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The satiating mechanisms of major food constituents – An aid to rational food design
Trends in Food Science & Technology 32 (2013) 43e50
Review
The satiating mechanisms of major food constituents e An aid to rational food design Susana Fiszman* and Paula Varela Instituto de Agroquımica y Tecnologıa de Alimentos (IATA-CSIC), Agustın Escardino 7, 46980 Paterna (Valencia), Spain (Tel.: D34 963900022; fax: D34 963636301; e-mails: [email protected]; pvarela@ iata.csic.es) The worldwide rise in the prevalence of excess weight lends great interest to preventive measures aimed at satiety/satiation. Human body-weight regulation is complex and is rooted in a superstructure that takes in sensory signals from food, neurohormonal signals from the digestive tract and signals from the body’s energy reserves. Recent research has contributed more insight into the satiating mechanisms of constituents/ingredients for new food design. Knowing why to select them, what they contribute to the food’s physical and sensory properties and how they are integrated into the food matrix will provide suitable tools for designing satiating foods.
Introduction The worldwide rise in the prevalence of excess weight and obesity that affects a high percentage of population lends great interest to preventive measures aimed at weight control and satiety. The western world produces obesitygenerating environments with an abundance of (possibly) not very healthy products (Shill et al., 2012) with a high energy density or an unbalanced nutritional profile. * Corresponding author. 0924-2244/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tifs.2013.05.006
The great advantage of formulating satiating foods is the immediate benefit of feeling full or not feeling hungry for a longer time, instead of a promise that requires sacrifices or a strong will before the benefits are felt. The type of food formulated and the way the satietypromoting ingredients are selected have direct implications for the way the body processes them, and the consumer’s satisfaction has implications for the perception of satiety as an additional value. It is worth noting that these products do not in themselves contribute to weight loss, although a given portion of them can work with adequate amounts of nutritious food to reduce the hunger pangs that occur at a certain time interval after their consumption (Booth, 2011). The quest for a magic ingredient has passed into history. However, the many mechanisms that have been described for each macronutrient and the levels on which they act, together with their diversity of structures and chemical composition, evidently make it possible to design foods that can act on more than one level and achieve overall acceptability. It is difficult to (re)formulate food products to enhance their satiating capacities because the constituents can themselves influence energy density, palatability, texture and a number of other factors that are involved in feeding behaviour. Some of the effects overlap, to an uncertain degree, emphasizing the need for integrative research. A radical change in diet evidently cannot and should not be recommended, but a feasible lifestyle adaptation to a moderately higher-protein, higher-fibre, controlledenergy diet should be possible (Hill, 2006). There is a need for healthier low-energy, low-fat, energy-dilute foods that are affordable, attractive and convenient, and e importantly e as tasty and gratifying as the unhealthier items they are intended to replace (Halford & Harrold, 2012). These food items will produce consumer satisfaction with their filling effects at particular times when the food product is eaten under specific conditions and could encourage healthy dietary habits while used in that way to prevent weight gain. This paper will focus on the satiating mechanisms of macronutrients and how they can contribute to the design of foods with enhanced satiating capacity. Particular interest will be paid to the important role of the food matrix in which the substance/ingredient is embedded.
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Appetite, satiation and satiety To understand the role of appetite in free individuals, the individual and combined environmental, psychological, and physiologic conditions that generate, modulate, and terminate appetite sensations would need to be quantified (Mattes, Hollis, Hayes, & Stunkard, 2005). Appetite is the motive that leads a person to seek food, choose it and eat it (De Graaf, Blom, Smeets, Stafleu, & Hendriks, 2004). Satiety is a state of suppression of appetite, while satiation moves into a deeper state of satiety. A vast amount of literature has reported the effects of some types of nutritional and compositional manipulation on appetite, observed through clinical trials involving within- and inter-meal measurements of the sensation of fullness, following the widely extended notion that tightly associates ‘satiety’ and ‘satiation’ to times between meals and within meals respectively (Blundell et al., 2009, 2010). These human intervention studies normally use a preload design, employing methods such as the so-called visual analogue scales (VAS) (EFSA, 2012), in which subjects rate their level of appetite/hunger/satiety on line scales or structured scales. Stubbs et al. (2000) reported that these kinds of rating are best used in conjunction with other measures (e.g. feeding behaviour, changes in plasma metabolites) (De Graaf et al., 2004; Lemmens, Martens, Kester, & Westerterp-Plantenga, 2011). The use of VAS has been criticized. In the opinion of some researchers, the amount of a test meal that a person eats is a subjective outcome accumulated from many choices of another mouthful, each subjected to several rapidly changing influences, so measurements of their effects on the apparent willingness to eat the available food at each moment during a meal would be needed to explain the amount consumed (Booth, 2009). According to this current of opinion, suppression of the appetite for portions of specific foods through the effects of eating these and other foods rises and falls from start to end of a meal (confounding the measurements of meal size), and over the interval until the next eating event, and involves separate mechanisms, many of which may be operative to some extent from during a meal until after it. According to Woods and Langhans (2012), failures to replicate the effects of compounds on food intake are commonplace because these effects are subject to numerous influences that can render them completely ineffective at times. Non-declarative methods such as facial expression (evaluated by filming the consumers while eating) have recently been reported as a new tool for satiation assessment (Espagnac, Laboure, Delarue, & Gurviez, 2012). Studies on satiating food. Major food constituents Because of improved knowledge of the neurobiological mechanisms of satiation (Gatta-Cherifi, 2012) and new and better assessment tools, the effects of different foods on appetite have been increasingly studied for many years now (Fig. 1).
Fig. 1. Evolution of the number of scientific papers on satiety/satiation since 1990.
The effect that a type of component/ingredient can have on satiety depends both on its physical properties when eaten and on its physiological effects in the gut (Benelam, 2009). It is remarkable how little information on the preparation of the foods administered in the clinical trials is generally found in the literature (mainly in nutrition-related journals). The dosage of the substance added to the food is mentioned, but the physical properties of the food in relation to the control or placebo are almost never measured or reported. Another factor that is not elucidated is the structure of the food. Physiological responses depend not only on the nutrient composition and energy content of the food but also on its structure, spatial distribution and particle size and shape, which in turn determine its texture, perception of moisture, etc., and the type and speed of digestion (Lundin, Golding, & Wooster, 2008). The volume of a food eaten as a preload can also affect satiety by introducing air, for example, quite apart from changes in energy density (Rolls, Bell, & Waugh, 2000). Further understanding of these multiple influences on food intake may lead to strategies for controlling hunger while reducing energy intake. Narumi, Ban, Kajinami, Tanikawa, and Hirose (2012) propose a method for modifying the perception of satiety based on changing the apparent size of the food through real-time shape deformation. Protein-enriched diets are well known to initiate satiety effects (Penhoat et al., 2011). Proteins are widely cited in the literature as the macronutrient with the most potent satiety-inducing effect (Van Kleef, Van Trijp, Van Den Borne, & Zonder, 2012), attenuating the rise of hunger before the next meal. However, rapidly digested carbohydrate and insoluble fibre have often been found to be more satiating than protein in the early period after a meal. The consensus regarding the relative satiety values of fat and carbohydrates is less clear (Gerstein, WoodwardLopez, Evans, Kelsey, & Drewnowski, 2004). Of the latter,
