Greek Yogurt and 12 Weeks of Exercise Training on Strength, Muscle Thickness and Body Composition in Lean, Untrained, University-Aged Males

Aaron Bridge, Joseph Brown, Hayden Snider, Matthew Nasato, Wendy E Ward, Brian D Roy, Andrea R Josse, Aaron Bridge, Joseph Brown, Hayden Snider, Matthew Nasato, Wendy E Ward, Brian D Roy, Andrea R Josse

Abstract

Milk and/or whey protein plus resistance exercise (RT) increase strength and muscle size, and optimize body composition in adult males and females. Greek yogurt (GY) contains similar muscle-supporting nutrients as milk yet it is different in several ways including being a semi-solid food, containing bacterial cultures and having a higher protein content (mostly casein) per serving. GY has yet to be investigated in the context of a RT program. The purpose of this study was to assess the effects of GY consumption plus RT on strength, muscle thickness and body composition in lean, untrained, university-aged males. Thirty untrained, university-aged (20.6 ± 2.2 years) males were randomized to 2 groups (n = 15/group): fat-free, plain GY or a Placebo Pudding (PP; isoenergetic carbohydrate-based pudding) and underwent a combined RT/plyometric training program 3 days/week for 12 weeks. They consumed either GY (20 g protein/dose) or PP (0 g protein/dose) daily, 3 times on training days and 2 times on non-training days. After 12 weeks, both groups significantly increased strength, muscle thickness and fat-free mass (FFM) (p < 0.05). The GY group gained more total strength (GY; 98 ± 37 kg, PP; 57 ± 15 kg), more biceps brachii muscular thickness (GY; 0.46 ± 0.3 cm, PP; 0.12 ± 0.2 cm), more FFM (GY; 2.4 ± 1.5 kg, PP; 1.3 ± 1.3 kg), and reduced % body fat (GY; -1.1 ± 2.2%, PP; 0.1 ± 2.6%) than PP group (p < 0.05 expressed as absolute change). Thus, consumption of GY during a training program resulted in improved strength, muscle thickness and body composition over a carbohydrate-based placebo. Given the results of our study, the general benefits of consuming GY and its distinctiveness from milk, GY can be a plausible, post-exercise, nutrient-rich alternative for positive strength, muscle, and body composition adaptations.

Keywords: Greek yogurt; body composition; intervention study; muscle thickness; muscular strength; protein nutrition; resistance training program; young males.

Figures

Figure 1
Figure 1
Total 1-RM strength before and 12 weeks after RT and PLY in GY (n = 14) and PP (n = 15) groups. Individual pre and post-responses are represented by the lines over the bars. The inset graph shows the change in total 1-RM strength from baseline. †Significantly different from Pre within the same group (p < 0.05). *Significantly different from PP in the change from baseline in inset (p < 0.001). Values are presented as mean ± SE. RM = Repetition maximum.
Figure 2
Figure 2
Fat-free mass before and 12 weeks after RT and PLY in GY (n = 14) and PP (n = 15). Individual pre and post-responses are represented by the lines over the bars. The inset graph shows the change in total fat-free mass from baseline. †Significantly different from Pre within the same group (p < 0.05). *Significantly different from PP in the change from baseline in inset (p < 0.05). Bars are presented as mean ± SE.
Figure 3
Figure 3
Total fat-free mass before and 12 weeks after RT and PLY in GY (n = 14) and PP (n = 15). Individual pre and post-responses are represented by the lines over the bars. The inset graph shows the change in total fat-free mass from baseline. α Significantly different at baseline between groups (p < 0.05). *Significantly different from PP in the change from baseline in inset as assessed by ANCOVA (p < 0.05). Bars are presented as mean ± SE.
Figure 4
Figure 4
Fat mass and Fat-free mass visually expressed as a percent of total mass change during the intervention for the GY and PP groups (GY = 14, PP = 15).

