REVIEW Open Access A High-protein Diet For Reducing Body .

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Pesta and Samuel Nutrition & Metabolism 2014, /11/1/53REVIEWOpen AccessA high-protein diet for reducing body fat:mechanisms and possible caveatsDominik H Pesta1,3,4* and Varman T Samuel1,2AbstractHigh protein diets are increasingly popularized in lay media as a promising strategy for weight loss by providingthe twin benefits of improving satiety and decreasing fat mass. Some of the potential mechanisms that account forweight loss associated with high-protein diets involve increased secretion of satiety hormones (GIP, GLP-1), reducedorexigenic hormone secretion (ghrelin), the increased thermic effect of food and protein-induced alterations ingluconeogenesis to improve glucose homeostasis. There are, however, also possible caveats that have to be consideredwhen choosing to consume a high-protein diet. A high intake of branched-chain amino acids in combination with awestern diet might exacerbate the development of metabolic disease. A diet high in protein can also pose asignificant acid load to the kidneys. Finally, when energy demand is low, excess protein can be converted toglucose (via gluconeogenesis) or ketone bodies and contribute to a positive energy balance, which is undesirable ifweight loss is the goal. In this review, we will therefore explore the mechanisms whereby a high-protein diet mayexert beneficial effects on whole body metabolism while we also want to present possible caveats associated with theconsumption of a high-protein diet.Keywords: High-protein diet, Weight loss, Satiety, Energy expenditure, Thermic effect of foodIntroductionDiets high in protein have been shown to be a potentialtool for weight loss [1]. General dietary guidelines foradults suggest an acceptable macronutrient distributionrange (AMDR) of 45-65% of total energy from carbohydrates (CHO), 20-35% from fat (F), and 10-35% fromprotein (P) with a recommended dietary allowance (RDA)of 46 and 56 g/d or 0.8 g/kg body weight (BW) of P for females and males, respectively [2]. A diet is therefore considered high in protein if it exceeds 0.8 g/kg BW or thehabitual 15-16% of total energy [3]. High-protein (and lowCHO) diets have recently received much attention in formof the Atkins diet which is a non-energy-restricting, lowCHO (as low as 30 g/day), high-protein/high-fat diet [4],the South Beach diet (low CHO/high protein diet), theStillman diet (low CHO/high protein/low fat) or the Zonediet (low CHO/high protein) (Table 1) [5]. But also dietshigh in protein but containing a normal amount of CHO* Correspondence: dh.pesta@gmail.com1Department of Internal Medicine, Yale University School of Medicine, NewHaven, Connecticut, USA3Department of Sport Science, Medical Section, University of Innsbruck,Innsbruck, AustriaFull list of author information is available at the end of the article(20% P, 50% CHO and 30% F) have been successfully usedto improve metabolic parameters, suggesting that weightmaintenance depends on the protein content but notnecessarily on a low CHO content [6]. Now, millions ofpeople all around the world follow these popular diets.In this critical review, nutrient-specific mechanisms ofprotein-induced satiety for weight loss and preservationof fat-free mass as well as possible caveats of a highprotein diet will be discussed.Mechanisms of satiation with a short-term high-protein dietSustained satiety is a key component to induce a negativeenergy balance and to promote weight loss. An idealweight loss strategy would promote satiety and maintainbasal metabolic rates despite a negative energy balanceand reduction in fat-free mass. Satiety is multifactorial andinfluenced by many components including but not limitedto the endocrine system, the cognitive and neural systemas well as the gastrointestinal system. A diet high inprotein seems to be able to influence certain systems. Thehierarchy for macronutrient-induced satiating efficiency issimilar to that observed for diet-induced thermogenesis(DIT): protein is the most satiating macronutrient followed 2014 Pesta and Samuel; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of theCreative Commons Attribution License (, which permits unrestricted use,distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons PublicDomain Dedication waiver ) applies to the data made available in thisarticle, unless otherwise stated.

