satiation. A review

Food Hydrocolloids 32 (2013) 147e154

Contents lists available at SciVerse ScienceDirect

Food Hydrocolloids journal homepage: www.elsevier.com/locate/foodhyd

Review

The role of gums in satiety/satiation. A review Susana Fiszman*, Paula Varela Instituto de Agroquímica y Tecnología de Alimentos (IATA-CSIC), Agustín Escardino 7, 46980 Paterna (Valencia), Spain

a r t i c l e i n f o

a b s t r a c t

Article history: Received 26 October 2012 Accepted 12 December 2012

Alongside proteins, soluble fibres are the most promising ingredients for formulating foods with high satiating capacity. Because of the considerable complexity and variety of composition and structure of polysaccharide gums, it is not easy to decide which ingredients are most effective in which products. They can often act in combination on more than one level. Moreover, the research results are often contradictory as it is extremely difficult to draw comparisons between different studies. The complexity of the methods and the absence of necessary information on the substances used for satiating purposes pose additional difficulties. This review aims to clarify the mechanisms governing the satiating effect of gums in formulated foods, update the information and draw attention to points that require further investigation. Ó 2012 Elsevier Ltd. All rights reserved.

Keywords: Gums Satiation Satiety Viscosity Gelation Fermentability

Contents 1. 2. 3. 4.

5.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .147 Dietary fibres and satiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .148 Assessment of satiating potential . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .148 Gums and satiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .149 4.1. Viscosity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 149 4.2. Gelation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 150 4.2.1. Acid- and/or ion-mediated gelation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 150 4.2.2. Temperature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 151 4.3. Fermentability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 151 4.4. Relevance of the food matrix . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 151 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .152 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 152 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 152

1. Introduction Homeostasis is the set of self-regulation mechanisms which ensure that the composition and properties of the human body’s internal environment remain constant. By this means, stable, tightly-regulated energy reserves are maintained over long periods of time. To maintain a neutral energy balance, energy intake, thermogenesis and physical activity need to be regulated by at least two separate, but interrelated systems: a) a short-term system that

* Corresponding author. Tel.: þ34 963900022; fax: þ34 96 3636301. E-mail address: sfi[email protected] (S. Fiszman). 0268-005X/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.foodhyd.2012.12.010

controls the initiation and termination of meals depending on the contents of the gastrointestinal tract; and b) a long-term system that defends the stability of the energy reserves and thereby that of body weight (Spiegelman & Flier, 2001). Much progress has been made in identifying the various hormonal and neural mechanisms by which the brain informs itself about the availability of ingested and stored nutrients and, in turn, generates behavioural, autonomic and endocrine output. While the hypothalamus and caudal brainstem play crucial roles in this homeostatic function, areas in the cortex and limbic system are important for processing information regarding prior experiences with food, reward, and emotion, as well as the social and environmental context (Berthoud & Morrison, 2008). While functional

148

S. Fiszman, P. Varela / Food Hydrocolloids 32 (2013) 147e154

brain imaging studies of the neurohormonal brainegut axis that regulates satiety are still at a preliminary stage, they are nevertheless important, as they are beginning to present a clear picture of a well-defined network of brain areas which are activated during nutrient ingestion, making it possible to study the modulation of this network by hedonic and psychological factors such as emotions (Aziz, 2012). Satiation and satiety are central concepts in the understanding of appetite control and both have to do with inhibition of eating. Satiation occurs during an eating episode and brings it to an end. Satiety starts after the end of eating and prevents further eating before the return of hunger (Bellisle, Drewnowski, Anderson, Westerterp-Plantenga, & Martins, 2012). Many studies have examined the various sensory, cognitive, post-ingestion and postabsorption factors that can potentially contribute to satiation/ satiety. Of these factors, the first two lead to feelings of satiation and short-term satiety while the last two are more related to midand long-term satiety. However, they operate together and interact (Van Kleef, Van Trijp, Van Den Borne, & Zonder, 2012). Nowadays, the opportunities to consume energy-dense, unhealthy snacks are encouraged by the obesogenic environment that has developed in the western world, particularly among adolescents (Hardy et al., 2012). If satiating products were readily available, this would allow better control of eating behaviour and encourage responsible consumption. Consequently, the ability to manufacture products with high satiating capacity is a matter of interest to the food industry nowadays. Proteins and fibres are both widely recognized to be the nutrients with the greatest potential for satiating food development (Halford & Harrold, 2012). 2. Dietary fibres and satiation The term “dietary fibre” has a long history of definitions. The latest is that of The Commission of the European Communities (2008): carbohydrate polymers with three or more monomeric units, which are neither digested nor absorbed in the human small intestine and belong to the following categories: 1) edible carbohydrate polymers naturally occurring in the food as consumed; 2) edible carbohydrate polymers which have been obtained from food raw material by physical, enzymatic or chemical means and which have a beneficial physiological effect demonstrated by generally accepted scientific evidence; and 3) edible synthetic carbohydrate polymers which have a beneficial physiological effect demonstrated by generally accepted scientific evidence.” The evolution of the definitions of dietary fibre reflects the complexity of the substances and compounds this term covers and of their different effects on the body. Gums e a very well-known term for Food Hydrocolloids readers e are all soluble dietary fibres that play a crucial part in developing foods with high satiating capacity. The purpose of the present paper is to update and review the information about the role of gums in the occurrence of satiety/satiation and their mechanisms of action. 3. Assessment of satiating potential The usual method of discovering the satiating potential of any component, macronutrient or food item is to conduct interventional studies. In such laboratory or clinical studies, careful attention to study design is crucial for correct interpretation of the results (Robinson, 2004). A number of individual and combined environmental cues such as the variety of available foods (Brondel et al., 2009), time of consumption (Chungchunlam, Moughan, Henare, & Ganesh, 2012), portion size (Spill, Birch, Roe, & Rolls, 2011), distraction while eating (Brunstrom & Mitchell, 2006;