References

    1. Devries M, Phillips S. Supplemental protein in support of muscle mass and health: advantage whey. J Food Sci. (2015) 1:8–15. 10.1111/1750-3841.12802
    1. Morton RW, Murphy KT, McKellar SR, Schoenfeld BJ, Henselmans M, Helms E, et al. . 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. Br J Sports Med. (2017) 52:376–84. 10.1136/bjsports-2017-097608
    1. Cermak NM, Res PT, De Groot LCPGM, Saris WHM, Van Loon LJC. 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. 10.3945/ajcn.112.037556
    1. Anthony JC, Anthony TG, Kimball SR, Jefferson LS. Signaling pathways involved in translational control of protein synthesis in skeletal muscle by leucine. J Nutr. (2001) 131:856–60. 10.1093/jn/131.3.856S
    1. Layman DK, Anthony TG, Rasmussen BB, Adams SH, Lynch CJ, Brinkworth GD, et al. . Defining meal requirements for protein to optimize metabolic roles of amino acids. Am J Clin Nutr. (2015) 101:1330S−8S. 10.3945/ajcn.114.084053
    1. Norton LE, Layman DK. Leucine regulates translation initiation of protein synthesis in skeletal muscle after exercise. J Nutr. (2006) 136:533S−7S. 10.1093/jn/136.2.533S
    1. Christensen R, Lorenzen JK, Svith CR, Bartels EM, Melanson EL, Saris WH, et al. . Effect of calcium from dairy and dietary supplements on faecal fat excretion: A meta-analysis of randomized controlled trials. Obes Rev. (2009) 10:475–86. 10.1111/j.1467-789X.2009.00599.x
    1. Panahi S, Tremblay A. The potential role of yogurt in weight management and prevention of type 2 diabetes. J Am Coll Nutr. (2016) 35:717–31. 10.1080/07315724.2015.1102103
    1. 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. 10.1080/07315724.2013.875365
    1. Boirie Y, Dangin M, Gachon P, Vasson MP, Maubois JL, Beaufrere B. Slow and fast dietary proteins differently modulate postprandial protein accretion. Proc Natl Acad Sci USA. (1997) 94:14930–5. 10.1073/pnas.94.26.14930
    1. Reitelseder S, Agergaard J, Doessing S, Helmark IC, Lund P, Kristensen NB, et al. Whey and casein labeled with L-[1-13C]leucine and muscle protein synthesis: effect of resistance exercise and protein ingestion. Am J Physiol Endocrinol Metab. (2011) 300:E231–42. 10.1152/ajpendo.00513.2010
    1. Hartman JW, Tang JE, Wilkinson SB, Tarnopolsky MA, Lawrence RL, Fullerton AV, et al. . Phillips SM. 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) 86:373–81. 10.1093/ajcn/86.2.373
    1. 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) 42:1122–30. 10.1249/MSS.0b013e3181c854f6
    1. Naclerio F, Larumbe-Zabala E. Effects of whey protein alone or as part of a multi-ingredient formulation on strength, fat-free mass, or lean body mass in resistance-trained individuals: a meta-analysis. Sports Med. (2016) 2016:125–37. 10.1007/s40279-015-0403-y
    1. Thorning TK, Bertram HC, Bonjour JP, De Groot L, Dupont D, Feeney E, et al. . Whole dairy matrix or single nutrients in assessment of health effects: current evidence and knowledge gaps. Am J Clin Nutr. (2017) 105:1033–45. 10.3945/ajcn.116.151548
    1. Josse AR, Phillips SM. Impact of milk consumption and resistance training on body composition of female athletes. Med Sport Sci. (2013) 59:94–103. 10.1159/000341968
    1. 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) 23:322–30. 10.1080/07315724.2004.10719375
