Effect of dairy proteins on appetite, energy expenditure, body weight, and composition: A review of the evidence from controlled clinical trials

Advances in Nutrition

Volumn 4, Issue 4, 2013, Pages 418-438

  Bendtsen, Line Q ^a   Lorenzen, Janne K ^a   Bendsen, Nathalie T ^a   Rasmussen, Charlotte ^b   Astrup, Arne ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN; GASTROINTESTINAL HORMONE; MILK PROTEIN; WHEY PROTEIN;

ABSORPTION; ANIMAL; APPETITE; BODY COMPOSITION; BODY WEIGHT; COMPARATIVE STUDY; CONTROLLED CLINICAL TRIAL (TOPIC); DAIRY PRODUCT; DIET; DIGESTION; DRUG EFFECTS; ENERGY METABOLISM; HUMAN; HUNGER; MEDLINE; SATIETY; SECRETION (PROCESS); TIME;

ABSORPTION; ANIMALS; APPETITE; BODY COMPOSITION; BODY WEIGHT; CASEINS; CONTROLLED CLINICAL TRIALS AS TOPIC; DAIRY PRODUCTS; DIET; DIGESTION; ENERGY METABOLISM; GASTROINTESTINAL HORMONES; HUMANS; HUNGER; MEDLINE; MILK PROTEINS; SATIATION; TIME FACTORS; WHEY PROTEINS;

EID: 84888389967     PISSN: 21618313     EISSN: 21565376     Source Type: Journal    
DOI: 10.3945/an.113.003723     Document Type: Review

References (88)

1. Larsen TM, Dalskov SM, van Baak M, Jebb SA, Papadaki A, Pfeiffer AF, Martinez JA, Handjieva-Darlenska T, Kunšová M, Pihlsgård M, et al.; Diet, Obesity, and Genes (DIOgenes) Project. Diets with high or low protein content and glycemic index for weight-loss maintenance. N Engl J Med. 2010;363:2102-13.
2. Skov AR, Toubro S, Ronn B, Holm L, Astrup A. Randomized trial on protein vs carbohydrate in ad libitum fat reduced diet for the treatment of obesity. Int J Obes Relat Metab Disord. 1999;23:528-36.
3. Weigle DS, Breen PA, Matthys CC, Callahan HS, Meeuws KE, Burden VR, Purnell JQ. A high-protein diet induces sustained reductions in appetite, ad libitum caloric intake, and body weight despite compensatory changes in diurnal plasma leptin and ghrelin concentrations. Am J Clin Nutr. 2005;82:41-8.
4. Mikkelsen PB, Toubro S, Astrup A. Effect of fat-reduced diets on 24-h energy expenditure: comparisons between animal protein, vegetable protein, and carbohydrate. Am J Clin Nutr. 2000;72:1135-41.
5. Astrup A. The satiating power of protein-a key to obesity prevention? Am J Clin Nutr. 2005;82:1-2.
6. Gilbert JA, Bendsen NT, Tremblay A, Astrup A. Effect of proteins from different sources on body composition. Nutr Metab Cardiovasc Dis. 2011;21: Suppl 2:B16-31.
7. Hall WL, Millward DJ, Long SJ, Morgan LM. Casein and whey exert different effects on plasma amino acid profiles, gastrointestinal hormone secretion and appetite. Br J Nutr. 2003;89:239-48.
8. Pal S, Ellis V. The acute effects of four protein meals on insulin, glucose, appetite and energy intake in lean men. Br J Nutr. 2010;104:1241-8.
9. Acheson KJ, Blondel-Lubrano A, Oguey-Araymon S, Beaumont M, Emady-Azar S, Ammon-Zufferey C, Monnard I, Pinaud S, Nielsen-Moennoz C, Bovetto L. Protein choices targeting thermogenesis and metabolism. Am J Clin Nutr. 2011;93:525-34.
10. 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.