Pesta and Samuel Nutrition & Metabolism 2014, /11/1/53Page 2 of 8Table 1 Popular high-protein diets and theirmacronutrient compositionDIETUSDA -35%0.8Atkins [4]6%59%35%2.3South Beach [5]28%33%39%2.6Stillman [5]3%33%64%4.3Zone [5]36%29%34%2.3High Protein, normalCHO [6]50%30%20%1.3*based on a 2000 kcal diet and a 75 kg CHOs and fat, which is least satiating [7]. This satiatingeffect is most significant after high-protein diets [8]. Basedon a visual analogue scale (VAS), which comprises a standard tool to measure subjective appetite and satiety [9], satiety was significantly greater after a 60% protein meal thanafter a 19% protein meal [10]. These findings were confirmed by Crovetti et al. who reported significantly greatersatiety after consumption of an isocaloric meal containing68% protein compared with a 10% protein meal [11]. Increased satiety helps to decrease energy intake, which is arequisite for successful weight loss. In general, increasedsatiety has been observed after meals with a protein contentin the range of 25% to 81% [12].Interestingly, different types of protein induce distincteffects on satiety and responses of (an)orexigenic hormones.Also the mechanism of satiety is different, especially forwhey and casein proteins. Hall et al. compared whey andcasein protein and reported decreased energy intake froma buffet meal offered after 90 min after whey protein ingestion, indicating an increased satiety response to whey[13]. As the absorption of casein is slower due to clot formation, 90 min may be too short to make the conclusionof increased satiety. Veldhorst et al. [14] compared thesatiating effects of either 10% or 25% of energy fromcasein-, soy-, or whey-protein. At 10%, whey provoked thestrongest reduction in hunger followed by casein and soy.Decreased hunger rates coincided with higher leucine, lysine, tryptophan, isoleucine, and threonine responses withthis protein type. For the 25% protein intake, the authorsreport larger responses in hormone concentrations forwhey-protein as compared to casein- or soy-protein.When Hochstenbach-Waelen et al. [15] compared theeffects of 2 diets with either 25% or 10% of energy fromcasein, they report increased energy expenditure, proteinbalance, satiety, and negative fat balance with the 25%casein diet as compared to the 10% diet, indicating adose-dependent satiating effect for this type of protein.Diepvens et al. [16] examined the effects of whey protein,pea protein hydrolysate, a combination of whey proteinand pea protein hydrolysate and control milk protein (80%casein and 20% whey) on appetite ratings and satiety hormones. They found that pea protein hydrolysate was mosteffective in suppressing hunger, followed by whey protein,as compared to milk protein. Surprisingly, these findings donot correlate with changes in satiety hormones, which werestimulated more by milk proteins, indicating that peptidehormone response does not always correlate with perceivedsatiety. Nieuwenhuizen et al. [17] hypothesized that tryptophan (Trp) which serves as a precursor for the anorexigenicneurotransmitter serotonin, would contribute to the satiating effect of this amino acid in dietary proteins. When comparing alpha-lactalbumin (high in Trp), gelatin (low in Trp)or gelatin with added Trp (high in Trp), the authors reportthat the breakfast containing alpha-lactalbumin suppressedhunger more than a gelatin or gelatin trypthophan breakfast. This observation, however, was independent of Trpconcentrations. In conclusion, it seems that different typesof proteins exert distinct effects on satiety and appetite ratings, mediated by a nutrient-specific secretion of hormones.These differences between the proteins seem to be relatedto timing and certain amino acid threshold levels.To assess the nutritional value of dietary proteins considering the protein source and dietary indispensable aminoacid content, the digestible indispensable amino acid score(DIAAS) has been established as a new protein qualitymeasure to replace the protein digestibility-corrected aminoacids score (PDCAAS) [18]. It is derived from the ratiobetween the amount (mg) of digestible dietary indispensable amino acid in 1 g of the dietary protein and theamount (mg) of the same dietary indispensable amino acidin 1g of the reference protein. The DIAAS can have valuesbelow or in certain circumstances above 100%. Valuesabove 100% should not be truncated as was done for thePDCAAS [19], except when the DIAAS is calculated forprotein or amino acid intakes for mixed diets or solesource foods. In general, protein quality, digestibility andutilization by the human body is highest in proteins fromanimal sources such as meat, milk and egg, followed bylegume plant protein such as soy with cereal protein suchas wheat concluding this list [20].Several factors contribute to increased protein-inducedsatiety in response to a short-term high-protein intake.The most important ones seem to be i) increased energyexpenditure, increased concentrations of ii) anorexigenichormones, and iii) metabolites such as amino acids and iv)altered gluconeogenesis. High protein diets can thereforefavorably alter the energy balance equation. Enhanced satiety allows for decreased food intake while an increasedthermic effect allows for greater calorie output.Energy expenditureThe thermic effect of food, also called diet-inducedthermogenesis (DIT), is a metabolic response to food.Food intake results in a transient increase in energy