Higgs & Donohoe, 2011), previous experiences with the same food (Hogenkamp, Brunstrom, Stafleu, Mars, & de Graaf, 2012), orosensory stimulation (Hetherington & Regan, 2011), expectations (Brunstrom, Shakeshaft, & Alexander, 2010), specific sensory satiety (Griffioen-Roose, Finlayson, Mars, Blundell, & de Graaf, 2010) or dietary conditions (Mok, 2010) generate, modulate, and terminate appetitive sensations in individuals (Mattes, Hollis, Hayes, & Stunkard, 2005). Consequently, it is necessary to take into consideration the many effects that these cues can produce. The most common interventional studies are short-term. Normally they follow a preload design. As conditions before consumption need to be standardized, the usual procedure is to use a preload for breakfast after a night of fasting. Another possibility is to intervene later, after consumption of a controlled meal. The preloads can be consumed ad libitum or over a set time. Satiety is measured by assessing subjective fullness, hunger, or desire-to-eat sensations (Blundell et al., 2010) before the preload, between the preload and the test meal and at fixed times after the meal, using validated visual analogue scales (Clegg, Pratt, Markey, Shafat, & Henry, 2012; EFSA, 2012). Difficulties in drawing comparisons between studies that use different designs have been reported in numerous papers. Schuring et al. (2012) have proposed a new way to analyse, compare and describe the effects of food stimuli on selfreported appetite-related measures via a modelling procedure for estimating and quantitatively comparing the durations of appetite related responses to foods. Some physiological indices can also be employed. Interest in the use of biomarkers to measure satiety is based on their potential to indicate putative mechanisms of action and their presumed lower susceptibility to subjectivity and modification by environmental factors. Several changes in the gastrointestinal hormones released during or after eating, such as cholecystokinin, can only be considered in the context of behavioural assessment (EFSA, 2012). Since the great majority of articles on satiety are closely related to weight management and obesity, many studies examine subsequent energy intake and weight maintenance in the longer term. In this context, it is increasingly acknowledged that research needs to be carried out in both healthy and overweight subjects, as stomach responses to food are different in obese persons, who tend to have larger empty stomach volumes than people of normal weight. Long-term effects may differ from the short-term effects of a test meal, so extrapolating results from short-term studies to gauge long term effects is not always straightforward. For example, a subject’s microbiota could show adaptive responses after repeated exposure to fibre (Van Kleef et al., 2012). Long-term changes in energy intake and body weight are of evident interest. Some indicators of metabolic health, such as body fat distribution and parameters related to glucose and fat metabolism, are evaluated during this type of study. Benelam (2009) considers that it is not clear whether the apparent short-term satiating effect of low-energy density diets can help to maintain weight loss in the long-term and recommends further long-term studies. Randomised controlled trials are recommended, whereby dietary intervention in human participants continues over a considerable length of time (a number of weeks or months) and the energy intake is recorded (Brownlee, 2011). In these tests, additional considerations have to be taken into account such as whether the subjects follow a normo- or hypocaloric diet, their sex differences, or their physical activity. However, familiarity with the basic factors that regulate potential satiating effects is a goal in itself. Eating meals that satiate without ingesting excessive calories makes it possible to avoid or control the feelings of hunger that lead to snacking between meals, leading to a healthy lifestyle and less compulsive eating.

S. Fiszman, P. Varela / Food Hydrocolloids 32 (2013) 147e154

4. Gums and satiation It is difficult to propose a classification that would allow the effect of gums on satiety/satiation to be studied systematically. This review identifies three aspects which prove essential for studying their action mechanism: viscosity, gelation and fermentability. 4.1. Viscosity An enormous number of studies have assessed the satiating capacity of a long list of soluble gums that are viscous in solution. The effect that most fibres which impart viscosity to their solutions have on the feeling of satiety are caused by mechanisms which are related with slowing down enzyme efficacy and/or with gastric antrum distension (as they absorb large quantities of liquid) and/or delaying gastric emptying, which, in turn, may increase or prolong the satiety signals from the stomach. In addition, a delay in absorption and small bowel transit time may prolong the period of contact between the nutrients and the small intestine epithelium (Slavin & Green, 2007). The intragastric distribution of meals is also influenced by viscosity, with more viscous meals increasing antral distension and satiety, and gastric secretion may also play a role by increasing gastric volumes in response to increased viscosity, as reported by Marciani et al. (2001), who also studied the relation between viscosity and nutrient content, using non-invasive magnetic resonance imaging techniques, and found that the two have an additive effect. Many authors point out that it is very difficult to compare the results because the tests are not standardized (Paeschke & Aimutis, 2011). This difficulty would indicate that the results are not very conclusive. Even more importantly, perhaps, the characteristics of the gum employed are not reported in sufficient detail e molecular weight, degree of crosslinking, water or oil absorption capacity, sensitivity to the presence of certain cations, optimum working pH and other chemical properties are an important source of information for calculating the gum’s performance in the system (Titoria, 2011). It should be remembered that most of these studies are published in human nutrition-related journals so their targets are individuals and their metabolic responses. Still more remarkable, were that possible, is the lack of other types of information. For instance, viscosity is one of the main properties that are reported when undertaking a study of the satiating capacity of gums, yet most papers mention ‘viscosity’ as though it was a discrete physical property and very few report on the rheological profile of the gum in question. In this field it is well known that when gums are hydrated they increase the viscosity of the solution medium and show a very wide range of rheological behaviour, generally pseudoplastic, depending on their concentration, chemical makeup and structure. Not only did the abovementioned studies not normally report the complete rheological characterization of the targeted gum, a number of them did not even report its apparent viscosity (at a single shear rate). It is only in more recent years that a few papers have begun to give the apparent viscosity value before ingestion of the beverages or meals with added gums. However, what is important is the gums’ capacity to develop their full viscosity-conferring potential in the gastrointestinal tract. A few studies have used in vitro models to measure some of the effects of the gums’ viscosity on simulated gastric and small intestinal digesta (Bordoloi, Singh, & Kaur, 2012; Dikeman, Murphy, & Fahey, 2006; Maisonnier, Gomez, & Carre, 2001). The drawback of in vitro studies is that a large proportion of water absorption occurs in the small intestine, as does the majority of macronutrient