11. Faghih S, Abadi AR, Hedayati M, Kimiagar SM. Comparison of the effects of cows' milk, fortified soy milk, and calcium supplement on weight and fat loss in premenopausal overweight and obese women. Nutr Metab Cardiovasc Dis. 2011;21:499-503.
12. Abargouei AS, Janghorbani M, Salehi-Marzijarani M, Esmaillzadeh A. Effect of dairy consumption on weight and body composition in adults: a systematic review and meta-analysis of randomized controlled clinical trials. Int J Obes (Lond) 2012;36:1485-93.
13. Chen M, Pan A, Malik VS, Hu FB. Effects of dairy intake on body weight and fat: a meta-analysis of randomized controlled trials. Am J Clin Nutr. 2012;96:735-47.
14. Anderson GH, Luhovyy B, Akhavan T, Panahi S. Milk proteins in the regulation of body weight, satiety, food intake and glycemia. Nestle Nutr Workshop Ser Pediatr Program. 2011;67:147-59.
15. Farrell HM, Jr., Jimenez-Flores R, Bleck GT, Brown EM, Butler JE, Creamer LK, Hicks CL, Hollar CM, Ng-Kwai-Hang KF, Swaisgood HE. Nomenclature of the proteins of cows' milk-sixth revision. J Dairy Sci. 2004;87:1641-74.
16. Luhovyy BL, Akhavan T, Anderson GH. Whey proteins in the regulation of food intake and satiety. J Am Coll Nutr. 2007;26:704S-12S.
17. 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 U S A. 1997;94:14930-5.
18. Veldhorst MA, Nieuwenhuizen AG, Hochstenbach-Waelen A, van Vught AJ, Westerterp KR, Engelen MP, Brummer RJ, Deutz NE, Westerterp-Plantenga MS. Dose-dependent satiating effect of whey relative to casein or soy. Physiol Behav. 2009;96:675-82.
19. Demling RH, DeSanti L. Effect of a hypocaloric diet, increased protein intake and resistance training on lean mass gains and fat mass loss in overweight police officers. Ann Nutr Metab. 2000;44:21-9.
20. Rolls BJ, Hetherington M, Burley VJ. The specificity of satiety: the influence of foods of different macronutrient content on the development of satiety. Physiol Behav. 1988;43:145-53.
21. Johnstone AM, Horgan GW, Murison SD, Bremner DM, Lobley GE. Effects of a high-protein ketogenic diet on hunger, appetite, and weight loss in obese men feeding ad libitum. Am J Clin Nutr. 2008;87:44-55.
22. Astrup A, Meinert LT, Harper A. Atkins and other low-carbohydrate diets: hoax or an effective tool for weight loss? Lancet. 2004;364:897-9.
23. Vandewater K, Vickers Z. Higher-protein foods produce greater sensory-specific satiety. Physiol Behav. 1996;59:579-83.
24. Dove ER, Hodgson JM, Puddey IB, Beilin LJ, Lee YP, Mori TA. Skim milk compared with a fruit drink acutely reduces appetite and energy intake in overweight men and women. Am J Clin Nutr. 2009;90:70-5.
25. Astbury NM, Stevenson EJ, Morris P, Taylor MA, Macdonald IA. Doseresponse effect of a whey protein preload on within-day energy intake in lean subjects. Br J Nutr 2010;104:1858-67.
26. Veldhorst MA, Nieuwenhuizen AG, Hochstenbach-Waelen A,Westerterp KR, Engelen MP, Brummer RJ, Deutz NE, Westerterp-Plantenga MS. Comparison of the effects of a high- and normal-casein breakfast on satiety, 'satiety' hormones, plasma amino acids and subsequent energy intake. Br J Nutr. 2009;101:295-303.
27. Hochstenbach-Waelen A, Veldhorst MA, Nieuwenhuizen AG, Westerterp-Plantenga MS, Westerterp KR. Comparison of 2 diets with either 25% or 10% of energy as casein on energy expenditure, substrate balance, and appetite profile. Am J Clin Nutr. 2009;89:831-8.
