and myopenia: update 2012. J Cachexia Sarcopenia Muscle 2012;3:213–7.
3. Kalyani RR, Corriere M, Ferrucci L. Age-related and disease-related muscle loss: the effect of diabetes, obesity, and other diseases. Lancet Diabetes Endocrinol 2014;2:819–29.
4. Roy B, Curtis ME, Fears LS, Nahashon SN, Fentress HM. Molecular mechanisms of obesity-induced osteoporosis and muscle atrophy. Front Physiol 2016;7:439.
5. Pedersen AN, Ovesen L, Schroll M, Avlund K, Era P. Body composition of 80-years old men and women and its relation to muscle strength, physical activity and functional ability. J Nutr Health Aging 2002;6:413–20.
6. Vincent HK, Vincent KR, Lamb KM. Obesity and mobility disability in the older adult. Obes Rev 2010;11:568–79.
7. Lee S, Kim TN, Kim SH. Sarcopenic obesity is more closely associated with knee osteoarthritis than is nonsarcopenic obesity: a cross-sectional study. Arthritis Rheum 2012;64:3947–54.
8. Nilwik R, Snijders T, Leenders M, Groen BB, van Kranenburg J, Verdijk LB, van Loon LJ. The decline in skeletal muscle mass with aging is mainly attributed to a reduction in type II muscle fiber size. Exp Gerontol 2013;48:492–8.
9. Verdijk LB, Gleeson BG, Jonkers RA, Meijer K, Savelberg HH, Dendale P, van Loon LJ. Skeletal muscle hypertrophy following resistance training is accompanied by a fiber type-specific increase in satellite cell content in elderly men. J Gerontol A Biol Sci Med Sci 2009;64:332–9.
10. Damas F, Phillips S, Vechin FC, Ugrinowitsch C. A review of resistance training-induced changes in skeletal muscle protein synthesis and their contribution to hypertrophy. Sports Med 2015;45: 801–7.
11. Yarasheski KE. Exercise, aging, and muscle protein metabolism. J Gerontol A Biol Sci Med Sci 2003;58:M918–22.
12. Peterson MD, Sen A, Gordon PM. Influence of resistance exercise on lean body mass in aging adults: a meta-analysis. Med Sci Sports Exerc 2011;43:249–58.
13. Tieland M, Dirks ML, van der Zwaluw N, Verdijk LB, van de Rest O, de Groot LC, van Loon LJ. Protein supplementation increases muscle mass gain during prolonged resistance-type exercise training in frail elderly people: a randomized, double-blind, placebo-controlled trial. J Am Med Dir Assoc 2012;13:713–9.
14. 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;96:1454–64.
15. Finger D, Goltz FR, Umpierre D, Meyer E, Rosa LH, Schneider CD. Effects of protein supplementation in older adults undergoing resistance training: a systematic review and meta-analysis. Sports Med 2015;45:245–55.
16. Miller PE, Alexander DD, Perez V. Effects of whey protein and resistance exercise on body composition: a meta-analysis of randomized controlled trials. J Am Coll Nutr 2014;33:163–75.
17. Coker RH, Miller S, Schutzler S, Deutz N, Wolfe RR. Whey protein and essential amino acids promote the reduction of adipose tissue and increased muscle protein synthesis during caloric restriction-induced weight loss in elderly, obese individuals. Nutr J 2012;11:105–11.
18. Maltais ML, Ladouceur JP, Dionne IJ. The effect of resistance training and different sources of postexercise protein supplementation on muscle mass and physical capacity in sarcopenic elderly men. J Strength Cond Res 2016;30:1680–7.
19. Hofmann M, Schober-Halper B, Oesen S, Franzke B, Tschan H, Bachl N, Strasser EM, Quittan M, Wagner KH, Wessner B. Effects of elastic band resistance training and nutritional supplementation on muscle quality and circulating muscle growth and degradation factors of institutionalized elderly women: the Vienna Active Ageing Study (VAAS). Eur J Appl Physiol 2016;116:885–97.
20. Zdzieblik D, Oesser S, Baumstark MW, Gollhofer A, König D. Collagen peptide supplementation in combination with resistance training improves body composition and increases muscle strength in elderly sarcopenic men: a randomised controlled trial. Br J Nutr 2015;114: 1237–45.
21. Verreijen AM, Verlaan S, Engberink MF, Swinkels S, de Vogel-van den Bosch J, Weijs PJ. A high whey protein-, leucine-, and vitamin D-enriched supplement preserves muscle mass during intentional weight loss in obese older adults: a double-blind randomized controlled trial. Am J Clin Nutr 2015;101:279–86.