149

absorption, and it remains unclear how this would affect the resulting viscosity. In addition, inability to account for secretion of fluids/mucous in the stomach and small intestine makes it difficult to predict the viscosity that a gum can develop in the digestive tract (Dikeman et al., 2006). Also, some enzymes seem not to display the same efficacy (Murphy, McCracken, McCann, George, & Bedford, 2009). On the other hand, an evaluation of the viscosity of fluid digesta ex vivo from the stomach and small intestine of monogastric animals is a complex and difficult task, as noted by Dikeman and Fahey (2006). Shear rates in the gastrointestinal tract may vary considerably with sampling location, individual animal, meal composition and gut motility. These authors reviewed the results from a number of separate studies that measured digesta viscosity in animals (normally euthanised) and human (volunteers with terminal ileostomies). They reported that shear rates used varied from 0.005 to 90 s1, making comparisons difficult. As a result, in vivo non invasive instrumental techniques have gained interest. The volume of secretions within the stomach 60 min after ingestion has been assessed by magnetic resonance imaging (MRI). It was higher for a high-viscosity meal, showing a heterogeneous process of progressive gastric dilution, whereas low-viscosity meals were uniformly diluted (Marciani et al., 2001). MRI has been demonstrated to be a unique technique which is capable of monitoring the viscosity of a meal and the gastric function in vivo (Marciani et al., 2000). It also makes it possible to follow gastric accommodation. This was described by Schwizer et al. (2002) as the reduction in gastric tone and increase in compliance that follows the ingestion of a meal and involves at least two responses: “receptive relaxation”, which allows the stomach to accept a volume load without a significant rise in gastric pressure, and “adaptive relaxation” which modulates gastric tone in response to the specific properties of the meal ingested. MRI technology has shown that increasing the viscosity of non-nutrient meals delays gastric emptying, increases satiety and decreases hunger. Image analysis has been used to quantify the activity of ex vivo stomach preparations, while perfusates with unusual flow properties have provided evidence that the progression of antrocorporal contractions is modulated in part by local flow and pressure conditions (mechanoreceptors) in the alimentary tract contents undergoing digestion (Lentle, Janssen, Goh, Chambers, & Hulls, 2010). Soluble fibres that form non-viscous solutions, such as resistant starch (RS), have been found to have no effect or only a weak one on satiety or hunger scores, even when large amounts of the isolated fibre are ingested (Nugent, 2005; Pasman, Wils, Saniez, & Kardinaal, 2006). According to Willis, Eldridge, Beiseigel, Thomas, and Slavin (2009), research on RS and satiety is sparse and inconsistent. In addition, these authors state that the palatability of a fibre-rich food may also play a role, making comparison difficult. In the same way, calorie-for-calorie, foods with different sensory effects differ considerably in the extent to which they are expected to deliver satiation and these expectations are highly correlated with predictions of the ‘actual’ satiety that a food confers (Wilkinson & Brunstrom, 2009). On the other hand, So et al. (2007) reported that as well as its other effects, RS affects appetite regulation, with the help of changes in neuronal activity in the hypothalamic appetite regulation centres which suggest satiation. Supplementing beverages with a small amount of low-viscosity pectin fibre can decrease energy intake at a subsequent meal, although no effect on subjective feelings of hunger were identified (Perrigue, Carter, Roberts, & Drewnowski, 2010). From the point of view of food formulation development it should be remembered that to obtain maximum viscosity, the gums