28. Sousa GT, Lira FS, Rosa JC, de Oliveira EP, Oyama LM, Santos RV, Pimentel GD. Dietary whey protein lessens several risk factors for metabolic diseases: a review. Lipids Health Dis. 2012;11:67.
29. Børsheim E, Tipton KD, Wolf SE, Wolfe RR. Essential amino acids and muscle protein recovery from resistance exercise. Am J Physiol Endocrinol Metab. 2002;283:E648-57.
30. Burton-Freeman BM. Glycomacropeptide (GMP) is not critical to whey-induced satiety, but may have a unique role in energy intake regulation through cholecystokinin (CCK). Physiol Behav. 2008;93:379-87.
31. Veldhorst MA, Nieuwenhuizen AG, Hochstenbach-Waelen A, Westerterp KR, Engelen MP, Brummer RJ, Deutz NE, Westerterp-Plantenga MS. Effects of complete whey-protein breakfasts versus whey without GMP-breakfasts on energy intake and satiety. Appetite. 2009;52:388-95.
32. Keogh JB, Woonton BW, Taylor CM, Janakievski F, Desilva K, Clifton PM. Effect of glycomacropeptide fractions on cholecystokinin and food intake. Br J Nutr. 2010;104:286-90.
33. Lam SM, Moughan PJ, Awati A, Morton HR. The influence of whey protein and glycomacropeptide on satiety in adult humans. Physiol Behav. 2009;96:162-8.
34. Veldhorst MA, Nieuwenhuizen AG, Hochstenbach-Waelen A,Westerterp KR, Engelen MP, Brummer RJ, Deutz NE, Westerterp-Plantenga MS. A breakfast with alpha-lactalbumin, gelatin, or gelatin + TRP lowers energy intake at lunch compared with a breakfast with casein, soy, whey, or whey-GMP. Clin Nutr. 2009;28:147-55.
35. Chatterton D, Smithers G, Roupas P, Brodkorb A. Bioactivity of blactoglobulin and a-lactalbumin-Technological implications for processing. Int Dairy J. 2006;16:1229-40.
36. Hursel R, van der Zee L, Westerterp-Plantenga MS. Effects of a breakfast yoghurt, with additional total whey protein or caseinomacropeptide-depleted alpha-lactalbumin-enriched whey protein, on dietinduced thermogenesis and appetite suppression. Br J Nutr. 2010;103:775-80.
37. Heine WE, Klein PD, Reeds PJ. The importance of alpha-lactalbumin in infant nutrition. J Nutr. 1991;121:277-83.
38. Anderson GH, Tecimer SN, Shah D, Zafar TA. Protein source, quantity, and time of consumption determine the effect of proteins on shortterm food intake in young men. J Nutr. 2004;134:3011-5.
39. Wilson J, Wilson GJ. Contemporary issues in protein requirements and consumption for resistance trained athletes. J Int Soc Sports Nutr. 2006;3:7-27.
40. Bowen J, Noakes M, Trenerry C, Clifton PM. Energy intake, ghrelin, and cholecystokinin after different carbohydrate and protein preloads in overweight men. J Clin Endocrinol Metab. 2006;91:1477-83.
41. Bowen J, Noakes M, Clifton PM. Appetite regulatory hormone responses to various dietary proteins differ by body mass index status despite similar reductions in ad libitum energy intake. J Clin Endocrinol Metab. 2006;91:2913-9.
42. Alfenas RCG, Bressan J, Paiva AC. Effects of protein quality on appetite and energy metabolism in normal weight subjects. Arq Bras Endocrinol Metabol. 2010;54:45-51.
43. Baer DJ, Stote KS, Paul DR, Harris GK, Rumpler WV, Clevidence BA. Whey protein but not soy protein supplementation alters body weight and composition in free-living overweight and obese adults. J Nutr. 2011;141:1489-94.