22. Oesen S, Halper B, Hofmann M, Jandrasits W, Franzke B, Strasser EM, Graf A, Tschan H, Bachl N, Quittan M, et al. Effects of elastic band resistance training and nutritional supplementation on physical performance of institutionalised elderly - A randomized controlled trial. Exp Gerontol 2015;72:99–108.
23. Kim GM, Woo JM. Determinants for heart rate variability in a normal Korean population. J Korean Med Sci 2011;26:1293–8.
24. Stout JR, Smith-Ryan AE, Fukuda DH, Kendall KL, Moon JR, Hoffman JR, Wilson JM, Oliver JS, Mustad VA. Effect of calcium beta-hydroxy-beta-methylbutyrate (CaHMB) with and without resistance training in men and women 65+yrs: a randomized, double-blind pilot trial. Exp Gerontol 2013;48:1303–10.
25. Leenders M, Verdijk LB, van der Hoeven L, van Kranenburg J, Nilwik R, Wodzig WK, Senden JM, Keizer HA, van Loon LJ. Protein supplementation during resistance-type exercise training in the elderly. Med Sci Sports Exerc 2013;45:542–52.
26. Chalé A, Cloutier GJ, Hau C, Phillips EM, Dallal GE, Fielding RA. Efficacy of whey protein supplementation on resistance exercise-induced changes in lean mass, muscle strength, and physical function in mobility-limited older adults. J Gerontol A Biol Sci Med Sci 2013; 68:682–90.
27. Arnarson A, Gudny Geirsdottir O, Ramel A, Briem K, Jonsson PV, Thorsdottir I. Effects of whey proteins and carbohydrates on the efficacy of resistance training in elderly people: double blind, randomised controlled trial. Eur J Clin Nutr 2013;67:821–6.
28. Mojtahedi MC, Thorpe MP, Karampinos DC, Johnson CL, Layman DK, Georgiadis JG, Evans EM. The effects of a higher protein intake during energy restriction on changes in body composition and physical function in older women. J Gerontol A Biol Sci Med Sci 2011; 66:1218–25.
29. Björkman MP, Pilvi TK, Kekkonen RA, Korpela R, Tilvis RS. Similar effects of leucine rich and regular dairy products on muscle mass and functions of older polymyalgia rheumatica patients: a randomized crossover trial. J Nutr Health Aging 2011;15:462–7.
30. Candow DG, Little JP, Chilibeck PD, Abeysekara S, Zello GA, Kazachkov M, Cornish SM, Yu PH. Low-dose creatine combined with protein during resistance training in older men. Med Sci Sports Exerc 2008;40:1645–52.
31. 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;97:548–56.
32. Vukovich MD, Stubbs NB, Bohlken RM. Body composition in 70-year-old adults responds to dietary beta-hydroxy-beta-methylbutyrate similarly to that of young adults. J Nutr 2001;131:2049–52.
33. Gryson C, Ratel S, Rance M, Penando S, Bonhomme C, Le Ruyet P, Duclos M, Boirie Y, Walrand S. Four-month course of soluble milk proteins interacts with exercise to improve muscle strength and delay fatigue in elderly participants. J Am Med Dir Assoc 2014;15: 958 e1–9.
34. Verdijk LB, Jonkers RA, Gleeson BG, Beelen M, Meijer K, Savelberg HH, Wodzig KW, Dendale P, van Loon LJ. Protein supplementation before and after exercise does not further augment skeletal muscle hypertrophy after resistance training in elderly men. Am J Clin Nutr 2009;89:608–16.
35. Shamseer L, Moher D, Clarke M, Ghersi D, Liberati A, Petticrew M, Shekelle P, Stewart LA. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. BMJ 2015;349:g7647.
36. Baumgartner RN. Body composition in healthy aging. Ann N Y Acad Sci 2000;904:437–48.
37. Villanueva MG, He J, Schroeder ET. Periodized resistance training with and without supplementation improve body composition and performance in older men. Eur J Appl Physiol 2014;114:891–905.
38. Kapur KC, Lamberson LR. Reliability in engineering design. New York: John Wiley & Sons Inc.; 1977.
39. Abrams KR, Gillies CL, Lambert PC. Meta-analysis of heterogeneously reported trials assessing change from baseline. Stat Med 2005; 24:3823–44.
40. Hume R. Prediction of lean body mass from height and weight. J Clin Pathol 1966;19:389–91.
41. Jacobs JV, Horak FB, Tran VK, Nutt JG. Multiple balance tests improve the assessment of postural stability in subjects with Parkinson’s disease. J Neurol Neurosurg Psychiatry 2006;77:322–6.