    1. Zhu Y, Hsu WH, Hollis JH. The impact of food viscosity on eating rate, subjective appetite, glycemic response and gastric emptying rate. PLoS ONE. (2013) 8:e67482. 10.1371/journal.pone.0067482
    1. Beena Divya J, Kulangara Varsha K, Madhavan Nampoothiri K, Ismail B, Pandey A. Probiotic fermented foods for health benefits. Eng Life Sci. (2012) 12:377–90. 10.1002/elsc.201100179
    1. Ismail MM, Ibrahim MM, Youssef EF, El Shorbagy KM. Plyometric training versus resistive exercises after acute lateral ankle sprain. Foot Ankle Int. (2010) 31:523–30. 10.3113/FAI.2010.0523
    1. Marco ML, Heeney D, Binda S, Cifelli CJ, Cotter PD, Foligne B, et al. . Health benefits of fermented foods: microbiota and beyond. Curr Opin Biotechnol. (2017) 44:94–102. 10.1016/j.copbio.2016.11.010
    1. Tamang JP, Shin DH, Jung SJ, Chae SW. Functional properties of microorganisms in fermented foods. Front Microbiol. (2016) 7:578. 10.3389/fmicb.2016.00578
    1. Jacques PF, Wang H. Yogurt and weight management. Am J Clin Nutr. (2014) 99:1229S−34S. 10.3945/ajcn.113.073031
    1. Fernandez MA, Marette A. Potential health benefits of combining yogurt and fruits based on their probiotic and prebiotic properties. Adv Nutr An Int Rev J. (2017) 8:155–64. 10.3945/an.115.011114
    1. Chandan RC. An overview of yogurt production and composition. Yogurt Health Dis Prev. (2017) 2017:31–47. 10.1016/B978-0-12-805134-4.00002-X
    1. 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) 19:18–33. 10.1123/ijsnem.19.1.18
    1. Zemel MB, Richards J, Mathis S, Milstead A, Gebhardt L, Silva E. Dairy augmentation of total and central fat loss in obese subjects. Int J Obes. (2005) 29:391–7. 10.1038/sj.ijo.0802880
    1. Thomas DT, Wideman L, Lovelady CA. Effects of a dairy supplement and resistance training on lean mass and insulin-like growth factor in women. Int J Sport Nutr Exerc Metab. (2011) 21:181–8. 10.1123/ijsnem.21.3.181
    1. Moore DR, Robinson MJ, Fry JL, Tang JE, Glover EI, Wilkinson SB, et al. . Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise in young men. Am J Clin Nutr. (2009) 89:161–8. 10.3945/ajcn.2008.26401
    1. Witard OC, Jackman SR, Breen L, Smith K, Selby A, Tipton KD. Myofibrillar muscle protein synthesis rates subsequent to a meal in response to increasing doses of whey protein at rest and after resistance exercise. Am J Clin Nutr. (2014) 99:86–95. 10.3945/ajcn.112.055517
    1. Danone (2019). Available online at: (accessed February 1, 2019).
    1. Natrel (2019). Available online at: (accessed February 1, 2019).
    1. Fisberg M, Machado R. History of yogurt and current patterns of consumption. Nutr Rev. (2015) 73:4–7. 10.1093/nutrit/nuv020
    1. Wu L, Sun D. Consumption of yogurt and the incident risk of cardiovascular disease: A meta-analysis of nine cohort studies. Nutrients. (2017) 9:315. 10.3390/nu9030315
    1. Dehghan M, Mente A, Rangarajan S, Sheridan P, Mohan V, Iqbal R, et al. . Association of dairy intake with cardiovascular disease and mortality in 21 countries from five continents (PURE): a prospective cohort study. Lancet. (2018) 392: 2288–2297. 10.1016/S0140-6736(18)31812-9
    1. Haff G, Haff E. Training Integration and Periodization. NSCA's Guide to Program Design. Windsor, ON: Human Kinetics, Inc; (2012).