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fibres look the most promising. Fat and carbohydrate satiety values tend to vary depending on whether they are measured in isolation or in foods; in addition, the impact of a food during digestion can obviously have a dramatic influence on the physiological outcome of the nutrients in vivo (Clegg et al., 2012). Proteins The mechanisms that explain protein-induced satiety are primarily nutrient-specific and consist mainly of coincidence, or synchronization, or a relationship with high amino acid concentrations (Veldhorst, Smeets, Soenen, Hochstenbach-Waelen, Hursel, et al., 2008). Given the normal protein intake range, meals averaging 20%e30% of energy from protein are high protein diets, when consumed in energy balance (Westerterp-Plantenga et al., 2006). Halton and Hu (2004) reviewed the literature on the effects of high protein foods and diets on satiety. At least in the short-term, they found convincing evidence that high-protein meals are more satiating than lower protein meals and affirmed that the mechanisms remain elusive. The late-satiating effects of protein were attributed in an early work to the substantial role of a high concentration of amino acids in the blood (Booth, Chase, & Campbell, 1970). More recently, it has been proposed that protein- and amino acid-induced satiety could be associated with the branch-chain amino acids found in complete proteins, which could be involved in the regulation of amino acid oxidation and gluconeogenesis (Aldrich et al., 2011). In addition, the good balance of indispensable amino acids usually obtained from food protein is sensed by the protein synthesizing machinery in specialized cells in the brain (Fromentin et al., 2012; Gietzen & Aja, 2012) which influences subsequent feeding-related responses. Other lines of research have pointed to the role of proteins in relation to satiety hormones (Westerterp-Plantenga, 2003). Research with different sources of protein is scarce but has been increasing since it was reported that different proteins cause different nutrient-related responses by anorexigenic hormones (Veldhorst et al., 2008). Consequently, in food formulation, proteins should not be considered generically. Appetite ratings did not display significant differences when a fish protein-rich meal was compared to an iso-energetic beef protein meal followed by reduced energy intake: Borzoei, Neovius, Barkeling, Teixeira-Pinto, and R€ ossner (2006) suggested serotonergic factors as well as a slower digestibility of fish proteins as a possible explanation of extended observations of fish protein enhanced satiety. Animal protein has been shown to produce higher energy expenditure than vegetable protein, resulting in reduced appetite (Westerterp-Plantenga, 2003). Anderson, Tecimer, Shah, and Zafar (2004) found that subjects who consumed whey protein had enhanced satiety relative to other proteins (egg-albumin and soy). Increased satiety response to whey compared with casein was found by Hall, Millward, Long, and Morgan (2003), implicating
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post-absorptive increases in plasma amino acids together with some hormones or peptides as potential mediators of that response. Anderson and Moore (2004) considered that this difference between casein and whey proteins could be attributed to clotting of the casein (unlike the soluble whey) in the acidic media of the stomach, giving it a longer exposure to gastric peptic hydrolysis. This adds a physicochemical property to the other mechanisms of action described above. From the food point of view, it should be pointed out that compliance is generally higher with higher-protein diets (Paddon-Jones et al., 2008). It is also important to note that the pleasantness of eating fish, for example, is not the same as that of eating meat, and that the type and quality of the fats or oils of the fish or meat used in the study also influence the feeding response. On the other hand, the versatility of milk proteins is greater than that of other types of protein from the point of view of predisposition and times when they are consumed. Similarly, many other factors influence a particular choice. Reformulating foods to increase the protein content can affect sensory properties. For instance, frankfurter-style sausages with double the protein of the normal formulation were perceived as more satiating during the first 90 min after the first meal and as less juicy, adhesive, harder and more granular than ones that contained less protein (Sivertsen, Ueland & Westad, 2010). Chewy texture, hardening with time and the appearance of unpleasant flavours have been reported in high-protein satiating bars formulated with whey proteins (Little, Gregory, & Robinson, 2009). Processing is another factor, because proteins normally require optimal pH control, protein concentration, heat treatment and evaluation of the risks from other ingredients (gums, minerals) in order to prevent flocculation, turbidity or sedimentation. However, proteins are a very varied group and some highly functional ones have been developed and optimized for different food systems. A number of satiety/satiation-related patents have taken out over the past ten years (Fig. 2). One of the principal approaches has consisted in adding proteins such as whey proteins, casein macropeptide, glycomacropeptides, whey protein hydrolysate, lactalbumin, sodium caseinate, intact pea and wheat protein, hydrolyzed yeast proteins, codfish, egg, or egg hydrolysate. Some patents mention the protein formulation’s potential for stimulating hunger controlrelated neurotransmitters or enzymes. Others use the fact that certain proteins have an unfolding transition in the stomach’s pH range, as in some cross-linked globular proteins that can form hydrogels. Fibre Food components appear in foods under many guises. This is particularly true for fibre, so it is difficult to isolate the satiating effect of the fibre itself from that of the other ingredients or the entire food. Even in prepared foods, adding different fibres or different quantities of the same fibre
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Fig. 2. Evolution of the number of patents on satiety/satiation since 1999.
causes variations in texture, appearance and flavour which, in turn, affect the perception of satiety. Equally, many foods with a naturally high fibre content are fortified with isolated fibres, making it difficult to distinguish between the effects of each. Consequently, here again an examination of the many works on fibre and satiety can lead to contradictory results. Several mechanisms that have been related to lower hunger/energy intake following the ingestion of dietary fibre (Howarth, Saltzman, & Roberts, 2001) are attributable to their unique chemical structure and such characteristic physical properties as bulk, viscosity, water holding capacity, absorption/binding, or fermentability (Burton-Freeman, 2000; Wanders et al., 2011), which generate satiety signals both pre- and post-absorptively. Oral processing and oral sensory exposure are very relevant influences on solid food intake (Zijlstra, Mars, Stafleu, & de Graaf, 2010). According to Slavin and Green (2007), fibre increases the force and time of chewing, which limits intake by promoting the secretion of saliva and gastric juice and results in an expansion of the stomach (see below). For this reason, the bulking and textural properties of fibre make it an attractive ingredient for enhancing satiation. Using fibre to add bulk also reduces the energy density of the diet. Increased gastric distension is another pre-absorptive factor with an impact on fibre-induced satiation. Fibre absorbs large amounts of water, adding bulk and weight and producing high-volume, low-energy-dense foods that trigger gastric and postgastric mechanisms (Norton, Anderson, & Hetherington, 2006; Rolls & Roe, 2002). The underlying hypothesis is that gastric capacity and sensitive mechanoreceptors to gastric distension are the key to regulating food intake (Burton-Freeman, 2000). Gastric distension during meal ingestion activates vagal afferents which send signals from the stomach to the brain and result in the perception of fullness and satiety (Wang et al., 2008).
In turn, the ability of several soluble fibres to form viscous mixtures in the gastrointestinal tract could induce feelings of fullness and promotes satiation (Slavin, 2005). Equally, several soluble fibres (such as pectin, alginate or low-temperature gelling methylcellulose) are able to form strong gels under gastric conditions (Knarr, Adden, Anderson, & H€ubner-Keese, 2012; Str€om et al., 2010). Satiating potential has also been reported for pHresponsive chitosan microparticle hydrogels (Pregent et al., 2012), or acid-sensitive mixed self-structuring biopolymers composed of low-methoxyl pectin and low-acyl gellan gum (Spyropoulos, Norton, & Norton, 2011). It has been hypothesized that viscous mixtures and/or gels decrease hunger due to distension of the gastric antrum and/or altered transport of nutrients to the small intestine in lumps, prolonging the intestinal phase of nutrient digestion and absorption and the time course of post-absorptive signals. On these lines, pectin, alginate, psyllium, barley, gum arabic and guar gum, among other hydrocolloids, have been reported to increase satiety (Nilsson, Ostman, Holst, & Bj€orck, 2008). Mattes and Rothacker (2001) critically examined the effect of viscosity on postprandial hunger, revealing a number of disputed results. The exact mechanism is still debated (Turgeon & Rioux, 2011) but it has been suggested that increased viscosity slows enzyme efficacy, and/or delays gastric emptying, and/or delays glucose transport to the absorption site, leading to lower postprandial glycaemic and insulinaemic responses (Makelainen et al., 2007). Important information (normally not given in the reported studies) that determines performance includes the different grades of the fibres, their degree of crosslinking, detailed chemical composition and the initiators required (Titoria, 2011). The dosage of the gums typically used to induce satiety may cause difficulties in food processing as well as sensory concerns: thick and slimy in solution or difficult to chew and tooth-packing in dry-form formulations (Paeschke & Aimutis, 2011). Conversely, soluble fibres with low viscosities such as soy show no significant effect on satiety (Simmons, Miller, Clinton, & Vodovotz, 2011). Not all fibres are equivalent in their effect because there are extreme variations not only in viscosity but also in solubility in the gut, fermentation profiles, and hormone responses (Lyly et al., 2009), which in turn could depend on the fibre particle size (Slavin, 2010). Some soluble low-viscosity fibres, such as oligofructose of several lengths (Hess, Birkett, Thomas & Slavin, 2011), resistant starch (Willis, Eldridge, Beiseigel, Thomas, & Slavin, 2009) or dextrins (Guerin-Deremaux et al., 2011), may induce satiety effects through hormonal and colonic responses (Parnell & Reimer, 2009) associated with the production and effects of short-chain fatty acids (Hess et al., 2011), such as modulation of the microbial ratios in the gut flora composition. From the point of view of satiety, whole grains can be viewed as the sum of their soluble and insoluble fibres.
