Dietary Protein, Weight Loss, And Weight Maintenance

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ANRV383-NU29-02ARI16 June 2009ANNUALREVIEWS7:54FurtherClick here for quick links toAnnual Reviews content online,including: Other articles in this volume Top cited articles Top downloaded articles Our comprehensive searchDietary Protein, Weight Loss,and Weight MaintenanceM.S. Westerterp-Plantenga,1,2 A. Nieuwenhuizen,1,2D. Tomé,3 S. Soenen,1,2 and K.R. Westerterp1,2Annu. Rev. Nutr. 2009.29:21-41. Downloaded from www.annualreviews.orgby Boston University on 07/20/13. For personal use only.1Department of Human Biology, Nutrim, Faculty of Health, Medicine, and Life Sciences,Maastricht University, 6200 MD, Maastricht, The Netherlands;email: m.westerterp@hb.unimaas.nl2TIFN, 6700 AN Wageningen, The Netherlands3AgroParisTech, Department of Life Sciences and Health, UMR914 Nutrition Physiologyand Ingestive Behavior, F75005, Paris, FranceAnnu. Rev. Nutr. 2009. 29:21–41Key WordsFirst published online as a Review in Advance onApril 28, 2009satiety, energy expenditure, substrate oxidation, body composition,protein metabolismThe Annual Review of Nutrition is online atnutr.annualreviews.orgThis article’s doi:10.1146/annurev-nutr-080508-141056c 2009 by Annual Reviews.Copyright All rights reserved0199-9885/09/0821-0021 20.00AbstractThe role of dietary protein in weight loss and weight maintenanceencompasses influences on crucial targets for body weight regulation,namely satiety, thermogenesis, energy efficiency, and body composition.Protein-induced satiety may be mainly due to oxidation of amino acidsfed in excess, especially in diets with “incomplete” proteins. Proteininduced energy expenditure may be due to protein and urea synthesisand to gluconeogenesis; “complete” proteins having all essential aminoacids show larger increases in energy expenditure than do lower-qualityproteins. With respect to adverse effects, no protein-induced effects areobserved on net bone balance or on calcium balance in young adults andelderly persons. Dietary protein even increases bone mineral mass andreduces incidence of osteoporotic fracture. During weight loss, nitrogen intake positively affects calcium balance and consequent preservation of bone mineral content. Sulphur-containing amino acids cause ablood pressure–raising effect by loss of nephron mass. Subjects withobesity, metabolic syndrome, and type 2 diabetes are particularly susceptible groups. This review provides an overview of how sustaining absolute protein intake affects metabolic targets for weight loss and weightmaintenance during negative energy balance, i.e., sustaining satiety andenergy expenditure and sparing fat-free mass, resulting in energy inefficiency. However, the long-term relationship between net proteinsynthesis and sparing fat-free mass remains to be elucidated.21

ANRV383-NU29-02ARI16 June 20097:54ContentsAnnu. Rev. Nutr. 2009.29:21-41. Downloaded from www.annualreviews.orgby Boston University on 07/20/13. For personal use only.INTRODUCTION . . . . . . . . . . . . . . . . . .PROTEIN-INDUCED SATIETYBY ACUTE HIGH-PROTEINMEALS AND MEDIUM-TERMHIGH-PROTEIN DIETS . . . . . . . . .Acute High-ProteinMeal-Induced Satiety . . . . . . . . . . .High-Protein Diet-InducedSatiety. . . . . . . . . . . . . . . . . . . . . . . . . .ENERGY EXPENDITURE . . . . . . . . . .Protein Intake and Diet-InducedEnergy Expenditure . . . . . . . . . . . . .Protein Intake and SleepingMetabolic Rate . . . . . . . . . . . . . . . . .Protein Intake and ProteinTurnover . . . . . . . . . . . . . . . . . . . . . . .PROTEIN AND AMINOACID METABOLISM,GLUCONEOGENESIS, ANDGLYCOGEN SYNTHESIS . . . . . . .Protein Turnover andMetabolism . . . . . . . . . . . . . . . . . . . . .Gluconeogenesis . . . . . . . . . . . . . . . . . . .BODY WEIGHT AND BODYCOMPOSITION . . . . . . . . . . . . . . . . .Protein Intake and Energy Intake . . .Sustained-Protein Dietsfor Body-Weight Loss . . . . . . . . . . .Sustained Relatively High-ProteinDiets for Body-WeightMaintenance . . . . . . . . . . . . . . . . . . . .POTENTIAL RISK OFHIGH-PROTEIN DIETS . . . . . . . . .HYPOTHESES TO BEASSESSED. . . . . . . . . . . . . . . . . . . . . . . .CONCLUSIONS . . . . . . . . . . . . . . . . . . . besity is a major health problem with seriouscomorbidities (70, 78). Weight loss is usuallyachieved more readily than weight maintenanceafter body weight loss (70, 107). Conditions forweight maintenance after weight loss are (a) sustained satiety despite negative energy balance,22Westerterp-Plantenga et al.