44. Lang V, Bellisle F, Oppert JM, Craplet C, Bornet FR, Slama G, Guy-Grand B. Satiating effect of proteins in healthy subjects: a comparison of egg albumin, casein, gelatin, soy protein, pea protein, and wheat gluten. Am J Clin Nutr. 1998;67:1197-204.
45. Lang V, Bellisle F, Alamowitch C, Craplet C, Bornet FR, Slama G, Guy-Grand B. Varying the protein source in mixed meal modifies glucose, insulin and glucagon kinetics in healthy men, has weak effects on subjective satiety and fails to affect food intake. Eur J Clin Nutr. 1999;53:959-65.
46. Lorenzen J, Frederiksen R, Hoppe C, Hvid R, Astrup A. The effect of milk proteins on appetite regulation and diet-induced thermogenesis. Eur J Clin Nutr. 2012;66:622-7.
47. Potier M, Fromentin G, Calvez J, Benamouzig R, Martin-Rouas C, Pichon L, Tome D, Marsset-Baglieri A. A high-protein, moderate-energy, regular cheesy snack is energetically compensated in human subjects. Br J Nutr. 2009;102:625-31.
48. Hochstenbach-Waelen A, Westerterp-Plantenga MS, Veldhorst MA, Westerterp KR. Single-protein casein and gelatin diets affect energy expenditure similarly but substrate balance and appetite differently in adults. J Nutr. 2009;139:2285-92.
49. Gietzen DW, Ross CM, Hao S, Sharp JW. Phosphorylation of eIF2alpha is involved in the signaling of indispensable amino acid deficiency in the anterior piriform cortex of the brain in rats. J Nutr. 2004;134:717-23.
50. Maurin AC, Jousse C, Averous J, Parry L, Bruhat A, Cherasse Y, Zeng H, Zhang Y, Harding HP, Ron D et al. The GCN2 kinase biases feeding behavior to maintain amino acid homeostasis in omnivores. Cell Metab. 2005;1:273-7.
51. Hochstenbach-Waelen A, Soenen S, Westerterp KR, Westerterp-Plantenga MS. Effects of a supra-sustained gelatin-milk protein diet compared with (supra-)sustained milk protein diets on body-weight loss. Br J Nutr. 2011;105:1388-98.
52. Hochstenbach-Waelen A, Westerterp KR, Soenen S, Westerterp-Plantenga MS. No long-term weight maintenance effects of gelatin in a supra-sustained protein diet. Physiol Behav. 2010;101:237-44.
53. Nieuwenhuizen AG, Hochstenbach-Waelen A, Veldhorst MA, Westerterp KR, Engelen MP, Brummer RJ, Deutz NE, Westerterp-Plantenga MS. Acute effects of breakfasts containing alpha-lactalbumin, or gelatin with or without added tryptophan, on hunger, 'satiety' hormones and amino acid profiles. Br J Nutr. 2009;101:1859-66.
54. Juvonen KR, Karhunen LJ, Vuori E, Lille ME, Karhu T, Jurado-Acosta A, Laaksonen DE, Mykkanen HM, Niskanen LK, Poutanen KS, et al. Structure modification of a milk protein-based model food affects postprandial intestinal peptide release and fullness in healthy young men. Br J Nutr. 2011;106:1890-8.
55. Dangin M, Boirie Y, Garcia-Rodenas C, Gachon P, Fauquant J, Callier P, Ballevre O. Beaufrere. The digestion rate of protein is an independent regulating factor of postprandial protein retention. Am J Physiol Endocrinol Metab. 2001;280:E340-8.
56. Dangin M, Guillet C, Garcia-Rodenas C, Gachon P, Bouteloup-Demange C, Reiffers-Magnani K, Fauquant J, Bellèvre O. Beaufrère B. The rate of protein digestion affects protein gain differently during aging in humans. J Physiol. 2003;549:635-44.
57. Koopman R, Crombach N, Gijsen AP, Walrand S, Fauquant J, Kies AK, Lemosquet S, Saris WH, Boirie Y, van Loon LJ. Ingestion of a protein hydrolysate is accompanied by an accelerated in vivo digestion and absorption rate when compared with its intact protein. Am J Clin Nutr. 2009;90:106-15.