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Oats, rye and barley contain about one-third soluble fibre and the rest is insoluble, wheat is lower in soluble fibre than most grains and rice contains almost no soluble fibre. The preparation, cooking and particle size of the grain structures may affect their accessibility and thus the metabolic response (Slavin, 2010). According to Mishra and Monro (2012), preservation of the native “primary” structure (“intactness”) can be used to modulate carbohydrate availability and digestion. The grain structure has been claimed to contribute satiety. Hlebowicz et al. (2008) reported satiating effects of whole-kernel wheat bread that they explained by increased antral distension after the ingestion of intact cereal kernels. Whole-grain rye breads and porridges also show a satiety-enhancing effect compared to an isocaloric sifted wheat bread (Isaksson et al. 2011). Additionally, the chewy, dense texture of whole grain products could be exploited to increase satiety sensations. The mucilage content of some hulls has also been reported to be proportional to their water-holding and fatabsorption capacity. However, the findings of Bodinham et al. (2011) do not support the epidemiological evidence that whole grains are beneficial in weight regulation because of their effects on satiety: the explanation lies rather in the tendency of those who eat high-wholegrain diets to consume high amounts of fruits and vegetables as well and to be non-smokers and physically active. Satiety/satiation-related patents taken out over the past ten years (Fig. 2) have considered the addition of fibre from different sources. Some of them are soluble fibres or hydrocolloids (methylcellulose, processed starches, alginate, pectin, low-methoxylated amidated pectin, etc.), or combinations of these, that form a stable gel in the stomach through a variety of mechanisms (cation-, temperature- or pH-mediated), or that swell or increase the viscosity of the stomach’s contents (guar gum, xanthan gum, hydrolyzed guar gum and glucomannan). Some patents claim to provide an optimized mixture of hydrocolloids or the optimum molecular pattern of a certain hydrocolloid. Others include insoluble fibres, whole grain products high in resistant starch, solubilized rice bran, flax seed mucilage, betaglucan-rich barley or oat bran concentrate, grain/seed sources of different soluble fibres, dextrins, polydextrose, or xylitol, which contribute a low glycaemic index or a range of satiety/satiation effects. Fat Fat has a significant impact on the energy density of common foodstuffs. Due to the close link between satiating foods and weight control, fat is not a particularly suitable macronutrient for formulating satiating foods since many consumers who look at the nutritional facts on food labels are seeking foods with a low fat content. Equally, adding fat to a food increases its palatability (enhancing mouth-feel, creaminess, and aroma), which could contribute to over-
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consumption. However, adding small quantities of fat could compensate for the unpalatability of formulations with a high fibre content, for instance. As for other macronutrients, it is difficult to compare diets with differing fat levels while maintaining the energy density, volume and palatability levels constant, so a large number of studies in this area have produced results that are contradictory or not really comparable. Various approaches have related fat and satiety. The physical state and spatial distribution of fat within the gastric lumen during digestion are critical factors influencing the rate of fat delivery to the small intestine. This, in turn, can be expected to affect the rate of fat absorption and metabolism and the signals between the gut and brain. One mechanism involves slowing down stomach empting, which gives the feeling of being full for longer. According to Marciani et al. (2009) it is necessary to stabilize the intragastric distribution of fat emulsions in relation to the gastric acid environment, which could have implications for the design of novel foods. A second mechanism is related to the metabolism of fats. The ileal brake theory, reviewed by Maljaars, Peters, Mela, & Masclee (2008), states that undigested and emulsified fat produces a number of signals that increase satiety and inhibit appetite, acting as a short-term control on food intake via negative feedback pathways and may promote secretion of satiety-enhancing gastrointestinal peptides. Based on this mechanism, a fractionated palm and oat oil in water emulsion product has appeared on the market for satiating purposes. This theory is largely unsupported according to Chan et al. (2012), nor has it been confirmed by studies that varied the thermal and shear processing conditions (Smit et al., 2011). However, it has obtained some confirmatory results (Diepvens, Steijns, Zuurendonk, & Westerterp-Plantenga, 2008). The role of physical and chemical properties in the satiating effect of fats is another controversial area. Different authors have obtained different results for the effects of fatty acid chain length or the degree of fatty acid saturation. The administration (oral or intraduodenal), the physical form of the fat (fat or emulsion), the fat type and the matrix (fat on its own or in a food) have also differed (Clegg et al., 2012). Over the last ten years, several fat formulations have been patented, normally oil in water emulsions with a variety of specifications for the fatty component (a lipid of which at least part is in a crystal form, milk fat or a milk fat analogue, long chain fatty acids, hydrogenated and unhydrogenated rapeseed oil, palm oil, triacylglycerols, fatty substance having a melting point of 43 C or higher, solid fat at ambient or body temperature, etc.). Others include a lipid matrix surrounded by a layer of phospholipids embedded with cross-linked proteins or, more curiously, a composition to be chewed and/or sucked containing one fatty acid and/or its derivatives.