150

S. Fiszman, P. Varela / Food Hydrocolloids 32 (2013) 147e154

need to be completely hydrated and form a colloidal suspension. That is not a problem when they are added to beverages, but in semi-solid or solid foods the hydrocolloids will reach the stomach without being fully hydrated and the shear forces created as the stomach muscles contract will be insufficient to develop their full functionality. As calculated by Kozu et al. (2010) using computational fluid dynamics to simulate and analyse intragastric fluid motions induced by human peristalsis, the shear rate due to gastric fluid motion reaches values of approximately 20 s1 in the most occluded region. Other factors such as dilution of the gums by stomach fluids and the possible effects of very low pH values, while very variable, also need to be taken into account to avoid diminishing the effectiveness of the gums. The rapid and accurate new image acquisition techniques mentioned above can be used to follow and measure some in vivo gastric functions, such as gastric dilution (Tyler, Moore, Marciani, & Gowland, 2004). These non-invasive methods of monitoring gastro-intestinal physiology will also be of value in studying postprandial changes in the small intestine contents (Hoad et al., 2009). Lastly, the sensory aspects of the final system should not be forgotten. Inducing satiety requires higher doses of hydrocolloids than those commonly employed to stabilize or improve the texture of food systems. Adding large quantities of viscous gums to beverages can affect the sensory properties, with consequences such as an unpleasant degree of thickness or a slimy texture, making them difficult to swallow. In solid foods, hydrocolloids that are not hydrated or only partially hydrated can give rise to a chewy texture and high adherence to the teeth (Titoria, 2011). 4.2. Gelation Gelling in the stomach, brought about by different triggering factors, is another mechanism by which some hydrocolloids can contribute to satiety. It is believed that in order for gastric gelation to induce satiety, not only must a gel form in the stomach but the gel must also possess some strength (Ström et al., 2009). 4.2.1. Acid- and/or ion-mediated gelation One example of this approach is the study by Hoad et al. (2004) that compared two types of alginates (which gel weakly or strongly on exposure to a stomach acid milieu) with guar gum (whose viscosity is unaffected by acid). The hydrocolloids were dispersed in a milk beverage so that during acidification some calcium ions released from the milk micelles would cause the alginate to form ionic gels; similarly, at pH levels below the pK of the uronic acid residues the alginates form acid gels. Intragastric gelling, gastric emptying, and meal dilution were assessed instrumentally by serial MRI while the participants’ satiety was recorded over a certain period of time. The images showed that all the meals became heterogeneous in the stomach except for guar, which remained homogeneous. The alginate meals formed lumps in the stomach, with the strongly-gelling alginate producing the largest volume. Although gastric emptying was similar, the sense of fullness for the same gastric volume was significantly greater for all the alginate or guar meals than for the control (without any hydrocolloid). Nonetheless, according to Spyropuolos, Norton, and Norton (2011), these acid gels are produced too quickly after entering the stomach and thus would give less than optimal structuring of its content. Based on purely mechanical instrumental measurements, these authors proposed another system: a mixed low-methoxy pectin/low-acyl gellan gum system for controlled “structuring” and “de-structuring” processes: the former (acid gelation) is controlled by varying the fractions of the individual components and the pH of the medium and the latter (breakdown) eventually takes place as

a result of the forces applied in the stomach. Searching for physical stability over time, with no gel forming during storage before consumption, and for low viscosity at neutral pH, Ström et al. (2009) proposed either a mixture of alginate and high methoxy pectin or a mixture of alginate and tricalcium phosphate for mildly acidic beverage and neutral product formulations respectively. They made, on one hand, instrumental measurements of the viscosity of the solutions and beverages and the fracture force of the gels formed in the laboratory; and on the other hand, recorded the subjects’ assessments of appetite, and obtained MRI in vivo images (of only two subjects). These authors emphasised the relevance of understanding the relationship between the mechanical strength of the gel in the stomach and the volume consumed and its impact on satiety enhancement. Further research is also needed to understand the possible impact of the nutrients in these systems on their efficacy in achieving satiety through gelling biopolymers. To study the behaviour of alginate gels in the human gastrointestinal tract, Hoad et al. (2009) gave strongly and weakly gelled alginate beads (prepared by long and short exposures to a calcium chloride gelling bath) to volunteers, who swallowed them without chewing. The results showed that both types of alginate beads were clearly visible in the stomach and small bowel on the MR images. Gastric emptying was delayed slightly by the presence of the stronger beads, due to gastric sieving, and the satiety score for fullness was increased slightly by the weakly gelled beads, probably due to greater gut wall distension as a result of the larger volume of beads consumed for this meal. Also using MRI techniques, Norton, Frith, and Ablett (2006) reviewed and studied the influence of the particle shape, gel strength, physical form and microstructure of a number of different gelled particles on their behaviour in the stomach and their relation with self-reported satiety. In addition, these authors studied gelation within the stomach by allowing some volunteers to drink an alginate meal. They observed “string-like” (inhomogeneous) gel structures that had developed as a result of stomach motility. The MRI results also showed that the gelled alginate meal remained in the stomach for significantly longer than a non-gelling locust bean gum meal and its overall emptying rate was slower. As discussed by Mattes (2007) when exploring the effects on appetite of adding alginate to a meal replacement bar (which also contained dibasic dicalcium phosphate), if the digesta did not stay in the stomach long enough to allow the pH to drop below 4.7 then free calcium would not be released to trigger alginate gelation. However, this author did not discuss the degree of hydration that the alginate might have achieved in the stomach. To clarify the effects on appetite of a strongly gelling alginate, a fully hydrated alginate in an acceptable, lowviscosity drink formulation was investigated by Peters et al. (2011): they added 0 (control), 0.6, or 0.8% of a high-guluronate alginate to a meal replacement drink that also contained protein and calcium and found that hunger was robustly reduced with 0.8% alginate and most effects were also significant with 0.6% alginate, revealing a dose-dependent effect, and that the gel-forming alginate is effective when it is fully hydrated. In this study they only recorded scores for subjective feelings of hunger, satiety, and palatability. Other gel-forming hydrocolloids also show the ability to form gels in acidic conditions. Temperature-dependant gelation behaviour of low-methoxyl pectin (LMP) and amidated LMP over a broad range of pH and calcium ion concentrations was reported by Capel, Nicolai, Durand, Boulenguer, and Langendorff (2006). They found that adding high amounts of calcium ion destabilized the LMP solutions, leading to the formation of increasingly heterogeneous athermal gels or precipitation, but amidation enhanced acidinduced gelation without significantly modifying the sensitivity to calcium. Yamamoto and Cunha (2007) characterized the