Pesta and Samuel Nutrition & Metabolism 2014, /11/1/53expenditure attributable to the various steps of nutrient processing (i.e. digestion, absorption, transport, metabolism and storage of nutrients). The DIT is mostlyindicated as percentage increase in energy expenditureover the basic metabolic rate (BMR). DIT values arehighest for protein ( 15-30%), followed by CHOs ( 5-10%)and fat ( 0-3%) [21,22]. Based on a recent meta-analysis,the thermic effect of food increases 29 kJ/4184 kJ ofingested food for each increase of 10 percentage points inthe percentage of energy from protein [23]. In other words,if a subject therefore consumes an 8368 kJ/d diet with 30%energy from protein, then the thermic effect of food will be58 kJ/d higher than if protein contributes only 20% of thedietary energy. This is only an estimate while actual measurements can be higher, as shown below.The high DIT of protein therefore affects energy balance. Whitehead et al. [24] used a room calorimeter toassess 24-h energy expenditure in subjects on a highprotein diet (36% energy from protein) against two with15% energy from protein, one high in carbohydrate and theother high in fat. The authors reported that energy expenditure was 297 kJ/d higher in subjects consuming the highprotein diet (P 0.05), which was in agreement withthe increase in sleeping metabolic rate. Mikkelsen et al.[25] found that subjects consuming a diet containing 29%of protein had a 891 kJ/d higher resting metabolic ratethan subjects consuming the same eucaloric diet with11% energy from protein. For weight loss, however,DIT-related satiety is even more important. A high proteindiet is associated with increased 24-h diet-induced energyexpenditure [26]. The increase in DIT may increase satiety.A potential mechanism to account for this observation isthe increase in oxygen demand to metabolize proteins,which can enhance satiety [26]. A similar phenomenonof appetite suppression can be observed at high altitudewhere oxygen is limited [27]. This increased oxygendemand stems from the high postprandial amino acidoxidation rate which is of even greater importance ifamino acids are given in excess of their deposition.Satiety hormonesThere are other possible mechanisms to explain the improvement in satiety with high-protein diets. Early observations that glucose was more expediently metabolizedafter an oral load versus a matched intravenous loadled to the discovery and characterization of the incretinhormones. Two key incretins are glucose-dependent insulinotropic polypeptide (GIP) and glucagon-like peptide-1(GLP-1). These hormones are synthesized in the gut andsecreted from enteroendocrine cells in the intestinalepithelium in response to an oral nutrient load [28]. Therelease of the two incretin hormones potentiates glucosestimulated insulin release from the beta-cells [29]. Incretinspotentiate glucose disposal by stimulating insulin secretion,Page 3 of 8estimated to account for at least 50% of the total postprandial insulin release [30,31]. Besides their insulinotropicaction, GLP-1 inhibits glucagon secretion in a glucosedependent manner, thus diminishing postprandial glucoseexcursions [29]. Extrapancreatic effects of GLP-1 includeinhibition of gastrointestinal motility and secretion andthereby regulation of appetite and food intake.Cholecystokinin (CCK) is a peptide hormone found inthe brain and the gastrointestinal tract [32]. CCK stimulatesintestinal motor activity and significantly contributes to theinhibition of gastric emptying. Ingestion of dietary proteinand especially digestion (hydrolisation) of proteins intoamino acids effectively stimulates CCK release in the gut[33]. It is now clear that CCK reduces food intake andmeal size and induces satiety [34] in a variety of mammalian species including rats, rhesus monkeys and humans.Brennan et al. [35] reported suppressed energy intake inlean and obese subjects after high-protein meals, an effectpotentially mediated by CCK and ghrelin. The short-termmeal-related satiety signal of the peptide is most likely mediated through the CCKA receptor [36] and may involveother satiety players such as insulin and leptin [37]. CCKsfunctions include stimulation of pancreatic secretion,gallbladder contraction and intestinal mobility as wellas inhibition of gastric emptying [38].A recent study showed that GLP-1 blunted postprandialglucose response and reduced insulin release by reducinggastric emptying at physiological doses in response toa mixed meal. This increased gastric retention, loweredhunger and the desire to eat and augmented satiety [39].The process of gastric emptying might play an importantrole in the perception of hunger and satiety. In the samestudy, GIP reduced postprandial glucose increment primarily through an increased insulin release with no effecton the gastric emptying rate [39]. GIP contributes to theregulation