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Digestible carbohydrates Digestible carbohydrates are a set of substances with very different compositions and structures. The site of carbohydrate breakdown in the gut, the rate and extent of breakdown (short-, medium-or long-chain carbohydrates), and the kinetics of absorption are key to understanding how they contribute to satiety (Elia & Cummings, 2007). The majority of mono- and disaccharides, together with maltodextrins and most starches, are hydrolyzed by pancreatic enzymes in the small intestine and at the epithelial surface. Generally speaking, native starch granules with a relatively high amylose content are more resistant to digestion. The vegetable source, the type of granular structure, and the degree of extraction and processing also influence starch digestion. The traditional method of assessing starch digestibility, both in vitro and in vivo, involves a measure of glucose release; however, the connection between blood glucose (GI) and the body’s mechanisms for controlling satiety is still under debate. Ingestion of high-GI food has increased hunger and lowered satiety in short-term human intervention studies, but appetite, hunger and satiety after the ingestion of foods with varying GIs have proved inconsistent in long-term human intervention studies. One of the reasons is presumably that the GI of each particular food is not reflected in that of the mixed meals as a whole. A clear relationship between GI, satietogenic leptin and appetitic ghrelin has not yet been established (Niwano et al., 2009). Conclusions A number of mechanisms by which the major food constituents deliver satiety sensations are known (and more will probably be known in future). It is important to make good use of this information to develop new, optimized food products. Researchers are encouraged to undertake studies that aim for a complete description (of both the properties and preparation) of the substances/foods used, which will make an enormous contribution to the development of new foods that are intended to deliver enhanced satiating properties. Reports on changes in colour, texture or appearance; degree of hydration/dissolution, or any change taking place between food preparation and consumption would be valuable tools for new developments. Obviously these changes come from or are related with the food matrix where the components are embedded, creating interactions that are worth knowing. Further understanding of these multiple influences on food intake may lead to strategies for controlling hunger while reducing energy intake. Whenever possible it is advisable to distinguish (unconfound) the effects of the constituents/ingredients from which the complete food product is produced, asking whether this component would behave in the same way in a different food matrix. High fibre and higher protein levels continue to be the best option for formulating foods to control hunger. As fibres do not have a uniform impact on satiety and work at
different levels, the type of fibre must be carefully considered. Proteins are somewhat more homogeneous in their satiating action but as with fibres, many questions about their effect on satiety and its assessment remain to be answered. Further research could consider combinations of ingredients that work at different stages, from the instant they are placed in the mouth until they reach the intestine. Knowing when, by how much and for which foods the appetite is suppressed after (and during) consumption of a specified normal amount of an “optimized” product, in comparison with the existing version in its usual combination with other foods, is a real goal for food developers. Finally, the authors want to point out that the satiety mechanisms of food constituents help to moderate intake but, importantly, that this depends on how the individual reacts to post-ingestional and other signals in interaction with the varieties of foods available at subsequent times. Consumers need to understand that in a particular pattern of eating, substances do not have fixed roles, allowing myriad influences to come into play. There is no such thing as a miracle product. Acknowledgements This work has been supported by the Spanish Ministry of the Economy and Competitiveness (MINECO) through Project AGL2012-36753-C02-01. Paula Varela is grateful for a MINECO Juan de la Cierva postdoctoral contract. Mary Georgina Hardinge assisted with the translation and corrected the English text. References Aldrich, N. D., Reicks, M. M., Sibley, S. D., Redmon, J. B., Thomas, W., & Raatz, S. K. (2011). Varying protein source and quantity do not significantly improve weight loss, fat loss, or satiety in reduced energy diets among midlife adults. Nutrition Research, 31, 104e112. Anderson, H., & Moore, S. E. (2004). Dietary proteins in the regulation of food intake and body weight in humans. Journal of Nutrition, 134, 974Se979S. Anderson, G. H., Tecimer, S. N., Shah, D., & Zafar, T. A. (2004). Protein source, quantity, and time of consumption determine the effect of proteins on short-term food intake in young men. Journal of Nutrition, 134, 3011e3015. Benelam, B. (2009). Satiation, satiety and their effects on eating behaviour. Nutrition Bulletin, 34, 126e173. Blundell, J. E., de Graaf, C., Finlayson, G., Halford, J. C. G., Hetherington, M., King, N., et al. (2009). Measuring food intake, hunger and satiation in the laboratory. In D. B. Allison, & M. L. Baskin (Eds.), Handbook of assessment methods for obesity and eating behaviour (2nd ed.). (pp. 283e326) Thousand Oaks: Sage Publications. Blundell, J. E., de Graaf, C., Hulshof, T., Jebb, S., Livingstone, B., Lluch, A., et al. (2010). Appetite control: methodological aspects of the evaluation of foods. Obesity Reviews, 11, 251e270. Bodinham, C. L., Katie, L., Hitchen, P., Youngman, J., Frost, G. S., & Robertson, M. D. (2011). Short-term effects of whole-grain wheat on appetite and food intake in healthy adults: a pilot study. British Journal of Nutrition, 106, 327e330.
S. Fiszman, P. Varela / Trends in Food Science & Technology 32 (2013) 43e50 Booth, D. A. (2009). Lines, dashed lines and “scale” ex-tricks. Objective measurements of appetite versus subjective tests of intake. Appetite, 53, 434e437. Booth, D. A. (2011). Weight is controlled by eating patterns, not by foods or drugs. Reply to comments on “Satiety. No way to slim”. Appetite, 57, 784e790. Booth, D. A., Chase, A., & Campbell, A. T. (1970). Relative effectiveness of protein in the late stages of appetite suppression in man. Physiology & Behavior, 5, 1299e1302. Borzoei, S., Neovius, M., Barkeling, B., Teixeira-Pinto, A., & R€ ossner, S. (2006). A comparison of effects of fish and beef protein on satiety in normal weight men. European Journal of Clinical Nutrition, 60, 897e902. Burton-Freeman, B. (2000). Dietary fiber and energy regulation. Journal of Nutrition, 130, 272Se275S. Chan, Y. K., Strik, C. M., Budgett, S. C., McGill, A. T., Proctor, J., & Poppitt, S. D. (2012). The emulsified lipid Fabuless (Olibra) does not decrease food intake but suppresses appetite when consumed with yoghurt but not alone or with solid foods: a food effect study. Physiology & Behavior, 105, 742e748. Clegg, M. E., Pratt, M., Markey, O., Shafat, A., Jeya, C., & Henry, K. (2012). Addition of different fats to a carbohydrate food: impact on gastric emptying, glycaemic and satiety responses and comparison with in vitro digestion. Food Research International, 48, 91e97. De Graaf, C., Blom, W., Smeets, A. J., Stafleu, A., & Hendriks, H. (2004). Biomarkers of satiation and satiety. American Journal of Clinical Nutrition, 79, 946e961. Diepvens, K., Steijns, J., Zuurendonk, P., & WesterterpPlantenga, M. S. (2008). Short-term effects of a novel fat emulsion on appetite and food intake. Physiology & Behavior, 95, 114e117. EFSA European Food Safety Authority. (2012). Panel on Dietetic Products, Nutrition and Allergies. Guidance on the scientific requirements for health claims related to appetite ratings, weight management, and blood glucose concentrations. EFSA Journal, 10(3), 2604. Elia, M., & Cummings, J. H. (2007). Physiological aspects of energy metabolism and gastrointestinal effects of carbohydrates. European Journal of Clinical Nutrition, 61(Suppl. 1), S40eS74. Espagnac, C., Laboure, H., Delarue, J., & Gurviez, P. (2012). Could implicit measurements and facial expressions be used to assess satiation?. In A sense of inspiration. 5th European Conference on Sensory and Consumer Research, Bern 9e12 September, 2012 Bern: Elsevier, Conference Abstracts. Fromentin, G., Darcel, N., Chaumontet, C., Marsset-Baglieri, A., Nadkarni, N., & Tome, D. (2012). Peripheral and central mechanisms involved in the control of food intake by dietary amino acids and proteins. Nutrition Research Reviews, 25, 29e39. Gatta-Cherifi, B. (2012). Neurobiology of food intake. Medecine des Maladies Metaboliques, 6, 115e119. Gerstein, D. E., Woodward-Lopez, G., Evans, A. E., Kelsey, K., & Drewnowski, A. (2004). Clarifying concepts about macronutrients’ effects on satiation and satiety. Journal of the American Dietetic Association, 104, 1151e1153. Gietzen, D. W., & Aja, S. M. (2012). The brain’s response to an essential amino acid-deficient diet and the circuitous route to a better meal. Molecular Neurobiology, 46, 332e348. Gu erin-Deremaux, L., Pochat, M., Reifer, C., Wils, D., Cho, S., & Miller, L. E. (2011). The soluble fibre nutriose induces a dosedependent beneficial impact on satiety over time in humans. Nutrition Research, 31, 665e672. Halford, J. C. G., & Harrold, J. A. (2012). Satiety-enhancing products for appetite control: science and regulation of functional foods for weight management. Proceedings of the Nutrition Society, 71, 350e362. Hall, W. L., Millward, D. J., Long, S. J., & Morgan, L. M. (2003). Casein and whey exert different effects on plasma amino acid
