Milk protein for improved metabolic health: a review of the evidence

Nutrition & Metabolism

Sally D Poppitt²  Robin A McGregor¹ 

[1] University of Auckland Human Nutrition Unit, 18 Carrick Place, Mt Eden, Auckland 1024, New Zealand;Riddet Institute, Palmerston North 4442, New Zealand

关键词: Body weight;    Inflammation;    Blood pressure;    Dyslipidaemia;    Hyperglycaemia;    Metabolic health;    Whey protein;    Milk;    Dairy protein;   

Others  :  803346
DOI  :  10.1186/1743-7075-10-46

 received in 2013-03-25, accepted in 2013-06-23,  发布年份 2013

【 摘 要 】

Epidemiological evidence shows that consumption of dairy products is associated with decreased prevalence of metabolic related disorders, whilst evidence from experimental studies points towards dairy protein as a dietary component which may aid prevention of type 2 diabetes (T2DM). Poor metabolic health is a common characteristic of overweight, obesity and aging, and is the forerunner of T2DM and cardiovascular disease (CVD), and an ever increasing global health issue. Progressive loss of metabolic control is evident from a blunting of carbohydrate, fat and protein metabolism, which is commonly manifested through decreased insulin sensitivity, inadequate glucose and lipid control, accompanied by a pro-inflammatory environment and hypertension. Adverse physiological changes such as excess visceral adipose tissue deposition and expansion, lipid overspill and infiltration into liver, muscle and other organs, and sarcopaenia or degenerative loss of skeletal muscle mass and function all underpin this adverse profile. ‘Sarcobesity’ and sarcopaenic diabetes are rapidly growing health issues. As well as through direct mechanisms, dairy protein may indirectly improve metabolic health by aiding loss of body weight and fat mass through enhanced satiety, whilst promoting skeletal muscle growth and function through anabolic effects of dairy protein-derived branch chain amino acids (BCAAs). BCAAs enhance muscle protein synthesis, lean body mass and skeletal muscle metabolic function. The composition and processing of dairy protein has an impact on digestion, absorption, BCAA kinetics and function, hence the optimisation of dairy protein composition through selection and combination of specific protein components in milk may provide a way to maximize benefits for metabolic health.

【 授权许可】

   
2013 McGregor and Poppitt; licensee BioMed Central Ltd.

【 参考文献 】

• [1]Gu D, Reynolds K, Wu X, Chen J, Duan X, Reynolds RF, et al.: Prevalence of the metabolic syndrome and overweight among adults in China. Lancet 2005, 365(9468):1398-1405.
• [2]Ford ES, Li C, Zhao G: Prevalence and correlates of metabolic syndrome based on a harmonious definition among adults in the US. J Diabetes 2010, 2(3):180-193.
• [3]Alberti KGMM, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, et al.: Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 2009, 120(16):1640-1645.
• [4]Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, et al.: Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation 2005, 112(17):2735-2752.
• [5]Eckel RH, Grundy SM, Zimmet PZ: The metabolic syndrome. Lancet 2005, 365(9468):1415-1428.
• [6]Parr EB, Coffey VG, Hawley JA: “Sarcobesity”: a metabolic conundrum. Maturitas 2013, 74:109-113.
• [7]Kwon E-Y, Shin S-K, Cho Y-Y, Jung UJ, Kim E, Park T, et al.: Time-course microarrays reveal early activation of the immune transcriptome and adipokine dysregulation leads to fibrosis in visceral adipose depots during diet-induced obesity. BMC Genomics 2012, 13(1):450.
• [8]Cornier M-A, Dabelea D, Hernandez TL, Lindstrom RC, Steig AJ, Stob NR, et al.: The metabolic syndrome. Endocr Rev 2008, 29(7):777-822.