58. Calbet JA, Holst JJ. Gastric emptying, gastric secretion and enterogastrone response after administration of milk proteins or their peptide hydrolysates in humans. Eur J Nutr. 2004;43:127-39.
59. Morifuji M, Ishizaka M, Baba S, Fukuda K, Matsumoto H, Koga J, Kanegae M, Higuchi M. Comparison of different sources and degrees of hydrolysis of dietary protein: effect on plasma amino acids, dipeptides, and insulin responses in human subjects. J Agric Food Chem. 2010;58:8788-97.
60. Akhavan T, Luhovyy BL, Brown PH, Cho CE, Anderson GH. Effect of premeal consumption of whey protein and its hydrolysate on food intake and postmeal glycemia and insulin responses in young adults. Am J Clin Nutr. 2010;91:966-75.
61. Mahé S, Roos N, Benamouzig R, Davin L, Luengo C, Gagnon L, Gausserges N, Rautureau J, Tome D. Gastrojejunal kinetics and the digestion of [15N] beta-lactoglobulin and casein in humans: the influence of the nature and quantity of the protein. Am J Clin Nutr. 1996;63:546-52.
62. Sam AH, Troke RC, Tan TM, Bewick GA. The role of the gut/brain axis in modulating food intake. Neuropharmacology. 2012;63:46-56.
63. Nilsson M, Stenberg M, Frid AH, Holst JJ, Bjorck IM. Glycemia and insulinemia in healthy subjects after lactoseequivalent meals of milk and other food proteins: the role of plasma amino acids and incretins. Am J Clin Nutr. 2004;80:1246-53.
64. Nilsson M, Holst JJ, Bjorck IME. Metabolic effects of amino acid mixtures and whey protein in healthy subjects: studies using glucose-equivalent drinks. Am J Clin Nutr. 2007;85:996-1004.
65. Holmer-Jensen J, Hartvigsen ML, Mortensen LS, Astrup A, de Vrese M, Holst JJ, Thomsen C, Hermansen K. Acute differential effects of milkderived dietary proteins on postprandial lipaemia in obese non-diabetic subjects. Eur J Clin Nutr. 2012;66:32-8.
66. Mortensen K, Christensen LL, Holst JJ, Orskov C. GLP-1 and GIP are colocalized in a subset of endocrine cells in the small intestine. Regul Pept. 2003;114:189-96.
67. Diepvens K, Häberer D, Westerterp-Plantenga M. Different proteins and biopeptides differently affect satiety and anorexigenic/orexigenic hormones in healthy humans. Int J Obes (Lond). 2008;32:510-8.
68. Halton TL, Hu FB. The effects of high protein diets on thermogenesis, satiety and weight loss: a critical review. J Am Coll Nutr. 2004;23:373-85.
69. Westerterp KR, Wilson SA, Rolland V. Diet induced thermogenesis measured over 24h in a respiration chamber: effect of diet composition. International journal of obesity and related metabolic disorders. Int J Obes Relat Metab Disord. 1999;23:287-292.
70. Robinson SM, Jaccard C, Persaud C, Jackson AA, Jequier E, Schutz Y. Protein turnover and thermogenesis in response to high-protein and high-carbohydrate feeding in men. Am J Clin Nutr. 1990;52:72-80.
71. Karst H, Steiniger J, Noack R, Steglich HD. Diet-induced thermogenesis in man: thermic effects of single proteins, carbohydrates and fats depending on their energy amount. Ann Nutr Metab. 1984;28:245-52.
72. Fouillet H, Juillet B, Gaudichon C, Mariotti F, Tome D, Bos C. Absorption kinetics are a key factor regulating postprandial protein metabolism in response to qualitative and quantitative variations in protein intake. Am J Physiol Regul Integr Comp Physiol. 2009;297:R1691-705.