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healthy subjects improves glucose tolerance, lowers inflammatory markers, and increases satiety after a subsequent standardized breakfast. Journal of Nutrition, 138, 732e739. Niwano, Y., Adachi, T., Kashimura, J., Sakata, T., Sasaki, H., Sekine, K., et al. (2009). Is glycemic index of food a feasible predictor of appetite, hunger, and satiety? Journal of Nutritional Science and Vitaminology, 55, 201e207. Norton, G. N. M., Anderson, A. S., & Hetherington, M. M. (2006). Volume and variety: relative effects on food intake. Physiology & Behavior, 87, 714e722. Paddon-Jones, D., Westman, E., Mattes, R. D., Wolfe, R. R., Astrup, A., & Westerterp-Plantenga, M. (2008). Protein, weight management, and satiety. American Journal of Clinical Nutrition, 87, 1558Se1561S. Paeschke, T. M., & Aimutis, W. R. (2011). Formulating for satiety with hydrocolloids. Food Technology, 65(3), 24e35. Parnell, J. A., & Reimer, R. A. (2009). Weight loss during oligofructose supplementation is associated with decreased ghrelin and increased peptide YY in overweight and obese adults. American Journal of Clinical Nutrition, 89, 1751e1759. Penhoat, A., Mutel, E., Amigo-Correig, M., Pillot, B., Stefanutti, A., Rajas, F., et al. (2011). Protein-induced satiety is abolished in the absence of intestinal gluconeogenesis. Physiology & Behavior, 105, 89e93. Pregent, S., Hoad, C. L., Ciampi, E., Kirkland, M., Cox, E. F., Marciani, L., et al. (2012). Investigation of the behaviour of chitosan microparticles as pH responsive hydrogels in the gastrointestinal tract using magnetic resonance imaging. Food Hydrocolloids, 26, 187e196. Rolls, B. J., Bell, E. A., & Waugh, B. A. (2000). Increasing the volume of a food by incorporating air affects satiety in men. American Journal of Clinical Nutrition, 72, 361e368. Rolls, B. J., & Roe, L. S. (2002). Effect of the volume of liquid food infused intragastrically on satiety in women. Physiology & Behavior, 76, 623e631. Shill, J., Mavoa, H., Allender, S., Lawrence, M., Sacks, G., Peeters, A., et al. (2012). Government regulation to promote healthy food environments e a view from inside state governments. Obesity Reviews, 13, 162e173. Simmons, A. L., Miller, C. K., Clinton, S. K., & Vodovotz, Y. (2011). A comparison of satiety, glycemic index, and insulinemic index of wheat-derived soft pretzels with or without soy. Food & Function, 2, 678e683. Sivertsen, H. K., Ueland, Ø., & Westad, F. (2010). Development of satiating and palatable high-protein meat products by using experimental design in food technology. Food and Nutrition Research, 54, Article Number 5114. Slavin, J. L. (2005). Dietary fiber and body weight. Nutrition, 21, 411e418. Slavin, J. L. (2010). Whole grains and digestive health. Cereal Chemistry, 87, 292e296. Slavin, J. L., & Green, H. (2007). Dietary fibre and satiety. Nutrition Bulletin, 32(Suppl. 1), 32e42. Smit, H. J., Keenan, E., Kovacs, E. M., Wiseman, S. A., Peters, H. P. F., Mela, D. J., et al. (2011). No efficacy of processed Fabuless
(Olibra) in suppressing appetite or food intake. European Journal of Clinical Nutrition, 65, 81e86. Spyropoulos, F., Norton, A. B., & Norton, I. T. (2011). Self-structuring foods based on acid-sensitive mixed biopolymer to impact on satiety. Procedia Food Science, 1, 1487e1493. Str€ om, A., Boers, H. M., Koppert, R., Melnikov, S. M., Wiseman, S., & Peters, H. P. F. (2010). Physico-chemical properties of hydrocolloids determine their appetite effects. In P. A. Williams, & G. O. Phillips (Eds.). Gums and stabilisers for the food industry 15, (pp. 341e355). Cambridge: RSC Publishing. Stubbs, R. J., Hughes, D. A., Johnstone, A. M., Rowley, E., Reid, C., Elia, M., et al. (2000). The use of visual analogue scales to assess motivation to eat in human subjects: a review of their reliability and validity with an evaluation of new hand-held computerized systems for temporal tracking of appetite ratings. British Journal of Nutrition, 84, 405e415. Titoria, P. M. (2011). Hydrocolloids for satiety. Food Industry Hi-Tech, 22(6), 54e56. Turgeon, S. L., & Rioux, L.-E. (2011). Food matrix impact on macronutrients nutritional properties. Food Hydrocolloids, 25, 1915e1924. Van Kleef, E., Van Trijp, J. C. M., Van Den Borne, J. J. G. C., & Zonder, C. (2012). Successful development of satiety enhancing food products: towards a multidisciplinary agenda of research challenges. Critical Reviews in Food Science and Nutrition, 52, 611e628. Veldhorst, M., Smeets, A., Soenen, S., Hochstenbach-Waelen, A., Hursel, R., Diepvens, K., et al. (2008). Protein-induced satiety: effects and mechanisms of different proteins. Physiology & Behavior, 94, 300e307. Wanders, A. J., van den Borne, J. J. G. C., de Graaf, C., Hulshof, T., Jonathan, M. C., Kristensen, M., et al. (2011). Effects of dietary fibre on subjective appetite, energy intake and body weight: a systematic review of randomized controlled trials. Obesity Reviews, 12, 724e739. Wang, G.-J., Tomasi, D., Backus, W., Wang, R., Telang, F., Geliebter, A., et al. (2008). Gastric distention activates satiety circuitry in the human brain. Neuroimage, 39, 1824e1831. Westerterp-Plantenga, M. S. (2003). The significance of protein in food intake and body weight regulation. Current Opinion in Clinical Nutrition and Metabolic Care, 6, 635e638. Westerterp-Plantenga, M. S., Luscombe-Marsh, N., Lejeune, M. P. G. M., Diepvens, K., Nieuwenhuizen, A., Engelen, M. P. K. J., et al. (2006). Dietary protein, metabolism, and body-weight regulation: dose-response effects. International Journal of Obesity, 30, S16eS23. Willis, H. J., Eldridge, A. L., Beiseigel, J., Thomas, W., & Slavin, J. L. (2009). Greater satiety response with resistant starch and corn bran in human subjects. Nutrition Research, 29, 100e105. Woods, S. C., & Langhans, W. (2012). Inconsistencies in the assessment of food intake. American Journal of PhysiologyEndocrinology and Metabolism, 303, E1408eE1418. Zijlstra, N., Mars, M., Stafleu, A., & de Graaf, C. (2010). The effect of texture differences on satiation in 3 pairs of solid foods. Appetite, 55, 490e497.
Review
The satiating mechanisms of major food constituents e An aid to rational food design Susana Fiszman* and Paula Varela Instituto de Agroquımica y Tecnologıa de Alimentos (IATA-CSIC), Agustın Escardino 7, 46980 Paterna (Valencia), Spain (Tel.: D34 963900022; fax: D34 963636301; e-mails: [email protected]; pvarela@ iata.csic.es) The worldwide rise in the prevalence of excess weight lends great interest to preventive measures aimed at satiety/satiation. Human body-weight regulation is complex and is rooted in a superstructure that takes in sensory signals from food, neurohormonal signals from the digestive tract and signals from the body’s energy reserves. Recent research has contributed more insight into the satiating mechanisms of constituents/ingredients for new food design. Knowing why to select them, what they contribute to the food’s physical and sensory properties and how they are integrated into the food matrix will provide suitable tools for designing satiating foods.
Introduction The worldwide rise in the prevalence of excess weight and obesity that affects a high percentage of population lends great interest to preventive measures aimed at weight control and satiety. The western world produces obesitygenerating environments with an abundance of (possibly) not very healthy products (Shill et al., 2012) with a high energy density or an unbalanced nutritional profile. * Corresponding author. 0924-2244/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tifs.2013.05.006
The great advantage of formulating satiating foods is the immediate benefit of feeling full or not feeling hungry for a longer time, instead of a promise that requires sacrifices or a strong will before the benefits are felt. The type of food formulated and the way the satietypromoting ingredients are selected have direct implications for the way the body processes them, and the consumer’s satisfaction has implications for the perception of satiety as an additional value. It is worth noting that these products do not in themselves contribute to weight loss, although a given portion of them can work with adequate amounts of nutritious food to reduce the hunger pangs that occur at a certain time interval after their consumption (Booth, 2011). The quest for a magic ingredient has passed into history. However, the many mechanisms that have been described for each macronutrient and the levels on which they act, together with their diversity of structures and chemical composition, evidently make it possible to design foods that can act on more than one level and achieve overall acceptability. It is difficult to (re)formulate food products to enhance their satiating capacities because the constituents can themselves influence energy density, palatability, texture and a number of other factors that are involved in feeding behaviour. Some of the effects overlap, to an uncertain degree, emphasizing the need for integrative research. A radical change in diet evidently cannot and should not be recommended, but a feasible lifestyle adaptation to a moderately higher-protein, higher-fibre, controlledenergy diet should be possible (Hill, 2006). There is a need for healthier low-energy, low-fat, energy-dilute foods that are affordable, attractive and convenient, and e importantly e as tasty and gratifying as the unhealthier items they are intended to replace (Halford & Harrold, 2012). These food items will produce consumer satisfaction with their filling effects at particular times when the food product is eaten under specific conditions and could encourage healthy dietary habits while used in that way to prevent weight gain. This paper will focus on the satiating mechanisms of macronutrients and how they can contribute to the design of foods with enhanced satiating capacity. Particular interest will be paid to the important role of the food matrix in which the substance/ingredient is embedded.