• [9]Nazare J-A, Smith JD, Borel A-L, Haffner SM, Balkau B, Ross R, et al.: Ethnic influences on the relations between abdominal subcutaneous and visceral adiposity, liver fat, and cardiometabolic risk profile: the International study of prediction of intra-abdominal adiposity and its relationship with cardiometabolic risk/intra-abdominal adiposity. Am J Clin Nutr 2012, 96(4):714-726.
• [10]Hotamisligil GS: Inflammation and metabolic disorders. Nature 2006, 444(7121):860-867.
• [11]Nicklas BJ, Wang X, You T, Lyles MF, Demons J, Easter L, et al.: Effect of exercise intensity on abdominal fat loss during calorie restriction in overweight and obese postmenopausal women: a randomized, controlled trial. Am J Clin Nutr 2009, 89(4):1043-1052.
• [12]Campbell WW, Haub MD, Wolfe RR, Ferrando AA, Sullivan DH, Apolzan JW, et al.: Resistance training preserves fat-free mass without impacting changes in protein metabolism after weight loss in older women. Obesity (Silver Spring) 2009, 17(7):1332-1339.
• [13]Foster-Schubert KE, Alfano CM, Duggan CR, Xiao L, Campbell KL, Kong A, et al.: Effect of diet and exercise, alone or combined, on weight and body composition in overweight-to-obese postmenopausal women. Obesity (Silver Spring) 2012, 20(8):1628-1638.
• [14]Kelley DE, Goodpaster B, Wing RR, Simoneau JA: Skeletal muscle fatty acid metabolism in association with insulin resistance, obesity, and weight loss. Am J Physiol 1999, 277(6 Pt 1):E1130-E1141.
• [15]Chung J-Y, Kang H-T, Lee D-C, Lee H-R, Lee Y-J: Body composition and its association with cardiometabolic risk factors in the elderly: a focus on sarcopenic obesity. Arch Gerontol Geriatr 2013, 56(1):270-278.
• [16]Malenfant P, Tremblay A, Doucet E, Imbeault P, Simoneau JA, Joanisse DR: Elevated intramyocellular lipid concentration in obese subjects is not reduced after diet and exercise training. Am J Physiol Endocrinol Metab 2001, 280(4):E632-E639.
• [17]Chevalier S, Marliss EB, Morais JA, Lamarche M, Gougeon R: Whole-body protein anabolic response is resistant to the action of insulin in obese women. Am J Clin Nutr 2005, 82(2):355-365.
• [18]Rennie MJ: Anabolic resistance: the effects of aging, sexual dimorphism, and immobilization on human muscle protein turnover. Appl Physiol Nutr Metab 2009, 34(3):377-381.
• [19]Pal S, Radavelli-Bagatini S: The effects of whey protein on cardiometabolic risk factors. Obes Rev 2012.
• [20]Rice BH, Cifelli CJ, Pikosky MA, Miller GD: Dairy components and risk factors for cardiometabolic syndrome: recent evidence and opportunities for future research. Adv Nutr 2011, 2(5):396-407.
• [21]Sousa GTD, Lira FS, Rosa JC, De Oliveira EP, Oyama LM, Santos RV, et al.: Dietary whey protein lessens several risk factors for metabolic diseases: a review. Lipids Health Dis 2012, 11:67.
• [22]Jakubowicz D, Froy O: Biochemical and metabolic mechanisms by which dietary whey protein may combat obesity and Type 2 diabetes. J Nutr Biochem 2013, 24(1):1-5.
• [23]Graf S, Egert S, Heer M: Effects of whey protein supplements on metabolism: evidence from human intervention studies. Curr Opin Clin Nutr Metab Care 2011, 14(6):569-580.
• [24]Crichton GE, Bryan J, Buckley J, Murphy KJ: Dairy consumption and metabolic syndrome: a systematic review of findings and methodological issues. Obes Rev 2011, 12(5):e190-e201.
• [25]Ricci-Cabello I, Herrera MO, Artacho R: Possible role of milk-derived bioactive peptides in the treatment and prevention of metabolic syndrome. Nutr Rev 2012, 70(4):241-255.