S. Fiszman, P. Varela / Food Hydrocolloids 32 (2013) 147e154

rheological behaviour and microstructure of gellan gum gels formed by slow acid release, using glucono delta lactone, under different heating conditions. They found that heating the solutions, raising the polymer concentration and lowering the final pH decreased the time taken to reach gel point. All these findings open the door to studies on the formation of these gels in the acid conditions of the stomach in relation to their potential as satiation agents. Using the same approach, Norton, Cox, and Spyropoulos (2011) studied in vitro acid-induced gelation of low acyl gellan in order to gain an insight into the acid gel structures that can be produced in different pH environments. They reported that both the structuring and de-structuring of gellan acid gels can be controlled by the process used for their production and by exposure to an acidic environment which, “conveniently”, can take place within a time scale that would make this approach applicable for controlling satiety. A number of compositions and complete foods have been patented, including several biopolymers that can gel in the stomach, mostly comprising alginates, pectin and processed starches (cf. Aimutis, Finocchiaro, Paeschke, & Sox, 2007; Aldred, Van Amerongen, Bodor, Mela, & Rayment, 2005; Boers, Strom, & Wisenman, 2008; Noble & Le Douaron, 2010; Tester & Hooper, 2007; Wolf, Blidner, Garleb, Lai, & Schenz, 2002). Solid foods such as cookies, bars or crisps, some using processes such as extrusion, and a combination of viscous and gel-forming soluble fibres have been proposed as satiating compositions in which hydration has to take place after ingestion (Aimutis et al., 2007; Aimuits et al., 2007). Along the same lines of hypothesizing about the satiating capacity of a solid formed in the stomach during digestion, Anderson and Moore (2004) analysed the differences in satiating capacity of several casein and whey proteins and suggested that the difference could be attributed to clotting of the casein (unlike the soluble whey) in the acidic medium of the stomach, which would respond to the same principle as hydrocolloid gel formation in the stomach. 4.2.2. Temperature A composition based on a novel methylcellulose (MC) with the ability to form a gel at temperatures below human body temperature, which therefore forms a gel mass in the individual’s stomach when ingested, has been claimed as a method for inducing satiety in the patent by Adden, Anderson, Huebner, and Knarr (2011). The mechanical characteristics of the gel formed by this MC at different concentrations have been found to be similar to those of alginate gel systems (Knarr, Adden, Anderson, & Hübner-Kesse, 2012). 4.3. Fermentability Virtually all the carbohydrate that enters the large bowel will be fermented by the commensal bacteria that live in the colon at densities of up to 1012/g. Only very resistant retrograded starches partly survive, with the amount depending on colonic transit time. Microcrystalline cellulose may resist fermentation because of its highly condensed structure, but cellulose naturally present in the cell wall of food is completely fermented unless it is associated with large amounts of lignin (Elia & Cummings, 2007). Gut fermentation of fibre affects satiety. Short-chain fatty acids (SCFA, such as butyrate, acetate, and propionate) produced by colonic fermentation may influence the response and actions of the gut hormones gastric inhibitory peptide, glucagon-like peptide-1, and cholecystokinin (CCK). A direct correlation has been reported between post-prandial CCK and subjective satiety scores following ingestion of foods with varying amounts of fibre (Slavin, Savarino, Paredes-Diaz, & Fotopoulos, 2009). According to these authors, soluble fibres that are slowly yet extensively fermented (e.g. wheat

151

dextrin) are tolerated more easily than those that ferment quickly, as the latter can produce larger amounts of gas in a shorter period of time, leading to bloating and flatulence. According to Karalus et al. (2012), the mechanisms that might be responsible for such effects are not fully understood, and there are very few reports comparing the effects on satiety of fermentable fibre and nonfermentable fibre. A number of factors including chemical structure, particle size, surface area, solubility, availability of other more readily fermentable substrates or the composition of the colonic microflora, among others, affect the extent rate, and site of fermentation in the gut and the nature of the SCFA produced (Blackwood, Salter, Dettmar, & Chaplin, 2000; Slavin, 2010). For example, low molecular weight guar gum, which is more easily incorporated into food, may have less pronounced physiological effects than the native form: its molecular weight has been positively correlated with acetate production and negatively correlated with propionate production in an in vitro fermentation study with human faecal inoculum (Stewart & Slavin, 2006). Other hydrocolloids such as alginate or partially hydrolysed guar gum have been investigated in vitro to ascertain their effects on the composition of the colonic mucus (the colonic mucosa’s first line of defence against luminal aggression), intestinal pH or the SCFA production profile (Ohashi et al., 2012; Ramnani et al., 2012). A comparison of konjac gum, guar gum, xanthan gum, pectin and carrageenan in human faecal inoculum in a 48-h static fermentation culture system showed that all the gums increased the acetate, propionate and total SCFA levels, but their production differed depending on the gum (Yang & Chen, 2008). Soluble fibres are fermented more readily and earlier in the colon than insoluble fibres. Terminal residues are fermented first and carbohydrates containing alpha-arabinose or alpha-galacturonic acid residues are generally more susceptible to fermentation. Xylans, pectins, and other gums are fermented significantly in the gut (whereas cellulose is only partly broken down and lignin is essentially an inert material). RS is completely degraded in the large bowel. Fibre fermentation continues for as long as any fibre remains in the large intestine, so short-term measures of fermentation (like increased breath hydrogen excretion) limit the ability to determine whether sustained fermentation and/or changes in microflora associated with long-term consumption can alter satiety and reduce food intake. Long-term consumption of fermentable fibre could be useful in providing new insight into satiety benefits. There is a need for appropriately designed, randomised controlled trial data to demonstrate the long-term benefits to health that are suggested by short-term physiological responses to fibre ingestion (Brownlee, 2011). 4.4. Relevance of the food matrix Food structure affects the rate and extent of digestion and the rate of absorption of any nutrient. Consequently, all important food processing methods (such as homogenization, grinding, heat treatment, etc.) could also affect these physiological processes to some extent (Turgeon & Rioux, 2011). Temelli (2008) analysed how the concentration process to isolate b-glucan from oat/barley grains, followed by the standard food processing operations to which product containing the b-glucan is subjected, could alter the molecular weight and/or solubility of the latter. Consuming a food also involves various oral operations, including first bite, chewing, transportation, bolus formation, swallowing, etc. (Chen, 2009). Food processing and transformation in the mouth, with particular attention to the rheology aspects of oral operations, may influence perceptions of satiety via anticipatory or sensory/preingestive cues.