(b) sustained basal energy expenditure despitebody weight loss, due to (c) sparing of fat-freemass, which is the main determinant of basalenergy expenditure.Diets with a relatively high-protein contentact on these metabolic targets (3). Doubling therelative protein content of the diet from thenormal level of 10 to 15 en% to 20 to 30 en% reduces food intake under ad libitum conditions,resulting in immediate body weight loss. In thelong term, body weight reaches a new value ata significantly lower level. Thus, an increase inthe relative protein content of the diet, irrespective of protein type, reduces the risk of a positiveenergy balance and the development of overweight. Increasing protein intake also increasesthe chance of maintenance of body weight after weight loss induced by an energy-restricteddiet. One of the mechanisms contributing tosuccessful maintenance is a sparing effect offat-free mass, reducing the weight loss–induceddecrease of energy expenditure.This review deals with the effects of relatively high-protein diets during energy balance,weight loss, and weight maintenance thereafteron specific metabolic targets: satiety, energy expenditure, protein and amino acid metabolism,and gluconeogenesis. Effects on body weightand body composition are highlighted, and potential risks of high-protein diets are discussed.Where possible, we take into account the typeand quantity of protein, administration of protein, timing of effects, characterization of subjects, energy balance, and duration of studies.Normal- and high-protein diets need tobe defined in relatively and absolutely normal/high protein diets in relation to energybalance (Table 1). Relatively high-proteindiets for weight loss and weight maintenancethereafter consist of at least 25% to 30% of energy from protein; thus, normal protein intakeremains as it was before the diet while totalenergy intake is decreased (see Table 1). Suchdiets are relatively high in protein, expressedas percentage energy from protein; however, inabsolute terms (g of protein) they contain onlya sufficient absolute amount of protein and lessenergy in total. The absolute amount of protein

ANRV383-NU29-02Table 1ARI16 June 20097:54Absolute or relative “normal”- or “high”-protein dietsRelative energy% of proteinEnergy balanceNormal10%–15% (WHO)1.2–1.8 MJ/d 67–100 g/dHigh18%–30%2.2–3.6 MJ/d 120–200 g/dNegative energy-balancee.g., 2 MJ/d“Normal”10%–15%0.2–0.3 MJ/d 11–17 g/d“High”47% (VLED)0.9 MJ/d 52 g/dPositive energy-balance after weight-lossAnnu. Rev. Nutr. 2009.29:21-41. Downloaded from www.annualreviews.orgby Boston University on 07/20/13. For personal use only.Absolute g proteine.g., 12 MJ/de.g., 8 MJ/d“Normal”10%–15%0.8–1.2 MJ/d 44–67 g/d“High”18%–30%1.4–2.2 MJ/d 80–120 g/dExample of calculated grams of protein ingested when relatively normal- or high-protein diets are consumed in energy balance of, for example, 12 MJ/d,or in negative energy balances of, respectively, 2 MJ/d as during a very-low-energy diet (VLED), or 8 MJ/d as during a weight-maintenance dietthereafter. The example shows that during a “high”-protein energy-restricted diet, absolute protein intake in the given ranges is still in the originally“normal” range. WHO, World Health the same in a relatively normal-protein diet(10% to 15% of energy from protein) inneutral-energy balance (energy intake matchesenergy requirement set by energy expenditure)as in a relatively high-protein diet (20% to 30%of energy from protein) in negative-energybalance (energy intake is lower than energyrequirement set