• [26]Esteves De Oliveira FC, Pinheiro Volp AC, Alfenas RC: Impact of different protein sources in the glycemic and insulinemic responses. Nutr Hosp 2011, 26(4):669-676.
• [27]Westerterp-Plantenga MS, Nieuwenhuizen A, Tomé D, Soenen S, Westerterp KR: Dietary protein, weight loss, and weight maintenance. Annu Rev Nutr 2009, 29(1):21-41.
• [28]Saito T: Antihypertensive peptides derived from bovine casein and whey proteins. Adv Exp Med Biol 2008, 606:295-317.
• [29]Cross ML, Gill HS: Immunomodulatory properties of milk. Br J Nutr 2000, 84(S1):81-89.
• [30]Fumeron F, Lamri A, Abi Khalil C, Jaziri R, Porchay-Baldérelli I, Lantieri O, et al.: Dairy consumption and the incidence of hyperglycemia and the metabolic syndrome: results from a french prospective study, Data from the Epidemiological Study on the Insulin Resistance Syndrome (DESIR). Diabetes Care 2011, 34(4):813-817.
• [31]Beydoun MA, Gary TL, Caballero BH, Lawrence RS, Cheskin LJ, Wang Y: Ethnic differences in dairy and related nutrient consumption among US adults and their association with obesity, central obesity, and the metabolic syndrome. Am J Clin Nutr 2008, 87(6):1914-1925.
• [32]Morr CV, Ha EY: Whey protein concentrates and isolates: processing and functional properties. Crit Rev Food Sci Nutr 1993, 33(6):431-476.
• [33]Dalgleish DG, Corredig M: The structure of the casein micelle of milk and its changes during processing. Annu Rev Food Sci Technol 2012, 3:449-467.
• [34]Huffman LM, Harper WJ: Maximizing the value of milk through separation technologies. J Dairy Sci 1999, 82(10):2238-2244.
• [35]Boye J, Wijesinha-Bettoni R, Burlingame B: Protein quality evaluation twenty years after the introduction of the protein digestibility corrected amino acid score method. Br J Nutr 2012, 108:S183-S211.
• [36]FAO United Nations Expert Consultation (Ed): Dietary protein quality evaluation in human nutrition. Auckland; 2011.
• [37]Pennings B, Boirie Y, Senden JM, Gijsen AP, Kuipers H, Van Loon LJ: Whey protein stimulates postprandial muscle protein accretion more effectively than do casein and casein hydrolysate in older men. Am J Clin Nutr 2011, 93(5):997-1005.
• [38]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(2):239-248.
• [39]Bassil MS, Gougeon R: Muscle protein anabolism in type 2 diabetes. Curr Opin Clin Nutr Metab Care 2013, 16(1):83-88.
• [40]Boirie Y, Dangin M, Gachon P, Vasson MP, Maubois JL, Beaufrère B: Slow and fast dietary proteins differently modulate postprandial protein accretion. Proc Natl Acad Sci USA 1997, 94(26):14930-14935.
• [41]Dangin M, Boirie Y, Garcia-Rodenas C, Gachon P, Fauquant J, Callier P, et al.: The digestion rate of protein is an independent regulating factor of postprandial protein retention. Am J Physiol Endocrinol Metab 2001, 280(2):E340-E348.
• [42]Calbet JAL, 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(3):127-139.
• [43]Claessens M, Saris WHM, Van Baak MA: Glucagon and insulin responses after ingestion of different amounts of intact and hydrolysed proteins. Br J Nutr 2008, 100(1):61-69.
• [44]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(1):E231-E242.
• [45]Nilsson M, Stenberg M, Frid AH, Holst JJ, Björck IME: Glycemia and insulinemia in healthy subjects after lactose-equivalent meals of milk and other food proteins: the role of plasma amino acids and incretins. Am J Clin Nutr 2004, 80(5):1246-1253.