152

S. Fiszman, P. Varela / Food Hydrocolloids 32 (2013) 147e154

Results on the effects of soluble fibres on appetite differ according to the type of fibre and to whether it is added as an isolated fibre supplement or occurs naturally in a food (Karalus et al., 2012). Adding fibre can affect the texture, appearance, and liking for the food product, which in turn would affect satiety scores. According to Yeomans, Weinberg, and James (2005), energy density is the major determinant of short-term energy intake. In this regard, fibres can dilute the energy density of the diet. Foods that contain fibre are normally more difficult to process in the mouth (they have more dense, compact textures), which increases exposure to the food in the oral cavity. This orosensory exposure is essential for prompting food intake feedback signals (Bolhuis, Lakemond, de Wijk, Luning, & de Graaf, 2011). When a product stays in the mouth for a longer time, there is more opportunity for the sensory receptors in the oral cavity to capture taste, smell, texture, and other properties of the food. Zijlstra, de Wijk, Mars, Stafleu, and de Graaf (2009) stated that this leads to early sensory satiation, which induces a reduction in bite size. Breast feeding may provide an important initial exposure to a general rule that thicker substances contain more calories than thinner substances (Zijlstra, Mars, de Wijk, Westerterp-Plantenga, & de Graaf, 2008). The importance of this type of stimulus in suppressing appetite has been demonstrated by studies that compare normal feeding with the direct infusion of specific nutrients or foods into different areas of the gastrointestinal tract combined with techniques to distend the stomach (French & Cecil, 2001). In the absence of orosensory cues that predict energy differences, learning flavoureenergy associations can, to some extent, allow short-term energy consumption to be regulated. Separation of solids and liquids within the stomach allows faster gastric emptying of liquids than solids, a phenomenon known as sieving. Marciani et al. (2012) demonstrated that blending the solid/ liquid meal into a viscous soup delays gastric emptying and increases the hormonal response to feeding, which may contribute to enhanced postprandial satiety. Yeomans and Chambers (2011) found that small changes in the sensory characteristics of drinks altered the degree to which added energy was satiating, which implies that nutrients become more satiating when they are predicted by relevant sensory cues (creaminess, for instance). From this point of view, adding gums to the formulations could play an important role. Each fibre structure has its own rate of breakdown and absorption, which is influenced by the food matrix structure and organization (Englyst & Englyst, 2005). The structure and availability of the fibre can also modulate the digestion kinetics of other nutrients, for example by decreasing proteolysis (Peyron, Mouecoucou, Fremont, Sanchez, & Gontard, 2006), so gums can act as ingesta modulators. Perceived food volume, independent of its energy density, can influence satiety (Rolls, Bell, & Waugh, 2000). Non-nutrients such as air and water can be exploited to manipulate perceived portion sizes without increasing the energy content; they also contribute sensory and other characteristics. Although increased gastric distension may be the main mechanism underlying the volume effects, pre-ingestive and ingestive impacts on cognitive, anticipatory and sensory responses also appear to be involved (Welch, 2011). Gums are known to stabilize foams and to absorb large amounts of water, so their addition could contribute to both effects by diluting the energy density of the food and increasing its volume. 5. Conclusions Alongside proteins, polysaccharide gums are the most promising ingredients and the ones that can play the most important