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Appetite, satiation and satiety To understand the role of appetite in free individuals, the individual and combined environmental, psychological, and physiologic conditions that generate, modulate, and terminate appetite sensations would need to be quantified (Mattes, Hollis, Hayes, & Stunkard, 2005). Appetite is the motive that leads a person to seek food, choose it and eat it (De Graaf, Blom, Smeets, Stafleu, & Hendriks, 2004). Satiety is a state of suppression of appetite, while satiation moves into a deeper state of satiety. A vast amount of literature has reported the effects of some types of nutritional and compositional manipulation on appetite, observed through clinical trials involving within- and inter-meal measurements of the sensation of fullness, following the widely extended notion that tightly associates ‘satiety’ and ‘satiation’ to times between meals and within meals respectively (Blundell et al., 2009, 2010). These human intervention studies normally use a preload design, employing methods such as the so-called visual analogue scales (VAS) (EFSA, 2012), in which subjects rate their level of appetite/hunger/satiety on line scales or structured scales. Stubbs et al. (2000) reported that these kinds of rating are best used in conjunction with other measures (e.g. feeding behaviour, changes in plasma metabolites) (De Graaf et al., 2004; Lemmens, Martens, Kester, & Westerterp-Plantenga, 2011). The use of VAS has been criticized. In the opinion of some researchers, the amount of a test meal that a person eats is a subjective outcome accumulated from many choices of another mouthful, each subjected to several rapidly changing influences, so measurements of their effects on the apparent willingness to eat the available food at each moment during a meal would be needed to explain the amount consumed (Booth, 2009). According to this current of opinion, suppression of the appetite for portions of specific foods through the effects of eating these and other foods rises and falls from start to end of a meal (confounding the measurements of meal size), and over the interval until the next eating event, and involves separate mechanisms, many of which may be operative to some extent from during a meal until after it. According to Woods and Langhans (2012), failures to replicate the effects of compounds on food intake are commonplace because these effects are subject to numerous influences that can render them completely ineffective at times. Non-declarative methods such as facial expression (evaluated by filming the consumers while eating) have recently been reported as a new tool for satiation assessment (Espagnac, Laboure, Delarue, & Gurviez, 2012). Studies on satiating food. Major food constituents Because of improved knowledge of the neurobiological mechanisms of satiation (Gatta-Cherifi, 2012) and new and better assessment tools, the effects of different foods on appetite have been increasingly studied for many years now (Fig. 1).
Fig. 1. Evolution of the number of scientific papers on satiety/satiation since 1990.
The effect that a type of component/ingredient can have on satiety depends both on its physical properties when eaten and on its physiological effects in the gut (Benelam, 2009). It is remarkable how little information on the preparation of the foods administered in the clinical trials is generally found in the literature (mainly in nutrition-related journals). The dosage of the substance added to the food is mentioned, but the physical properties of the food in relation to the control or placebo are almost never measured or reported. Another factor that is not elucidated is the structure of the food. Physiological responses depend not only on the nutrient composition and energy content of the food but also on its structure, spatial distribution and particle size and shape, which in turn determine its texture, perception of moisture, etc., and the type and speed of digestion (Lundin, Golding, & Wooster, 2008). The volume of a food eaten as a preload can also affect satiety by introducing air, for example, quite apart from changes in energy density (Rolls, Bell, & Waugh, 2000). Further understanding of these multiple influences on food intake may lead to strategies for controlling hunger while reducing energy intake. Narumi, Ban, Kajinami, Tanikawa, and Hirose (2012) propose a method for modifying the perception of satiety based on changing the apparent size of the food through real-time shape deformation. Protein-enriched diets are well known to initiate satiety effects (Penhoat et al., 2011). Proteins are widely cited in the literature as the macronutrient with the most potent satiety-inducing effect (Van Kleef, Van Trijp, Van Den Borne, & Zonder, 2012), attenuating the rise of hunger before the next meal. However, rapidly digested carbohydrate and insoluble fibre have often been found to be more satiating than protein in the early period after a meal. The consensus regarding the relative satiety values of fat and carbohydrates is less clear (Gerstein, WoodwardLopez, Evans, Kelsey, & Drewnowski, 2004). Of the latter,
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fibres look the most promising. Fat and carbohydrate satiety values tend to vary depending on whether they are measured in isolation or in foods; in addition, the impact of a food during digestion can obviously have a dramatic influence on the physiological outcome of the nutrients in vivo (Clegg et al., 2012). Proteins The mechanisms that explain protein-induced satiety are primarily nutrient-specific and consist mainly of coincidence, or synchronization, or a relationship with high amino acid concentrations (Veldhorst, Smeets, Soenen, Hochstenbach-Waelen, Hursel, et al., 2008). Given the normal protein intake range, meals averaging 20%e30% of energy from protein are high protein diets, when consumed in energy balance (Westerterp-Plantenga et al., 2006). Halton and Hu (2004) reviewed the literature on the effects of high protein foods and diets on satiety. At least in the short-term, they found convincing evidence that high-protein meals are more satiating than lower protein meals and affirmed that the mechanisms remain elusive. The late-satiating effects of protein were attributed in an early work to the substantial role of a high concentration of amino acids in the blood (Booth, Chase, & Campbell, 1970). More recently, it has been proposed that protein- and amino acid-induced satiety could be associated with the branch-chain amino acids found in complete proteins, which could be involved in the regulation of amino acid oxidation and gluconeogenesis (Aldrich et al., 2011). In addition, the good balance of indispensable amino acids usually obtained from food protein is sensed by the protein synthesizing machinery in specialized cells in the brain (Fromentin et al., 2012; Gietzen & Aja, 2012) which influences subsequent feeding-related responses. Other lines of research have pointed to the role of proteins in relation to satiety hormones (Westerterp-Plantenga, 2003). Research with different sources of protein is scarce but has been increasing since it was reported that different proteins cause different nutrient-related responses by anorexigenic hormones (Veldhorst et al., 2008). Consequently, in food formulation, proteins should not be considered generically. Appetite ratings did not display significant differences when a fish protein-rich meal was compared to an iso-energetic beef protein meal followed by reduced energy intake: Borzoei, Neovius, Barkeling, Teixeira-Pinto, and R€ ossner (2006) suggested serotonergic factors as well as a slower digestibility of fish proteins as a possible explanation of extended observations of fish protein enhanced satiety. Animal protein has been shown to produce higher energy expenditure than vegetable protein, resulting in reduced appetite (Westerterp-Plantenga, 2003). Anderson, Tecimer, Shah, and Zafar (2004) found that subjects who consumed whey protein had enhanced satiety relative to other proteins (egg-albumin and soy). Increased satiety response to whey compared with casein was found by Hall, Millward, Long, and Morgan (2003), implicating
45
post-absorptive increases in plasma amino acids together with some hormones or peptides as potential mediators of that response. Anderson and Moore (2004) considered that this difference between casein and whey proteins could be attributed to clotting of the casein (unlike the soluble whey) in the acidic media of the stomach, giving it a longer exposure to gastric peptic hydrolysis. This adds a physicochemical property to the other mechanisms of action described above. From the food point of view, it should be pointed out that compliance is generally higher with higher-protein diets (Paddon-Jones et al., 2008). It is also important to note that the pleasantness of eating fish, for example, is not the same as that of eating meat, and that the type and quality of the fats or oils of the fish or meat used in the study also influence the feeding response. On the other hand, the versatility of milk proteins is greater than that of other types of protein from the point of view of predisposition and times when they are consumed. Similarly, many other factors influence a particular choice. Reformulating foods to increase the protein content can affect sensory properties. For instance, frankfurter-style sausages with double the protein of the normal formulation were perceived as more satiating during the first 90 min after the first meal and as less juicy, adhesive, harder and more granular than ones that contained less protein (Sivertsen, Ueland & Westad, 2010). Chewy texture, hardening with time and the appearance of unpleasant flavours have been reported in high-protein satiating bars formulated with whey proteins (Little, Gregory, & Robinson, 2009). Processing is another factor, because proteins normally require optimal pH control, protein concentration, heat treatment and evaluation of the risks from other ingredients (gums, minerals) in order to prevent flocculation, turbidity or sedimentation. However, proteins are a very varied group and some highly functional ones have been developed and optimized for different food systems. A number of satiety/satiation-related patents have taken out over the past ten years (Fig. 2). One of the principal approaches has consisted in adding proteins such as whey proteins, casein macropeptide, glycomacropeptides, whey protein hydrolysate, lactalbumin, sodium caseinate, intact pea and wheat protein, hydrolyzed yeast proteins, codfish, egg, or egg hydrolysate. Some patents mention the protein formulation’s potential for stimulating hunger controlrelated neurotransmitters or enzymes. Others use the fact that certain proteins have an unfolding transition in the stomach’s pH range, as in some cross-linked globular proteins that can form hydrogels. Fibre Food components appear in foods under many guises. This is particularly true for fibre, so it is difficult to isolate the satiating effect of the fibre itself from that of the other ingredients or the entire food. Even in prepared foods, adding different fibres or different quantities of the same fibre
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Fig. 2. Evolution of the number of patents on satiety/satiation since 1999.