• [46]Nilsson M, Holst JJ, Björck IM: Metabolic effects of amino acid mixtures and whey protein in healthy subjects: studies using glucose-equivalent drinks. Am J Clin Nutr 2007, 85(4):996-1004.
• [47]Pistrosch F, Natali A, Hanefeld M: Is Hyperglycemia a cardiovascular risk factor? Diabetes Care 2011, 34(S2):S128-S131.
• [48]Gerich JE: CLinical significance, pathogenesis, and management of postprandial hyperglycemia. Arch Intern Med 2003, 163(11):1306-1316.
• [49]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(4):966-975.
• [50]Claessens M, Calame W, Siemensma AD, Van Baak MA, Saris WHM: The effect of different protein hydrolysate/carbohydrate mixtures on postprandial glucagon and insulin responses in healthy subjects. Eur J Clin Nutr 2009, 63(1):48-56.
• [51]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(8):1241-1248.
• [52]Gunnerud UJ, Heinzle C, Holst JJ, Ostman EM, Björck IME: Effects of pre-meal drinks with protein and amino acids on glycemic and metabolic responses at a subsequent composite meal. PLoS One 2012, 7(9):e44731.
• [53]Frid AH, Nilsson M, Holst JJ, Björck IME: Effect of whey on blood glucose and insulin responses to composite breakfast and lunch meals in type 2 diabetic subjects. Am J Clin Nutr 2005, 82(1):69-75.
• [54]Ma J, Stevens JE, Cukier K, Maddox AF, Wishart JM, Jones KL, et al.: Effects of a protein preload on gastric emptying, glycemia, and gut hormones after a carbohydrate meal in diet-controlled type 2 diabetes. Diabetes Care 2009, 32(9):1600-1602.
• [55]Moller DE: New drug targets for type 2 diabetes and the metabolic syndrome. Nature 2001, 414(6865):821-827.
• [56]Manders RJF, Praet SFE, Meex RCR, Koopman R, De Roos AL, Wagenmakers AJM, et al.: Protein hydrolysate/leucine co-ingestion reduces the prevalence of hyperglycemia in type 2 diabetic patients. Diabetes Care 2006, 29(12):2721-2722.
• [57]Manders RJF, Praet SFE, Vikström MH, Saris WHM, Van Loon LJC: Protein hydrolysate co-ingestion does not modulate 24 h glycemic control in long-standing type 2 diabetes patients. Eur J Clin Nutr 2009, 63(1):121-126.
• [58]Van Loon LJC, Kruijshoop M, Menheere PPCA, Wagenmakers AJM, Saris WHM, Keizer HA: Amino acid ingestion strongly enhances insulin secretion in patients with long-term type 2 diabetes. Diabetes Care 2003, 26(3):625-630.
• [59]Pal S, Ellis V, Dhaliwal S: Effects of whey protein isolate on body composition, lipids, insulin and glucose in overweight and obese individuals. Br J Nutr 2010, 104(5):716-723.
• [60]Ginsberg HN, Zhang Y-L, Hernandez-Ono A: Metabolic syndrome: focus on dyslipidemia. Obesity 2006, 14(S2):41S-49S.
• [61]Jackson KG, Poppitt SD, Minihane AM: Postprandial lipemia and cardiovascular disease risk: Interrelationships between dietary, physiological and genetic determinants. Atherosclerosis 2012, 220(1):22-33.
• [62]Holm C: Molecular mechanisms regulating hormone-sensitive lipase and lipolysis. Biochem Soc Trans 2003, 31(Pt 6):1120-1124.
• [63]Cohen JC: Protein ingestion does not affect postprandial lipaemia or chylomicron-triglyceride clearance. Eur J Clin Nutr 1989, 43(7):497-499.
• [64]Westphal S, Kästner S, Taneva E, Leodolter A, Dierkes J, Luley C: Postprandial lipid and carbohydrate responses after the ingestion of a casein-enriched mixed meal. Am J Clin Nutr 2004, 80(2):284-290.