    1. Mayhew JL, Johnson BD, Lamonte MJ, Lauber D, Kemmler W. Accuracy of prediction equations for determining one repetition maximum bench press in women before and after resistance training. J Strength Cond Res. (2008) 22:1570–7. 10.1519/JSC.0b013e31817b02ad
    1. LeSuer DA, McCormick JH, Mayhew JL, Wasserstein RL, Arnold MD. The accuracy of prediction equations for estimating 1-rm performance in the bench press, squat, and deadlift. J Strength Cond Res. (1997) 11:211.
    1. Dohoney P, Chromiak JA, Lemire D, Abadie BR, Kovacs C. Prediction of one repetition maximum (1-RM) strength from a 4-6 RM and a7-10 RM submaximal strength test in healthy young adult males. J Exerc Physiol. (2002) 5:54–9. Available online at:
    1. Bamman MM, Newcomer BR, Larson-Meyer DE, Weinsier RL, Hunter GR. Evaluation of the strength-size relationship in vivo using various muscle size indices. Med Sci Sports Exerc. (2000) 32:1307–13. 10.1097/00005768-200007000-00019
    1. Lemon PW. Beyond the zone: protein needs of active individuals. J Am Coll Nutr. (2000) 19:513S−21S. 10.1080/07315724.2000.10718974
    1. Schoenfeld BJ, Aragon AA. How much protein can the body use in a single meal for muscle-building? Implications for daily protein distribution. J Int Soc Sports Nutr. (2018) 15:10. 10.1186/s12970-018-0215-1
    1. Hakkinen K, Pakarinen A, Alen M, Kauhanen H, Komi PV. Neuromuscular and hormonal adaptations in athletes to strength training in two years. J Appl Physiol. (1988) 65:2406–12. 10.1152/jappl.1988.65.6.2406
    1. Phillips SM. Protein requirements and supplementation in strength sports. Nutrition. (2004) 20:689–95. 10.1016/j.nut.2004.04.009
    1. Snijders T, Res PT, Smeets JSJ, Vliet SV, Kranenburg JV, Maase K, et al. . Protein ingestion before sleep increases muscle mass and strength gains during prolonged resistance-type exercise training in healthy young men. J Nutr. (2015) 145:1178–84. 10.3945/jn.114.208371
    1. 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) 32:467–77. 10.1007/s00726-006-0398-7
    1. Andersen LL, Tufekovic G, Zebis MK, Crameri RM, Verlaan G, Kjaer M, et al. . The effect of resistance training combined with timed ingestion of protein on muscle fiber size and muscle strength. Metabolism. (2005) 54:151–6. 10.1016/j.metabol.2004.07.012
    1. Folland JP, Williams AG. The adaptations to strength training: morphological and neurological contributions to increased strength. Sport Med. (2007) 37:145–68. 10.2165/00007256-200737020-00004
    1. Schoenfeld BJ. The mechanisms of muscle hypertrophy and their application to resistance training. J Strength Cond Res. (2010) 24:2857–72. 10.1519/JSC.0b013e3181e840f3
    1. Schoenfeld BJ. Potential mechanisms for a role of metabolic stress in hypertrophic adaptations to resistance training. Sport Med. (2013) 43:179–94. 10.1007/s40279-013-0017-1
    1. Phillips SM, Hartman JW, Wilkinson SB. Dietary protein to support anabolism with resistance exercise in young men. J Am Coll Nutr. (2005) 24:134S−9S. 10.1080/07315724.2005.10719454
    1. 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. (2010) 7:51. 10.1186/1743-7075-7-51
    1. Ahtiainen JP, Hoffren M, Hulmi JJ, Pietikäinen M, Mero AA, Avela J, et al. . Panoramic ultrasonography is a valid method to measure changes in skeletal muscle cross-sectional area. Eur J Appl Physiol. (2010) 108:273–9. 10.1007/s00421-009-1211-6