causes variations in texture, appearance and flavour which, in turn, affect the perception of satiety. Equally, many foods with a naturally high fibre content are fortified with isolated fibres, making it difficult to distinguish between the effects of each. Consequently, here again an examination of the many works on fibre and satiety can lead to contradictory results. Several mechanisms that have been related to lower hunger/energy intake following the ingestion of dietary fibre (Howarth, Saltzman, & Roberts, 2001) are attributable to their unique chemical structure and such characteristic physical properties as bulk, viscosity, water holding capacity, absorption/binding, or fermentability (Burton-Freeman, 2000; Wanders et al., 2011), which generate satiety signals both pre- and post-absorptively. Oral processing and oral sensory exposure are very relevant influences on solid food intake (Zijlstra, Mars, Stafleu, & de Graaf, 2010). According to Slavin and Green (2007), fibre increases the force and time of chewing, which limits intake by promoting the secretion of saliva and gastric juice and results in an expansion of the stomach (see below). For this reason, the bulking and textural properties of fibre make it an attractive ingredient for enhancing satiation. Using fibre to add bulk also reduces the energy density of the diet. Increased gastric distension is another pre-absorptive factor with an impact on fibre-induced satiation. Fibre absorbs large amounts of water, adding bulk and weight and producing high-volume, low-energy-dense foods that trigger gastric and postgastric mechanisms (Norton, Anderson, & Hetherington, 2006; Rolls & Roe, 2002). The underlying hypothesis is that gastric capacity and sensitive mechanoreceptors to gastric distension are the key to regulating food intake (Burton-Freeman, 2000). Gastric distension during meal ingestion activates vagal afferents which send signals from the stomach to the brain and result in the perception of fullness and satiety (Wang et al., 2008).
In turn, the ability of several soluble fibres to form viscous mixtures in the gastrointestinal tract could induce feelings of fullness and promotes satiation (Slavin, 2005). Equally, several soluble fibres (such as pectin, alginate or low-temperature gelling methylcellulose) are able to form strong gels under gastric conditions (Knarr, Adden, Anderson, & H€ubner-Keese, 2012; Str€om et al., 2010). Satiating potential has also been reported for pHresponsive chitosan microparticle hydrogels (Pregent et al., 2012), or acid-sensitive mixed self-structuring biopolymers composed of low-methoxyl pectin and low-acyl gellan gum (Spyropoulos, Norton, & Norton, 2011). It has been hypothesized that viscous mixtures and/or gels decrease hunger due to distension of the gastric antrum and/or altered transport of nutrients to the small intestine in lumps, prolonging the intestinal phase of nutrient digestion and absorption and the time course of post-absorptive signals. On these lines, pectin, alginate, psyllium, barley, gum arabic and guar gum, among other hydrocolloids, have been reported to increase satiety (Nilsson, Ostman, Holst, & Bj€orck, 2008). Mattes and Rothacker (2001) critically examined the effect of viscosity on postprandial hunger, revealing a number of disputed results. The exact mechanism is still debated (Turgeon & Rioux, 2011) but it has been suggested that increased viscosity slows enzyme efficacy, and/or delays gastric emptying, and/or delays glucose transport to the absorption site, leading to lower postprandial glycaemic and insulinaemic responses (Makelainen et al., 2007). Important information (normally not given in the reported studies) that determines performance includes the different grades of the fibres, their degree of crosslinking, detailed chemical composition and the initiators required (Titoria, 2011). The dosage of the gums typically used to induce satiety may cause difficulties in food processing as well as sensory concerns: thick and slimy in solution or difficult to chew and tooth-packing in dry-form formulations (Paeschke & Aimutis, 2011). Conversely, soluble fibres with low viscosities such as soy show no significant effect on satiety (Simmons, Miller, Clinton, & Vodovotz, 2011). Not all fibres are equivalent in their effect because there are extreme variations not only in viscosity but also in solubility in the gut, fermentation profiles, and hormone responses (Lyly et al., 2009), which in turn could depend on the fibre particle size (Slavin, 2010). Some soluble low-viscosity fibres, such as oligofructose of several lengths (Hess, Birkett, Thomas & Slavin, 2011), resistant starch (Willis, Eldridge, Beiseigel, Thomas, & Slavin, 2009) or dextrins (Guerin-Deremaux et al., 2011), may induce satiety effects through hormonal and colonic responses (Parnell & Reimer, 2009) associated with the production and effects of short-chain fatty acids (Hess et al., 2011), such as modulation of the microbial ratios in the gut flora composition. From the point of view of satiety, whole grains can be viewed as the sum of their soluble and insoluble fibres.