• [65]Westphal S, Taneva E, Kästner S, Martens-Lobenhoffer J, Bode-Böger S, Kropf S, et al.: Endothelial dysfunction induced by postprandial lipemia is neutralized by addition of proteins to the fatty meal. Atherosclerosis 2006, 185(2):313-319.
• [66]Pal S, Ellis V, Ho S: Acute effects of whey protein isolate on cardiovascular risk factors in overweight, post-menopausal women. Atherosclerosis 2010, 212(1):339-344.
• [67]Brader L, Holm L, Mortensen L, Thomsen C, Astrup A, Holst JJ, et al.: Acute effects of casein on postprandial lipemia and incretin responses in type 2 diabetic subjects. Nutr Metab Cardiovasc Dis 2010, 20(2):101-109.
• [68]Holmer-Jensen J, Hartvigsen ML, Mortensen LS, Astrup A, De Vrese M, Holst JJ, et al.: Acute differential effects of milk-derived dietary proteins on postprandial lipaemia in obese non-diabetic subjects. Eur J Clin Nutr 2012, 66(1):32-38.
• [69]Mortensen LS, Hartvigsen ML, Brader LJ, Astrup A, Schrezenmeir J, Holst JJ, et al.: Differential effects of protein quality on postprandial lipemia in response to a fat-rich meal in type 2 diabetes: comparison of whey, casein, gluten, and cod protein. Am J Clin Nutr 2009, 90(1):41-48.
• [70]Gouni-Berthold I, Schulte DM, Krone W, Lapointe J-F, Lemieux P, Predel H-G, et al.: The whey fermentation product malleable protein matrix decreases TAG concentrations in patients with the metabolic syndrome: a randomised placebo-controlled trial. Br J Nutr 2012, 107(11):1694-1706.
• [71]Hamad EM, Taha SH, Abou Dawood A-GI, Sitohy MZ, Abdel-Hamid M: Protective effect of whey proteins against nonalcoholic fatty liver in rats. Lipids Health Dis 2011, 10:57.
• [72]Kris-Etherton PM, Grieger JA, Hilpert KF, West SG: Milk products, dietary patterns and blood pressure management. J Am Coll Nutr 2009, 28(S1):103S-119S.
• [73]Schinzari F, Tesauro M, Rovella V, Galli A, Mores N, Porzio O, et al.: Generalized impairment of vasodilator reactivity during hyperinsulinemia in patients with obesity-related metabolic syndrome. Am J Physiol Endocrinol Metab 2010, 299(6):E947-E952.
• [74]Ballard KD, Kupchak BR, Volk BM, Mah E, Shkreta A, Liptak C, et al.: Acute effects of ingestion of a novel whey-derived extract on vascular endothelial function in overweight, middle-aged men and women. Br J Nutr 2012, 13:1-12.
• [75]Fluegel SM, Shultz TD, Powers JR, Clark S, Barbosa-Leiker C, Wright BR, et al.: Whey beverages decrease blood pressure in prehypertensive and hypertensive young men and women. Int Dairy J 2010, 20(11):753-760.
• [76]Pins JJ, Keenan JM: Effects of whey peptides on cardiovascular disease risk factors. J Clin Hypertens (Greenwich) 2006, 8(11):775-782.
• [77]Pal S, Ellis V: The chronic effects of whey proteins on blood pressure, vascular function, and inflammatory markers in overweight individuals. Obesity (Silver Spring) 2010, 18(7):1354-1359.
• [78]Sharpe SJ, Gamble GD, Sharpe DN: Cholesterol-lowering and blood pressure effects of immune milk. Am J Clin Nutr 1994, 59(4):929-934.
• [79]Kawase M, Hashimoto H, Hosoda M, Morita H, Hosono A: Effect of administration of fermented milk containing whey protein concentrate to rats and healthy men on serum lipids and blood pressure. J Dairy Sci 2000, 83(2):255-263.