by energy expenditure) whensubjects consume, for instance, only half oftheir energy requirements in order to losebody weight.PROTEIN-INDUCED SATIETYBY ACUTE HIGH-PROTEINMEALS AND MEDIUM-TERMHIGH-PROTEIN DIETSA hierarchy prevails for the satiating efficaciesof the macronutrients protein, carbohydrate,and fat, with protein being the most satiating and fat the least satiating. This sequencealso represents the priority with respect to metabolizing these macronutrients (97, 107). Indaily life as well as in many experiments, mixedproteins are consumed from meat, fish, dairyproducts, or plants. A dose-dependent satiating effect of mixed protein has been shown,with quite a range of concentrations of protein offered acutely, in a single meal, to subjects who are in energy balance and are weightstable (83, 97, 107). In addition, persistentprotein-induced satiety is shown when a mixedhigh-protein diet is given for 24 hours up toseveral days (48, 49, 106). Acute, high-proteinmeal- or drink-induced satiety and mediumterm, high-protein diet-induced satiety are discussed in this section. Mechanisms contributingto protein-induced satiety are considered.Acute High-ProteinMeal-Induced SatietyThis section focuses on acute protein-inducedsatiety with single meals, with contents of 25%to 81% of energy from mixed protein or specific proteins, followed by subsequent energyintake reduction (97). Given the average“normal” protein intake range of 10% to 15%of energy, meals with an average of 20% to30% of energy from protein are representative of high-protein diets when consumed inenergy balance (107). Using these protein levels, Smeets et al. (83) examined healthy volunteers with a body mass index (BMI) of 23.8 2.8 kg/m2 and a percentage body fat of 26 8.9and showed that after a high-protein lunch, satiety and energy expenditure were significantlyhigher than after a normal-protein lunch, without differences in ghrelin and peptide tyrosintyrosin (PYY) responses. The lower glucagonlike peptide 1 (GLP-1) response following thehigh-protein lunch is due to the Dietary Protein, Weight Loss, and Weight Maintenance23

ARI16 June 20097:54with the high-carbohydrate-induced GLP-1response during the normal-protein lunch,showing clearly that a GLP-1 response is primarily nutrient related and only secondarilysatiety related (83).The satiating power of a high-protein mealis optimized when timing of the interval between the first administration of a meal containing protein (versus control) and the subsequenttest meal synchronizes with timing of the aminoacid profiles following protein intake (50), ghrelin concentrations (92–97), or visual analoguescale (VAS) satiety ratings (92–97). Ratings ona 100 mm VAS represent feelings of satiety,hunger, fullness, or desire to eat as detected bythe subject. Questions related to appetite profile are anchored with the extreme negative andpositive ratings. A point on the scale then givesthe value of hunger, satiety, etc. Veldhorst et al.(92–97) timed test meals beforehand, by running the experiments in healthy normal-weightsubjects (BMI 23.9 0.3 kg/m2 ) twice: firstdetermining the moment when differences insatiety or ghrelin concentrations were still significantly present, then offering the test mealat that moment in the next experiment. Outcomes appear to differ due to the type or quantity of protein intake, or both. For instance,higher satiating effects due to higher concentrations of casein (93) or soy (94) (25 en% versus10 en%) appear to be related to kinetics ofamino acid profiles (93, 94). Also, with wheyas a single protein in a specifically standardizedcustard breakfast, energy intake was decreasedby 13% at three hours after a breakfast withwhey containing glyco-macropeptide (GMP)compared to energy intake after a breakfastwith whey not containing GMP, irrespective ofwhether the whey-protein content was 10% or25% of energy in the custard breakfast. This decrease in energy intake coincided with increasedconcentrations of certain amino acids, e.g., serine, threonine, alanine, and isoleucine (92). In acomparison of the effects of seven different proteins, in two different concentrations, on energyintake during the subsequent meal, Veldhorstet al. (97) showed (in the same healthy normalweight subjects mentioned above) a moreAnnu. Rev. Nutr. 2009.29:21-41. Downloaded from www.annualreviews.orgby Boston University on 07/20/13. For personal use only.ANRV383-NU29-0224Westerterp-Plantenga et al.satiating effect from incomplete proteins, i.e.,proteins that lack some essential amino acids,versus complete proteins, which contain the essential amino acids. At the level of 10 en% andof 25 en% from one type of protein consumedwith a breakfast custard, energy intake at lunchwas about 20% less after an alpha-lactalbuminor gelatin with or without added tryptophanbreakfast, compared with after a casein, soy, orwhey breakfast; differences in energy intakesof about 20% were a function of differencesin satiety ratings of about 40% (97). In an assessment of different proteins and hydrolysates,Diepvens et al. (19) showed in healthy overweight subjects (BMI 27.6 1.7 kg/m2 ; bodyfat% 32.6 7.9) indications of lower hungerand desire to eat or higher satiety after consumption of pea protein hydrolysate (PPH) orwhey protein (WP) compared to milk protein(MP) or WP PPH. As mentioned above,effects on relevant hormones were primarilynutrient related. Cholecystokinin (CCK) andGLP-1 concentrations were relatively more increased by MP, whereas PYY concentrationswere relatively more elevated and ghrelin concentrations more reduced by WP PPH (19).No effect on energy intake was seen (19). Asimilar effect of protein consumption on PYYconcentration changes was shown by Batterhamet al. (4), who observed significantly higherplasma PYY responses to a high-protein mealin both lean and obese subjects.With respect to different fractions ofprotein, such as alpha-lactalbumin or betalactoglobulin, Pichon et al. (69) showed thatfood intake and body weight gain are significantly lower in rats fed a diet containing betalactoglobulin, which is unrelated to palatability.When different proteins or amino acids areconsumed at very high levels, satiety is veryhigh and differences in satiating effects areno longer observed. For instance Bowen et al.(11, 12) reported no difference between effectsof casein and whey protein, with high-proteinmeals inducing a larger satiating effect thanhigh-carbohydrate meals in healthy normalweight subjects. Furthermore, they noted different appetite-regulatory hormone responses

Annu. Rev. Nutr. 2009.29:21-41. Downloaded from www.annualreviews.orgby Boston University on 07/20/13. For personal use only.ANRV383-NU29-02ARI16 June 20097:54after whey, soy, or gluten preload despite similarreductions in ad libitum energy intake (12). Ina study of food intake in healthy normal-weightto overweight (BMI 25 1.5 kg/m2 ) subjects,Burton-Freeman et al. (13) did not find a difference at the test meal between the conditionswith preloads consisting of whey with or without GMP, whereas CCK release coincided withthe magnitude of satiety ratings.Effects of protein-containing drinks versuscontrol drinks appear when sufficient proteinand energy are present in the drinks. A comparison of isoenergetic dairy fruit drink preloads(300 mL 1.25 MJ) differing in macronutrient composition in normal-weight men (BMI22.6 0.4 kg/m2 ) revealed significantly lessenergy consumption at lunch 120 minutes after the protein (3.2 MJ) than after the control (3.5 MJ) and carbohydrate (CHO) preloads(3.6 MJ), without complete energy-intake compensation (7). A study comparing the effects ofa sugar-sweetened beverage (cola) and a chocolate milk drink (0.9 MJ, 500 mL) in healthysubjects (BMI 22 2 kg/m2 ) showed thatsatiety and fullness were significantly greater30 minutes after consumption of chocolate milkthan after cola, although no significant difference in energy intake occurred during lunch(3.2 MJ after chocolate milk versus 3.3 MJ aftercola) (35). Soenen et al. (84) found no differencein effects on appetite, energy intake, and energy