role when designing foods with high satiating capacity. A number of studies have shown the benefits of dietary intervention with soluble-gum-rich foods for metabolic profiles, but the effects of each gum have not yet been isolated from those of other compounds in these foods. The effect of the food matrix and the rheology and composition of each gum on the physiological effect is complex and requires an interdisciplinary approach. An increasing number of studies is showing the positive effects of gums on satiety and suggesting beneficial synergies between gums that have different effects. New instrumental imaging techniques developed over the past decade make it possible to follow their action in vivo. However, more research is needed to develop gastrointestinal models e simulating different gut areas to allow evaluation of the intestinal absorption of food ingredients e and validate them in vitro in order to extrapolate the results to real, in vivo situations. The source of the gums, the method by which they are obtained, their purity and the experimental processing conditions are just a few other factors that may affect the physiological results. The composition of the complete food to which the gums are added is important, as its effect on gastric functions need to be assessed, bearing in mind the effects of in-mouth processing, nutrient content and energy density, the volume ingested and the oral exposure, among other factors. Enormous advances have been made in studying the mechanisms governing the physiological effects of soluble hydrocolloids on satiety, and while the road ahead may seem long, it looks very promising. 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 Adden, R., Anderson, W., Huebner, B., & Knarr. (2011). Methods and compositions for inducing satiety. Patent WO2011139763. Aimuits, W., Paeschke, T. M., Sun, N., Johnson, S. D., Sweeney, J. F., Patist, A., et al. (2007). Fiber satiety compositions. Patent WO2007044608. Aimutis, W. R., Finocchiaro, E. T., Paeschke, T. M., & Sox, T. E. (2007). Compositions and methods for inducing satiety and reducing caloric intake. Patent WO2007044663. Aldred, D. L. V., Amerongen, I. A., Bodor, J., Mela, D. J., & Rayment, P. (2005). Satiety enhancing food compositions. Patent WO/2005/020717. Anderson, H., & Moore, S. E. (2004). Dietary proteins in the regulation of food intake and body weight in humans. Journal of Nutrition, 134, 974Se979S. Aziz, Q. (2012). Brainegut interactions in the regulation of satiety: new insights from functional brain imaging. Gut, 61, 1521e1522. Bellisle, F., Drewnowski, A., Anderson, G. H., Westerterp-Plantenga, M., & Martins, C. K. (2012). Sweetness, satiation, and satiety. Journal of Nutrition, 142, 1149Se1154S. Benelam, B. (2009). Satiation, satiety and their effects on eating behaviour. Nutrition Bulletin, 34, 126e173. Berthoud, H.-R., & Morrison, C. (2008). The brain, appetite, and obesity. Annual Review of Psychology, 59, 55e92. Blackwood, A. D., Salter, J., Dettmar, P. W., & Chaplin, M. F. (2000). Dietary fibre, physicochemical properties and their relationship to health. The Journal of the Royal Society for the Promotion of Health, 120, 242e247. 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. Boers, H. M., Strom, A. H. E., & Wisenman, S. A. (2008). Liquid satiety enhancing composition. Patent WO2008022857. Bolhuis, D. P., Lakemond, C. M. M., de Wijk, R. A., Luning, P. A., & de Graaf, C. (2011). Both longer oral sensory exposure to and higher intensity of saltiness decrease ad libitum food intake in healthy normal-weight men. Journal of Nutrition, 141, 2242e2248.

S. Fiszman, P. Varela / Food Hydrocolloids 32 (2013) 147e154 Bordoloi, A., Singh, J., & Kaur, L. (2012). In vitro digestibility of starch in cooked potatoes as affected by guar gum: microstructural and rheological characteristics. Food Chemistry, 133, 1206e1213. Brondel, L., Romer, M., Van Wymelbeke, V., Pineau, N., Jiang, T., Hanus, C., et al. (2009). Variety enhances food intake in humans: role of sensory-specific satiety. Physiology & Behavior, 97, 44e51. Brownlee, I. A. (2011). The physiological roles of dietary fibre. Food Hydrocolloids, 25, 238e250. Brunstrom, J. M., & Mitchell, G. L. (2006). Effects of distraction on the development of satiety. British Journal of Nutition, 96, 761e769. Brunstrom, J. M., Shakeshaft, N. G., & Alexander, E. (2010). Familiarity changes expectations about fullness. Appetite, 54, 587e590. Capel, F., Nicolai, T., Durand, D., Boulenguer, P., & Langendorff, V. (2006). Calcium and acid induced gelation of (amidated) low methoxyl pectin. Food Hydrocolloids, 20, 901e907. Chen, J. (2009). Food oral processing e a review. Food Hydrocolloids, 23, 1e25. Chungchunlam, S. M. S., Moughan, P. J., Henare, S. J., & Ganesh, S. (2012). Effect of time of consumption of preloads on measures of satiety in healthy normal weight women. Appetite, 59, 281e288. Clegg, M. E., Pratt, M., Markey, O., Shafat, A., & Henry, C. J. 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. Dikeman, C. L., & Fahey, G. C., Jr. (2006). Viscosity as related to dietary fiber: a review. Critical Reviews in Food Science and Nutrition, 46, 649e663. Dikeman, C. L., Murphy, M. R., & Fahey, G. C., Jr. (2006). Dietary fibers affect viscosity of solutions and simulated human gastric and small intestinal digesta. Journal of Nutrition, 136, 913e919. EFSA, European Food Safety Authority, & Panel on dietetic products, nutrition and allergies. (2012). 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. Englyst, K. N., & Englyst, H. N. (2005). Carbohydrate bioavailability. British Journal of Nutrition, 94, 1e11. French, S. J., & Cecil, J.,E. (2001). Oral, gastric and intestinal influences on human feeding. Physiology & Behavior, 74, 729e734. Griffioen-Roose, S., Finlayson, G., Mars, M., Blundell, J. E., & de Graaf, C. (2010). Measuring food reward and the transfer effect of sensory specific satiety. Appetite, 55, 648e655. 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. Hardy, L. L., Grunseit, A., Khambalia, A., Bell, C., Wolfenden, L., & Milat, A. J. (2012). Co-occurrence of obesogenic risk factors among adolescents. The Journal of Adolescent Health, 51, 265e271. Hetherington, M. M., & Regan, M. F. (2011). Effects of chewing gum on short-term appetite regulation in moderately restrained eaters. Appetite, 57, 475e482. Higgs, S., & Donohoe, J. E. (2011). Focusing on food during lunch enhances lunch memory and decreases later snack intake. Appetite, 57, 202e206. Hoad, C. L., Rayment, P., Cox, E., Wright, P., Butler, M., Spiller, R. C., et al. (2009). Investigation of alginate beads for gastro-intestinal functionality, part 2: in vivo characterisation. Food Hydrocolloids, 23, 833e839. Hoad, C. L., Rayment, P., Spiller, R. C., Marciani, L., Alonso, B. de C., Traynor, C., et al. (2004). In vivo imaging of intragastric gelation and its effect on satiety in humans. Journal of Nutrition, 134, 2293e2300. Hogenkamp, P. S., Brunstrom, J. M., Stafleu, A., Mars, M., & de Graaf, C. (2012). Expected satiation after repeated consumption of low- or high-energy-dense soup. British Journal of Nutrition, 108, 182e190. Karalus, M., Clark, M., Greaves, K. A., Thomas, W., Vickers, Z., Kuyama, M., et al. (2012). Fermentable fibers do not affect satiety or food intake by women who do not practice restrained eating. Journal of The Academy of Nutrition and Dietetics, 112, 1356e1362. Knarr, M., Adden, R., Anderson, W. H. K., & Hübner-Keese, B. (2012). Characterization of in-vitro gel performance of novel MC with respect to the suitability for satiety applications. Food Hydrocolloids, 29, 317e325. Kozu, H., Kobayashi, I., Nakajima, M., Uemura, K., Sato, S., & Ichikawa, S. (2010). Analysis of flow phenomena in gastric contents induced by human gastric peristalsis using CFD. Food Biophysics, 5, 330e336. Lentle, R. G., Janssen, P. W. M., Goh, K., Chambers, P., & Hulls, C. (2010). Quantification of the effects of the volume and viscosity of gastric contents on antral and fundic activity in the rat stomach maintained ex vivo. Digestive Diseases and Sciences, 55, 3349e3360. Maisonnier, S., Gomez, J., & Carre, B. (2001). Nutrient digestibility and intestinal viscosities in broiler chickens fed on wheat diets, as compared to maize diets with added guar gum. British Poultry Science, 42, 102e110. Marciani, L., Gowland, P. A., Spiller, R. C., Manoj, P., Moore, R. J., Young, P., et al. (2000). Gastric response to increased meal viscosity assessed by echo-planar magnetic resonance imaging in humans. The Journal of Nutrition, 130, 122e127. Marciani, L., Gowland, P. A., Spiller, R. C., Manoj, P., Moore, R. J., Young, P., et al. (2001). Effect of meal viscosity and nutrients on satiety, intragastric dilution, and emptying assessed by MRI. American Journal of Physiology e Gastrointestinal and Liver Physiology, 280(6), G1227eG1233.