• [80]Xu J-Y, Qin L-Q, Wang P-Y, Li W, Chang C: Effect of milk tripeptides on blood pressure: A meta-analysis of randomized controlled trials. Nutrition 2008, 24(10):933-940.
• [81]Pal S, Ellis V: Acute effects of whey protein isolate on blood pressure, vascular function and inflammatory markers in overweight postmenopausal women. Br J Nutr 2011, 105(10):1512-1519.
• [82]Ghanim H, Aljada A, Hofmeyer D, Syed T, Mohanty P, Dandona P: Circulating mononuclear cells in the obese are in a proinflammatory state. Circulation 2004, 110(12):1564-1571.
• [83]Otani H, Hata I: Inhibition of proliferative responses of mouse spleen lymphocytes and rabbit Peyer’s patch cells by bovine milk caseins and their digests. J Dairy Res 1995, 62(2):339-348.
• [84]Eriksen EK, Vegarud GE, Langsrud T, Almaas H, Lea T: Effect of milk proteins and their hydrolysates on in vitro immune responses. Small Rumin Res 2008, 79(1):29-37.
• [85]Wong CW, Seow HF, Husband AJ, Regester GO, Watson DL: Effects of purified bovine whey factors on cellular immune functions in ruminants. Vet Immunol Immunopathol 1997, 56(1–2):85-96.
• [86]Holmer-Jensen J, Karhu T, Mortensen LS, Pedersen SB, Herzig K-H, Hermansen K: Differential effects of dietary protein sources on postprandial low-grade inflammation after a single high fat meal in obese non-diabetic subjects. Nutr J 2011, 10:115.
• [87]Perrone F, Da-Silva-Filho AC, Adôrno IF, Anabuki NT, Leal FS, Colombo T, et al.: Effects of preoperative feeding with a whey protein plus carbohydrate drink on the acute phase response and insulin resistance. A randomized trial. Nutr J 2011, 10:66.
• [88]Sugawara K, Takahashi H, Kashiwagura T, Yamada K, Yanagida S, Homma M, et al.: Effect of anti-inflammatory supplementation with whey peptide and exercise therapy in patients with COPD. Respir Med 2012, 106(11):1526-1534.
• [89]Barkeling B, Rössner S, Björvell H: Effects of a high-protein meal (meat) and a high-carbohydrate meal (vegetarian) on satiety measured by automated computerized monitoring of subsequent food intake, motivation to eat and food preferences. Int J Obes 1990, 14(9):743-751.
• [90]Porrini M, Crovetti R, Testolin G, Silva S: Evaluation of satiety sensations and food intake after different preloads. Appetite 1995, 25(1):17-30.
• [91]Poppitt SD, McCormack D, Buffenstein R: Short-term effects of macronutrient preloads on appetite and energy intake in lean women. Physiol Behav 1998, 64(3):279-285.
• [92]Anderson GH, Moore SE: Dietary proteins in the regulation of food intake and body weight in humans. J Nutr 2004, 134(4):974S-979S.
• [93]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(5):373-385.
• [94]Weigle DS, Breen PA, Matthys CC, Callahan HS, Meeuws KE, Burden VR, et al.: 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(1):41-48.
• [95]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(8):2913-2919.
• [96]Blom WAM, Lluch A, Stafleu A, Vinoy S, Holst JJ, Schaafsma G, et al.: Effect of a high-protein breakfast on the postprandial ghrelin response. Am J Clin Nutr 2006, 83(2):211-220.
• [97]Bowen J, Noakes M, Clifton PM: Appetite hormones and energy intake in obese men after consumption of fructose, glucose and whey protein beverages. Int J Obes (Lond) 2007, 31(11):1696-1703.
• [98]Aldrich ND, Reicks MM, Sibley SD, Redmon JB, Thomas W, Raatz SK: Varying protein source and quantity do not significantly improve weight loss, fat loss, or satiety in reduced energy diets among midlife adults. Nutr Res 2011, 31(2):104-112.