73. Krieger JW, Sitren HS, Daniels MJ, Langkamp-Henken B. Effects of variation in protein and carbohydrate intake on body mass and composition during energy restriction: a meta-regression 1. Am J Clin Nutr. 2006;83:260-74.
74. Cribb PJ, Williams AD, Carey MF, Hayes A. The effect of whey isolate and resistance training on strength, body composition, and plasma glutamine. Int J Sport Nutr Exerc Metab. 2006;16:494-509.
75. Colker CM, Swain MA, Fabrucini B, Shi Q, Kaiman DS. Effects of supplemental protein on body composition and muscular strength in healthy athletic male adults. Curr Ther Res 2000;61:19-28.
76. Kerksick CM, Rasmussen CJ, Lancaster SL, Magu B, Smith P, Melton C, Greenwood M, Almada AL, Earnest CP, Kreider RB. The effects of protein and amino acid supplementation on performance and training adaptations during ten weeks of resistance training. J Strength Cond Res. 2006;20:643-53.
77. Tang JE, Moore DR, Kujbida GW, Tarnopolsky MA, Phillips SM. Ingestion of whey hydrolysate, casein, or soy protein isolate: effects on mixed muscle protein synthesis at rest and following resistance exercise in young men. J Appl Physiol. 2009;107:987-992.
78. Lollo PCB, Amaya-Farfan J, de Carvalho-Silva LB. Physiological and physical effects of different milk protein supplements in elite soccer players. J Hum Kinet. 2011;30:49-57.
79. Frestedt JL, Zenk JL, Kuskowski MA, Ward LS, Bastian ED. A wheyprotein supplement increases fat loss and spares lean muscle in obese subjects: a randomized human clinical study. Nutr Metab (Lond). 2008;5:8.
80. Anderson JW, Hoie LH. Weight loss and lipid changes with low-energy diets: comparator study of milk-based versus soy-based liquid meal replacement interventions. J Am Coll Nutr. 2005;24:210-6.
81. Anderson JW, Fuller J, Patterson K, Blair R, Tabor A. Soy compared to casein meal replacement shakes with energy-restricted diets for obese women: randomized controlled trial. Metabolism. 2007;56:280-8.
82. Soenen S, Hochstenbach-Waelen A, Westerterp-Plantenga MS. Efficacy of alpha-lactalbumin and milk protein on weight loss and body composition during energy restriction. Obesity (Silver Spring). 2011;19:370-9.
83. Pilvi TK, Harala S, Korpela R, Mervaala EM. Effects of high-calcium diets with different whey proteins on weight loss and weight regain in high-fat-fed C57BL/6J mice. Br J Nutr. 2009;102:337-41.
84. Keogh JB, Clifton P. The effect of meal replacements high in glycomacropeptide on weight loss and markers of cardiovascular disease risk. Am J Clin Nutr. 2008;87:1602-5.
85. Royle PJ, McIntosh GH, Clifton PM. Whey protein isolate and glycomacropeptide decrease weight gain and alter body composition in male Wistar rats. Br J Nutr. 2008;100:88-93.
86. Claessens M, van Baak MA, Monsheimer S, Saris WH. The effect of a low-fat, high-protein or high-carbohydrate ad libitum diet on weight loss maintenance and metabolic risk factors. Int J Obes (Lond). 2009;33:296-304.
87. Takahira M, Noda K, Fukushima M, Zhang B, Mitsutake R, Uehara Y, Ogawa M, Kakuma T, Saku K. Randomized, double-blind, controlled, comparative trial of formula food containing soy protein vs. milk protein in visceral fat obesity. -FLAVO study-. Circ J. 2011;75:2235-43.
88. Hermansen K, Hansen B, Jacobsen R, Clausen P, Dalgaard M, Dinesen B, Holst JJ, Pedersen E, Astrup A. Effects of soy supplementation on blood lipids and arterial function in hypercholesterolaemic subjects. Eur J Clin Nutr. 2005;59:843-50.