of glucose uptake and stimulates triglyceridestorage in adipocytes [40]. Chronic exposure to incretinmimetics leads to weight reduction in type 2 diabetics [41].The ubiquitous serine protease dipeptidyl peptidase-4(DPP-4) is responsible for the degradation of these peptides. While incretin mimetics do promote weight loss, theeffect of DPP-4 inhibitors on weight control is less clear.Nevertheless, pharmacological inhibition of DPP-4 activitymay be a strategy to decrease appetite and improve thecondition of type-2-diabetes. Inhibition of DPP-4 activityby certain foods is therefore of great importance for medical nutrition therapy. It was shown that the tripeptideIle-Pro-Ala (IPA) generated by proteinase K mediated proteolysis of the whey protein component beta-lactoglobulincan act as a DPP-4 inhibitor, thereby delaying GIP andGLP-1 degradation [42]. It was suggested by the authorsthat after luminal degradation, the IPA fragments mayact in situ as competitive inhibitors of DPP-4 as it cleavespeptides with an N-terminal alanine or proline amino acid

Pesta and Samuel Nutrition & Metabolism 2014, /11/1/53residue [43], suggesting a similar, albeit more modest, effectas pharmacological DPP-4 inhibitors such as Sitagliptin. Increased incretin levels mediate postprandial insulin release,thereby inducing satiety [44] and the preference for foodrelated cues [45].The secretion of gut neuropeptides that induce satiation,GLP-1, CCK, and peptide YY (PYY) seem to be increasedin response to a high-protein diet whereas concentrationsof orexigenic hormones such as ghrelin seem to be reduced [46,47]. Enteroendocrine cells which release GLP-1and GIP are in direct contact with the gut lumen and bythis means seem to be able to sense arrival and passage ofnutrients along the gastrointestinal tract. Studies involvinghuman enteroendocrine cell lines have shown that essential amino acids (after hydrolytic digestion of complexproteins) activated p38 MAPK and ERK1/2 pathway resulting in nutrient-stimulated GLP-1 release [48]. It has to benoted, however, that GLP-1 secretion is nutrient related(increased after a protein meal in combination with CHOs)[49]. These gut neuropeptides were increased in womenfed a high protein diet (30% P/40% CHO/30% F) whencompared to an adequate protein diet (10% P/60% CHO/30% F) [46]. Increased GLP-1 concentrations were alsofound in men after a high protein breakfast, lunch anddinner [50]. A study in humans by Blom et al. showedincreased satiety due to decreased postprandial ghrelinconcentrations in response to a high-protein breakfastcompared to an isocaloric high-carbohydrate breakfast[51]. It is very likely that increased protein-induced satiety leads to reduced subsequent energy intake whichis beneficial for weight loss. This effect is not related to aconditioned taste aversion. A decreased gastric emptying rate following a high-protein diet has also been observed [52].Plasma amino acid levelsHigh-protein diets may directly promote a satiety response.In 1956 the aminostatic hypothesis was introduced: increased serum amino acid concentrations produced feelings of satiety whereas decreasing concentrations createdfeelings of hunger [53]. Diets high in protein will elevateconcentrations of plasma amino acids [54]. According toNefti et al. high intake of protein induces a vagal feedbackto the satiety center of the nucleus tractus solitarius in thebrainstem and the hypothalamus to suppress hunger [55].Poppitt et al. [56] showed that the satiating effect after ahigh-protein preload was significantly larger than preloadscontaining an iso-energetic amount of carbohydrates orfats. Along these lines, Westerterp-Plantenga [26] found asignificant increase in 24-h satiety in subjects consuming ahigh-protein diet compared to a high-fat diet. The aminostatic hypothesis has been supported by several, but notall studies [57], showing that high-protein diets resultin higher levels of satiety, however, complex homeostaticPage 4 of 8mechanisms between the peripheral organs and thecentral nervous system which cause the aminostatic effectare not yet fully understood. More research in this area isnecessary to elucidate this hypothesis.GluconeogenesisAlteration of gluconeogenesis has been found to contributeto satiety [58]. High-protein and low-carbohydrate dietspromote hepatic gluconeogenesis to maintain plasmaglucose levels. Two key enzymes of gluconeogenesis,phosphoenolpyruvate carboxykinase (PEPCK) and glucose6-phosphatase (G6P), are upregulated in rats fed a highprotein diet, suggesting that gluconeogenesis is stimulated by a high-protein diet [59]. A modulation of hepaticgluconeogenesis and increased glucose homeostasis couldbe responsible for the satiating effect in this animalmodel [60]. Veldhorst et al. [61] also report an increase ingluconeogenesis in healthy

High protein diets are increasingly popularized in lay media as a promising strategy for weight loss by providing the twin benefits of improving satiety and decreasing fat mass. Some of the potential mechanisms that account for weight loss associated with high-protein diets involve incr

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