• [99]Penhoat A, Mutel E, Amigo-Correig M, Pillot B, Stefanutti A, Rajas F, et al.: Protein-induced satiety is abolished in the absence of intestinal gluconeogenesis. Physiol Behav 2011, 105(1):89-93.
• [100]Clifton PM, Keogh JB, Noakes M: Long-term effects of a high-protein weight-loss diet. Am J Clin Nutr 2008, 87(1):23-29.
• [101]Kushner RF, Doerfler B: Low-carbohydrate, high-protein diets revisited. Curr Opin Gastroenterol 2008, 24(2):198-203.
• [102]Noakes M: The role of protein in weight management. Asia Pac J Clin Nutr 2008, 17(Suppl 1):169-171.
• [103]Paddon-Jones D, Westman E, Mattes RD, Wolfe RR, Astrup A, Westerterp-Plantenga M: Protein, weight management, and satiety. Am J Clin Nutr 2008, 87(5):1558S-1561S.
• [104]Gilbert J-A, Bendsen NT, Tremblay A, Astrup A: Effect of proteins from different sources on body composition. Nutr Metab Cardiovasc Dis 2011, 21(Suppl 2):B16-B31.
• [105]Larsen TM, Dalskov S-M, Van Baak M, Jebb SA, Papadaki A, Pfeiffer AFH, et al.: Diets with high or low protein content and glycemic index for weight-loss maintenance. N Engl J Med 2010, 363(22):2102-2113.
• [106]Josse AR, Atkinson SA, Tarnopolsky MA, Phillips SM: Increased consumption of dairy foods and protein during diet- and exercise-induced weight loss promotes fat mass loss and lean mass gain in overweight and obese premenopausal women. J Nutr 2011, 141(9):1626-1634.
• [107]Veldhorst MAB, Nieuwenhuizen AG, Hochstenbach-Waelen A, Van Vught AJAH, Westerterp KR, Engelen MPKJ, et al.: Dose-dependent satiating effect of whey relative to casein or soy. Physiol Behav 2009, 96(4–5):675-682.
• [108]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(8):1489-1494.
• [109]Anderson GH, Tecimer SN, Shah D, Zafar TA: Protein source, quantity, and time of consumption determine the effect of proteins on short-term food intake in young men. J Nutr 2004, 134(11):3011-3015.
• [110]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(5):622-627.
• [111]Veldhorst MAB, Nieuwenhuizen AG, Hochstenbach-Waelen A, Westerterp KR, Engelen MPKJ, Brummer R-JM, et al.: 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(2):147-155.
• [112]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(2):286-290.
• [113]Poppitt S, Strik C, McArdle B, McGill A, Hall R: Evidence of enhanced serum amino acid profile but not appetite suppression by dietary glycomacropeptide (GMP): a comparison of dairy whey proteins. J Am Coll Nutrin press
• [114]De Graaf C, Blom WAM, Smeets PAM, Stafleu A, Hendriks HFJ: Biomarkers of satiation and satiety. Am J Clin Nutr 2004, 79(6):946-961.
• [115]Karhunen LJ, Juvonen KR, Huotari A, Purhonen AK, Herzig KH: Effect of protein, fat, carbohydrate and fibre on gastrointestinal peptide release in humans. Regul Pept 2008, 149(1–3):70-78.
• [116]Fromentin G, Darcel N, Chaumontet C, Marsset-Baglieri A, Nadkarni N, Tomé D: Peripheral and central mechanisms involved in the control of food intake by dietary amino acids and proteins. Nutr Res Rev 2012, 25(1):29-39.
• [117]Veldhorst MAB, Nieuwenhuizen AG, Hochstenbach-Waelen A, Westerterp KR, Engelen MPKJ, Brummer R-JM, et al.: Effects of complete whey-protein breakfasts versus whey without GMP-breakfasts on energy intake and satiety. Appetite 2009, 52(2):388-395.