    1. Ishida Y, Carroll JF, Pollock ML, Graves JE, Leggett SH. Reliability of B-mode ultrasound for the measurement of body fat and muscle thickness. Am J Hum Biol. (1992) 4:511–20. 10.1002/ajhb.1310040410
    1. Reeves ND, Maganaris CN, Narici MV. Ultrasonographic assessment of human skeletal muscle size. Eur J Appl Physiol. (2004) 91:116–8. 10.1007/s00421-003-0961-9
    1. Phillips SM, Tipton KD, Aarsland A, Wolf SE, Wolfe RR. Mixed muscle protein synthesis and breakdown after resistance exercise in humans. Am J Physiol Metab. (1997) 273:99–107. 10.1152/ajpendo.1997.273.1.E99
    1. Hulmi JJ, Tannerstedt J, Selänne H, Kainulainen H, Kovanen V, Mero AA. Resistance exercise with whey protein ingestion affects mTOR signaling pathway and myostatin in men. J Appl Physiol. (2009) 106:1720–9. 10.1152/japplphysiol.00087.2009
    1. Tsuchiya A, Almiron-Roig E, Lluch A, Guyonnet D, Drewnowski A. Higher satiety ratings following yogurt consumption relative to fruit drink or dairy fruit drink. J Am Diet Assoc. (2006) 106:550–7. 10.1016/j.jada.2006.01.004
    1. Tremblay A, Doyon C, Sanchez M. Impact of yogurt on appetite control, energy balance, and body composition. Nutr Rev. (2015) 73:23–7. 10.1093/nutrit/nuv015
    1. Douglas SM, Ortinau LC, Hoertel HA, Leidy HJ. Low, moderate, or high protein yogurt snacks on appetite control and subsequent eating in healthy women. Appetite. (2013) 60:117–22. 10.1016/j.appet.2012.09.012
    1. Zemel MB, Thompson W, Milstead A, Morris K, Campbell P. Calcium and dairy acceleration of weight and fat loss during energy restriction in obese adults. Obes Res. (2004) 12:582–90. 10.1038/oby.2004.67
    1. Moore DR, Churchward-Venne TA, Witard O, Breen L, Burd NA, Tipton KD, et al. . Protein ingestion to stimulate myofibrillar protein synthesis requires greater relative protein intakes in healthy older versus younger men. J Gerontol A Biol Sci Med Sci. (2015) 70:57–62. 10.1093/gerona/glu103
    1. Roberts MD, Haun CT, Mobley CB, Mumford PW, Romero MA, Roberson PA, et al. . Physiological differences between low versus high skeletal muscle hypertrophic responders to resistance exercise training: current perspectives and future research directions. Front Physiol. (2018) 9:834. 10.3389/fphys.2018.00834
    1. Trommelen J, Loon L. Pre-sleep protein ingestion to improve the skeletal muscle adaptive response to exercise training. Nutrients. (2016) 8:763. 10.3390/nu8120763
    1. Trommelen J, Holwerda AM, Kouw IWK, Langer H, Halson SL, Rollo I, et al. . Resistance exercise augments postprandial overnight muscle protein synthesis rates. Med Sci Sports Exerc. (2016) 48:2517–25. 10.1249/MSS.0000000000001045
    1. Res PT, Groen B, Pennings B, Beelen M, Wallis GA, Gijsen AP, et al. . Protein ingestion before sleep improves postexercise overnight recovery. Med Sci Sports Exerc. (2012) 44:1560–9. 10.1249/MSS.0b013e31824cc363
    1. Bong DD, Moraru CI. Use of micellar casein concentrate for Greek-style yogurt manufacturing: effects on processing and product properties. J Dairy Sci. (2014) 97:1259–69. 10.3168/jds.2013-7488
    1. Liljeberg H, Björck I. Delayed gastric emptying rate may explain improved glycaemia in healthy subjects to a starchy meal with added vinegar. Eur J Clin Nutr. (1998) 52:368–71. 10.1038/sj.ejcn.1600572