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Oats, rye and barley contain about one-third soluble fibre and the rest is insoluble, wheat is lower in soluble fibre than most grains and rice contains almost no soluble fibre. The preparation, cooking and particle size of the grain structures may affect their accessibility and thus the metabolic response (Slavin, 2010). According to Mishra and Monro (2012), preservation of the native “primary” structure (“intactness”) can be used to modulate carbohydrate availability and digestion. The grain structure has been claimed to contribute satiety. Hlebowicz et al. (2008) reported satiating effects of whole-kernel wheat bread that they explained by increased antral distension after the ingestion of intact cereal kernels. Whole-grain rye breads and porridges also show a satiety-enhancing effect compared to an isocaloric sifted wheat bread (Isaksson et al. 2011). Additionally, the chewy, dense texture of whole grain products could be exploited to increase satiety sensations. The mucilage content of some hulls has also been reported to be proportional to their water-holding and fatabsorption capacity. However, the findings of Bodinham et al. (2011) do not support the epidemiological evidence that whole grains are beneficial in weight regulation because of their effects on satiety: the explanation lies rather in the tendency of those who eat high-wholegrain diets to consume high amounts of fruits and vegetables as well and to be non-smokers and physically active. Satiety/satiation-related patents taken out over the past ten years (Fig. 2) have considered the addition of fibre from different sources. Some of them are soluble fibres or hydrocolloids (methylcellulose, processed starches, alginate, pectin, low-methoxylated amidated pectin, etc.), or combinations of these, that form a stable gel in the stomach through a variety of mechanisms (cation-, temperature- or pH-mediated), or that swell or increase the viscosity of the stomach’s contents (guar gum, xanthan gum, hydrolyzed guar gum and glucomannan). Some patents claim to provide an optimized mixture of hydrocolloids or the optimum molecular pattern of a certain hydrocolloid. Others include insoluble fibres, whole grain products high in resistant starch, solubilized rice bran, flax seed mucilage, betaglucan-rich barley or oat bran concentrate, grain/seed sources of different soluble fibres, dextrins, polydextrose, or xylitol, which contribute a low glycaemic index or a range of satiety/satiation effects. Fat Fat has a significant impact on the energy density of common foodstuffs. Due to the close link between satiating foods and weight control, fat is not a particularly suitable macronutrient for formulating satiating foods since many consumers who look at the nutritional facts on food labels are seeking foods with a low fat content. Equally, adding fat to a food increases its palatability (enhancing mouth-feel, creaminess, and aroma), which could contribute to over-
47
consumption. However, adding small quantities of fat could compensate for the unpalatability of formulations with a high fibre content, for instance. As for other macronutrients, it is difficult to compare diets with differing fat levels while maintaining the energy density, volume and palatability levels constant, so a large number of studies in this area have produced results that are contradictory or not really comparable. Various approaches have related fat and satiety. The physical state and spatial distribution of fat within the gastric lumen during digestion are critical factors influencing the rate of fat delivery to the small intestine. This, in turn, can be expected to affect the rate of fat absorption and metabolism and the signals between the gut and brain. One mechanism involves slowing down stomach empting, which gives the feeling of being full for longer. According to Marciani et al. (2009) it is necessary to stabilize the intragastric distribution of fat emulsions in relation to the gastric acid environment, which could have implications for the design of novel foods. A second mechanism is related to the metabolism of fats. The ileal brake theory, reviewed by Maljaars, Peters, Mela, & Masclee (2008), states that undigested and emulsified fat produces a number of signals that increase satiety and inhibit appetite, acting as a short-term control on food intake via negative feedback pathways and may promote secretion of satiety-enhancing gastrointestinal peptides. Based on this mechanism, a fractionated palm and oat oil in water emulsion product has appeared on the market for satiating purposes. This theory is largely unsupported according to Chan et al. (2012), nor has it been confirmed by studies that varied the thermal and shear processing conditions (Smit et al., 2011). However, it has obtained some confirmatory results (Diepvens, Steijns, Zuurendonk, & Westerterp-Plantenga, 2008). The role of physical and chemical properties in the satiating effect of fats is another controversial area. Different authors have obtained different results for the effects of fatty acid chain length or the degree of fatty acid saturation. The administration (oral or intraduodenal), the physical form of the fat (fat or emulsion), the fat type and the matrix (fat on its own or in a food) have also differed (Clegg et al., 2012). Over the last ten years, several fat formulations have been patented, normally oil in water emulsions with a variety of specifications for the fatty component (a lipid of which at least part is in a crystal form, milk fat or a milk fat analogue, long chain fatty acids, hydrogenated and unhydrogenated rapeseed oil, palm oil, triacylglycerols, fatty substance having a melting point of 43 C or higher, solid fat at ambient or body temperature, etc.). Others include a lipid matrix surrounded by a layer of phospholipids embedded with cross-linked proteins or, more curiously, a composition to be chewed and/or sucked containing one fatty acid and/or its derivatives.
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Digestible carbohydrates Digestible carbohydrates are a set of substances with very different compositions and structures. The site of carbohydrate breakdown in the gut, the rate and extent of breakdown (short-, medium-or long-chain carbohydrates), and the kinetics of absorption are key to understanding how they contribute to satiety (Elia & Cummings, 2007). The majority of mono- and disaccharides, together with maltodextrins and most starches, are hydrolyzed by pancreatic enzymes in the small intestine and at the epithelial surface. Generally speaking, native starch granules with a relatively high amylose content are more resistant to digestion. The vegetable source, the type of granular structure, and the degree of extraction and processing also influence starch digestion. The traditional method of assessing starch digestibility, both in vitro and in vivo, involves a measure of glucose release; however, the connection between blood glucose (GI) and the body’s mechanisms for controlling satiety is still under debate. Ingestion of high-GI food has increased hunger and lowered satiety in short-term human intervention studies, but appetite, hunger and satiety after the ingestion of foods with varying GIs have proved inconsistent in long-term human intervention studies. One of the reasons is presumably that the GI of each particular food is not reflected in that of the mixed meals as a whole. A clear relationship between GI, satietogenic leptin and appetitic ghrelin has not yet been established (Niwano et al., 2009). Conclusions A number of mechanisms by which the major food constituents deliver satiety sensations are known (and more will probably be known in future). It is important to make good use of this information to develop new, optimized food products. Researchers are encouraged to undertake studies that aim for a complete description (of both the properties and preparation) of the substances/foods used, which will make an enormous contribution to the development of new foods that are intended to deliver enhanced satiating properties. Reports on changes in colour, texture or appearance; degree of hydration/dissolution, or any change taking place between food preparation and consumption would be valuable tools for new developments. Obviously these changes come from or are related with the food matrix where the components are embedded, creating interactions that are worth knowing. Further understanding of these multiple influences on food intake may lead to strategies for controlling hunger while reducing energy intake. Whenever possible it is advisable to distinguish (unconfound) the effects of the constituents/ingredients from which the complete food product is produced, asking whether this component would behave in the same way in a different food matrix. High fibre and higher protein levels continue to be the best option for formulating foods to control hunger. As fibres do not have a uniform impact on satiety and work at
different levels, the type of fibre must be carefully considered. Proteins are somewhat more homogeneous in their satiating action but as with fibres, many questions about their effect on satiety and its assessment remain to be answered. Further research could consider combinations of ingredients that work at different stages, from the instant they are placed in the mouth until they reach the intestine. Knowing when, by how much and for which foods the appetite is suppressed after (and during) consumption of a specified normal amount of an “optimized” product, in comparison with the existing version in its usual combination with other foods, is a real goal for food developers. Finally, the authors want to point out that the satiety mechanisms of food constituents help to moderate intake but, importantly, that this depends on how the individual reacts to post-ingestional and other signals in interaction with the varieties of foods available at subsequent times. Consumers need to understand that in a particular pattern of eating, substances do not have fixed roles, allowing myriad influences to come into play. There is no such thing as a miracle product. Acknowledgements This work has been supported by the Spanish Ministry of the Economy and Competitiveness (MINECO) through Project AGL2012-36753-C02-01. Paula Varela is grateful for a MINECO Juan de la Cierva postdoctoral contract. Mary Georgina Hardinge assisted with the translation and corrected the English text. References Aldrich, N. D., Reicks, M. M., Sibley, S. D., Redmon, J. B., Thomas, W., & Raatz, S. K. (2011). Varying protein source and quantity do not significantly improve weight loss, fat loss, or satiety in reduced energy diets among midlife adults. Nutrition Research, 31, 104e112. Anderson, H., & Moore, S. E. (2004). Dietary proteins in the regulation of food intake and body weight in humans. Journal of Nutrition, 134, 974Se979S. Anderson, G. H., Tecimer, S. N., Shah, D., & Zafar, T. A. (2004). Protein source, quantity, and time of consumption determine the effect of proteins on short-term food intake in young men. Journal of Nutrition, 134, 3011e3015. Benelam, B. (2009). Satiation, satiety and their effects on eating behaviour. Nutrition Bulletin, 34, 126e173. Blundell, J. E., de Graaf, C., Finlayson, G., Halford, J. C. G., Hetherington, M., King, N., et al. (2009). Measuring food intake, hunger and satiation in the laboratory. In D. B. Allison, & M. L. Baskin (Eds.), Handbook of assessment methods for obesity and eating behaviour (2nd ed.). (pp. 283e326) Thousand Oaks: Sage Publications. Blundell, J. E., de Graaf, C., Hulshof, T., Jebb, S., Livingstone, B., Lluch, A., et al. (2010). Appetite control: methodological aspects of the evaluation of foods. Obesity Reviews, 11, 251e270. Bodinham, C. L., Katie, L., Hitchen, P., Youngman, J., Frost, G. S., & Robertson, M. D. (2011). Short-term effects of whole-grain wheat on appetite and food intake in healthy adults: a pilot study. British Journal of Nutrition, 106, 327e330.
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