intake compensation 50 minutes after consumption of 800 ml 1.5 MJ milk, or carbohydrate drinks in their study of 40 young healthynormal-weight (BMI 22.1 1.9 kg/m2 ) menand women. A study of normal-weight andobese boys showed that 60 minutes after consumption of glucose and whey-protein drinks(250 mL 3.5 MJ), food intake was suppressedmore by whey protein (2.7 MJ) than by glucose (3.1 MJ) or control (3.6 MJ) drinks (6).Taken together, these results indicate that thereis a bandwidth in protein amount and concentrations in which relatively more protein ismore satiating and promotes less energy intake, supported by relatively elevated aminoacid concentrations, anorexigenic hormones, orenergy expenditure feeding back on the centralnervous system. Mellinkoff (58) suggested asearly as 1956 that an elevated concentrationof blood or plasma amino acids, which cannot be channeled into protein synthesis, servesas a satiety signal for a food intake–regulatingmechanism and thereby results in depressedfood intake.There may be some specificity in the effectsof individual amino acids on satiety since specific amino acids also serve as precursors forspecific neurotransmitters involved in appetiteor body-weight regulation or directly influencebiochemical pathways involved in eating behavior. For instance, the amino acid tryptophanmay act as a precursor for the neurotransmitterserotonin (113). It has been suggested that brainserotonin is involved in appetite regulation (47),a hypothesis that is supported by the anorexigenic effects of serotonergic drugs in humans(32, 91). Several dietary intervention studieshave attempted to increase brain serotonergicactivity, mainly through increasing central tryptophan availability (5, 51, 52, 113). Tryptophantransport to the brain is facilitated by the socalled l-transporter, which also facilitates thetransport of other large neutral amino acids(LNAAs), valine, leucine, isoleucine, tyrosine,and phenylalanine in a competitive manner(8, 113). Therefore, brain tryptophan uptakemay depend not only on plasma tryptophanconcentrations, but also on the plasma ratio oftryptophan to the sum of these other LNAAs(8, 113). The whey peptide alphalactalbumincontains relatively high levels of tryptophan andhas been shown to increase plasma tryptophanconcentrations and plasma tryptophan/LNAAratio when ingested alone (5, 51, 52) or aspart of a meal (8). Indeed, an alphalactalbumincontaining breakfast suppressed hunger morethan did a breakfast containing gelatin (whichcontains very low levels of tryptophan) (64).However, tryptophan addition to the gelatincontaining breakfast did not affect hunger ratings. Also, plasma concentrations of tryptophanas well as the plasma tryptophan/LNAA ratiowere not related to hunger. Therefore, thesedata suggest that tryptophan (and hence, serotonin) is unlikely to play a role in this effect (64) Dietary Protein, Weight Loss, and Weight Maintenance25

ARI16 June 20097:54In a test of the same hypothesis, Koren et al. (45)studied healthy overweight subjects (BMI 27 2.3 kg/m2 ) and concluded that an increase ineither carbohydrate or protein intake increasessatiety and leads to significant weight loss independent of an increase in plasma concentrationof tryptophan or the tryptophan/LNAA ratio.Likewise, the amino acid tyrosine can beconverted into the neurotransmitters dopamineand norepinephrine, both of which have shownto be involved in food-intake regulation (101).Although alterations in tyrosine metabolismhave been observed in eating disorders suchas anorexia (1), there is no direct evidenceof a role for tyrosine in protein-induced satiety. A third amino acid that functions as aprecursor for a neurotransmitter is histidi

Relatively high-protein diets for weight loss and weight maintenance thereafter consist of at least 25% to 30% of en-ergy from protein; thus, normal protein intake remains as it was before the diet while total energy intake is decreased (see Table 1). Such diets are relatively high in

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