    1. Churchward-Venne TA, Snijders T, Linkens AM, Hamer HM, van Kranenburg J, van Loon LJ. Ingestion of casein in a milk matrix modulates dietary protein digestion and absorption kinetics but does not modulate postprandial muscle protein synthesis in older men. J Nutr. (2015) 145:1438–45. 10.3945/jn.115.213710
    1. Soop M, Nehra V, Henderson GC, Boirie Y, Ford GC, Nair KS. Coingestion of whey protein and casein in a mixed meal: demonstration of a more sustained anabolic effect of casein. AJP Endocrinol Metab. (2012) 1:152–62. 10.1152/ajpendo.00106.2012
    1. Tate DF, Turner-McGrievy G, Lyons E, Stevens J, Erickson K, Polzien K, et al. . Replacing caloric beverages with water or diet beverages for weight loss in adults: main results of the choose healthy options consciously everyday (CHOICE) randomized clinical trial. Am J Clin Nutr. (2012) 95:555–63. 10.3945/ajcn.111.026278
    1. Weaver CM, Miller JW. Challenges in conducting clinical nutrition research. Nutr Rev. (2017) 75:491–9. 10.1093/nutrit/nux026
    1. Staudacher HM, Irving PM, Lomer MCE, Whelan K. The challenges of control groups, placebos and blinding in clinical trials of dietary interventions. Proc Nutr Soc. (2017) 76:628 10.1017/S0029665117002816
    1. Hébert JR, Frongillo EA, Adams SA, Turner-McGrievy GM, Hurley TG, Miller DR, et al. Perspective: Randomized controlled trials are not a panacea for diet-related research. Adv Nutr. (2016) 7:423–32. 10.3945/an.115.011023
    1. Thibault R, Pichard C. The evaluation of body composition: a useful tool for clinical practice. Ann Nutr Metab. (2012) 60:6–16. 10.1159/000334879
    1. Hangartner TN, Warner S, Braillon P, Jankowski L, Shepherd J. The official positions of the international society for clinical densitometry: acquisition of dual-energy x-ray absorptiometry body composition and considerations regarding analysis and repeatability of measures. J Clin Densitom. (2013) 16:520–36. 10.1016/j.jocd.2013.08.007
    1. Salamat MR, Shanei A, Khoshhali M, Salamat AH, Siavash M, Asgari M. Use of conventional regional DXA scans for estimating whole body composition. Arch Iran Med. (2014) 17:674–8.
    1. Lowry DW, Tomiyama AJ. Air displacement plethysmography versus dual-energy X-ray absorptiometry in underweight, normal-weight, and overweight/obese individuals. PLoS ONE. (2015) 10:e0115086. 10.1371/journal.pone.0115086
    1. Fields DA, Goran MI, McCrory MA. Body-composition assessment via air-displacement plethysmography in adults and children: a review. Am J Clin Nutr. (2002) 75:453–67. 10.1093/ajcn/75.3.453
    1. Morelli L. Yogurt, living cultures, and gut health. Am J Clin Nutr. (2014) 99: 1248S−50S. 10.3945/ajcn.113.073072
    1. Adolfsson O, Meydani SN, Russell RM. Yogurt and gut function. Am J Clin Nutr. (2004) 80:245–56. 10.1093/ajcn/80.2.245
    1. Pei R, Martin DA, DiMarco DM, Bolling BW. Evidence for the effects of yogurt on gut health and obesity. Crit Rev Food Sci Nutr. (2017) 57:1569–83. 10.1080/10408398.2014.883356
    1. Rizzoli R. Dairy products, yogurts, and bone health. Am J Clin Nutr. (2014) 99: 1256S−2S. 10.3945/ajcn.113.073056
    1. Rizzoli R, Biver E. Effects of fermented milk products on bone. Calcif Tissue Int. (2018) 102:489–500. 10.1007/s00223-017-0317-9
    1. Sahni S, Tucker KL, Kiel DP, Quach L, Casey VA, Hannan MT. Milk and yogurt consumption are linked with higher bone mineral density but not with hip fracture: the framingham offspring study. Arch Osteoporos. (2013) 8:119 10.1007/s11657-013-0119-2

Source: PubMed

3
Abonner