42. Bowden J, Tierney JF, Copas AJ, Burdett S. Quantifying, displaying and accounting for heterogeneity in the meta-analysis of RCTs using standard and generalised Q statistics. BMC Med Res Methodol 2011; 11:41.
43. Sedgwick P, Marston L. How to read a funnel plot in a meta-analysis. BMJ 2015;351:h4718.
44. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997;315:629–34.
45. de Morton NA. The PEDro scale is a valid measure of the methodological quality of clinical trials: a demographic study. Aust J Physiother 2009;55:129–33.
46. Maher CG, Sherrington C, Herbert RD, Moseley AM, Elkins M. Reliability of the PEDro scale for rating quality of randomized controlled trials. Phys Ther 2003;83:713–21.
47. Foley NC, Bhogal SK, Teasell RW, Bureau Y, Speechley MR. Estimates of quality and reliability with the physiotherapy evidence-based database scale to assess the methodology of randomized controlled trials of pharmacological and nonpharmacological interventions. Phys Ther 2006;86:817–24.
48. Lagally KM, Robertson RJ. Construct validity of the OMNI resistance exercise scale. J Strength Cond Res 2006;20:252–6.
49. McCraty R, Atkinson M, Tomasino D, Stuppy WP. Analysis of twenty-four hour heart rate variability in patients with panic disorder. Biol Psychol 2001;56:131–50.
50. Wilson GJ, Wilson JM, Manninen AH. Effects of beta-hydroxy-beta-methylbutyrate (HMB) on exercise performance and body composition across varying levels of age, sex, and training experience: a review. Nutr Metab (Lond) 2008;5:1.
51. Hulmi JJ, Lockwood CM, Stout JR. Effect of protein/essential amino acids and resistance training on skeletal muscle hypertrophy: a case for whey protein. Nutr Metab (Lond) 2010;7:51.
52. West DW, Burd NA, Coffey VG, Baker SK, Burke LM, Hawley JA, Moore DR, Stellingwerff T, Phillips SM. Rapid aminoacidemia enhances myofibrillar protein synthesis and anabolic intramuscular signaling responses after resistance exercise. Am J Clin Nutr 2011;94: 795–803.
53. Fry CS, Drummond MJ, Glynn EL, Dickinson JM, Gundermann DM, Timmerman KL, Walker DK, Volpi E, Rasmussen BB. Skeletal muscle autophagy and protein breakdown following resistance exercise are similar in younger and older adults. J Gerontol A Biol Sci Med Sci 2013;68:599–607.
54. Weinheimer EM, Conley TB, Kobza VM, Sands LP, Lim E, Janle EM, Campbell WW. Whey protein supplementation does not affect exercise training-induced changes in body composition and indices of metabolic syndrome in middle-aged overweight and obese adults. J Nutr 2012; 142:1532–9.
55. Han TS, Tajar A, Lean ME. Obesity and weight management in the elderly. Br Med Bull 2011;97:169–96.
56. Newman AB, Lee JS, Visser M, Goodpaster BH, Kritchevsky SB, Tylavsky FA, Nevitt M, Harris TB. Weight change and the conservation of lean mass in old age: the Health, Aging and Body Composition Study. Am J Clin Nutr 2005;82:872–8.
57. Li Z, Heber D. Sarcopenic obesity in the elderly and strategies for weight management. Nutr Rev 2012;70:57–64.
58. Poggiogalle E, Migliaccio S, Lenzi A, Donini LM. Treatment of body composition changes in obese and overweight older adults: insight into the phenotype of sarcopenic obesity. Endocrine 2014;47:699–716.
59. van de Rest O, van der Zwaluw NL, Tieland M, Adam JJ, Hiddink GJ, van Loon LJ, de Groot LC. Effect of resistance-type exercise training with or without protein supplementation on cognitive functioning in frail and pre-frail elderly: secondary analysis of a randomized, double-blind, placebo-controlled trial. Mech Ageing Dev 2014;136-137:85–93.
60. Burd NA, Tang JE, Moore DR, Phillips SM. Exercise training and protein metabolism: influences of contraction, protein intake, and sex-based differences. J Appl Physiol (1985) 2009;106:1692–701.
61. Pasco JA, Holloway KL, Dobbins AG, Kotowicz MA, Williams LJ, Brennan SL. Body mass index and measures of body fat for defining obesity and underweight: a cross-sectional, population-based study. BMC Obes 2014;1:9.
62. Waters DL, Baumgartner RN. Sarcopenia and obesity. Clin Geriatr Med 2011;27:401–21.