• [118]Mars M, Stafleu A, De Graaf C: Use of satiety peptides in assessing the satiating capacity of foods. Physiol Behav 2012, 105(2):483-488.
• [119]Phillips SM, Tang JE, Moore DR: The role of milk- and soy-based protein in support of muscle protein synthesis and muscle protein accretion in young and elderly persons. J Am Coll Nutr 2009, 28(4):343-354.
• [120]Van Loon LJC: Leucine as a pharmaconutrient in health and disease. Curr Opin Clin Nutr Metab Care 2012, 15(1):71-77.
• [121]Frestedt J, Zenk J, Kuskowski M, Ward L, Bastian E: A whey-protein supplement increases fat loss and spares lean muscle in obese subjects: a randomized human clinical study. Nutr Metab (Lond) 2008, 5(1):8.
• [122]Treyzon L, Chen S, Hong K, Yan E, Carpenter CL, Thames G, et al.: A controlled trial of protein enrichment of meal replacements for weight reduction with retention of lean body mass. Nutr J 2008, 7:23.
• [123]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.
• [124]Adechian S, Balage M, Remond D, Migné C, Quignard-Boulangé A, Marset-Baglieri A, et al.: Protein feeding pattern, casein feeding, or milk-soluble protein feeding did not change the evolution of body composition during a short-term weight loss program. Am J Physiol Endocrinol Metab 2012, 303(8):E973-E982.
• [125]Claessens M, Van Baak MA, Monsheimer S, Saris WHM: 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(3):296-304.
• [126]Atherton PJ, Smith K: Muscle protein synthesis in response to nutrition and exercise. J Physiol 2012, 590(5):1049-1057.
• [127]Volpi E, Mittendorfer B, Rasmussen BB, Wolfe RR: The response of muscle protein anabolism to combined hyperaminoacidemia and glucose-induced hyperinsulinemia is impaired in the elderly. J Clin Endocrinol Metab 2000, 85(12):4481-4490.
• [128]Robinson MM, Turner SM, Hellerstein MK, Hamilton KL, Miller BF: Long-term synthesis rates of skeletal muscle DNA and protein are higher during aerobic training in older humans than in sedentary young subjects but are not altered by protein supplementation. FASEB J 2011, 25(9):3240-3249.
• [129]Lacroix M, Bos C, Léonil J, Airinei G, Luengo C, Daré S, et al.: Compared with casein or total milk protein, digestion of milk soluble proteins is too rapid to sustain the anabolic postprandial amino acid requirement. Am J Clin Nutr 2006, 84(5):1070-1079.
• [130]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. Am J Physiol Endocrinol Metab 2012, 303(1):E152-E162.
• [131]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, 36(12):2073-2081.
• [132]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(3):987-992.
• [133]Sheikholeslami Vatani D, Ahmadi Kani Golzar F: Changes in antioxidant status and cardiovascular risk factors of overweight young men after six weeks supplementation of whey protein isolate and resistance training. Appetite 2012, 59(3):673-678.
• [134]Hawley JA, Burke LM, Phillips SM, Spriet LL: Nutritional modulation of training-induced skeletal muscle adaptations. J Appl Physiol 2011, 110(3):834-845.
• [135]Mojtahedi MC, Thorpe MP, Karampinos DC, Johnson CL, Layman DK, Georgiadis JG, et al.: 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(11):1218-1225.
• [136]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(5):494-509.
• [137]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, 16(3):233-244.
• [138]Cermak NM, De Groot LC, Van Loon LJC: Perspective: protein supplementation during prolonged resistance type exercise training augments skeletal muscle mass and strength gains. J Am Med Dir Assoc 2013, 14(1):71-72.
• [139]Verdijk LB, Jonkers RAM, Gleeson BG, Beelen M, Meijer K, Savelberg HHCM, et al.: 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(2):608-616.