153

Marciani, L., Hall, N., Pritchard, S. E., Cox, E. F., Totman, J. J., Lad, M., et al. (2012). Preventing gastric sieving by blending a solid/water meal enhances satiation in healthy humans. Journal of Nutrition, 142, 1253e1258. Mattes, R. D. (2007). Effects of a combination fiber system on appetite and energy intake in overweight humans. Physiology & Behavior, 90, 705e711. Mattes, R. D., Hollis, J., Hayes, D., & Stunkard, A. J. (2005). Appetite: measurement and manipulation misgivings. Journal of The American Dietetic Association, 105(5 Suppl.), S87eS97. Mok, L. W. (2010). The effect of variety and dietary restraint on food intake in lean young women: a preliminary study. Journal of General Psychology, 137, 63e83. Murphy, T. C., McCracken, J. K., McCann, M. E. E., George, J., & Bedford, M. R. (2009). Broiler performance and in vivo viscosity as influenced by a range of xylanases, varying in ability to affect wheat in vitro viscosity. British Poultry Science, 50, 716e724. Noble, O., & Le Douaron, M. (2010). Acidic beverage containing low-methoxyl amidated pectin and no added calcium for a satiety effect. Patent WO2010116210. Norton, A. B., Cox, P. W., & Spyropoulos, F. (2011). Acid gelation of low acyl gellan gum relevant to self-structuring in the human stomach. Food Hydrocolloids, 25, 1105e1111. Norton, I. T., Frith, W. J., & Ablett, S. (2006). Fluid gels, mixed fluid gels and satiety. Food Hydrocolloids, 20, 229e239. Nugent, A. P. (2005). Health properties of resistant starch. Nutrition Bulletin, 30, 27e54. Ohashi, Y., Harada, K., Tokunaga, M., Ishihara, N., Okubo, T., Ogasawara, Y., et al. (2012). Faecal fermentation of partially hydrolyzed guar gum. Journal of Functional Foods, 4, 398e402. Paeschke, T. M., & Aimutis, W. R. (2011). Formulating for satiety with hydrocolloids. Food Technology, 65(3), 24e35. Pasman, W., Wils, D., Saniez, M.-H., & Kardinaal, A. (2006). Long-term gastrointestinal tolerance of nutriose FB in healthy men. European Journal of Clinical Nutrition, 60, 1024e1034. Perrigue, M., Carter, B., Roberts, S. A., & Drewnowski, A. (2010). A low-calorie beverage supplemented with low-viscosity pectin reduces energy intake at a subsequent meal. Journal of Food Science, 75, H300eH305. Peters, H. P., Koppert, R. J., Boers, H. M., Ström, A., Melnikov, S. M., Haddeman, E., et al. (2011). Dose-dependent suppression of hunger by a specific alginate in a low-viscosity drink formulation. Obesity, 19, 1171e1176. Peyron, S., Mouecoucou, J., Fremont, S., Sanchez, C., & Gontard, N. (2006). Effects of heat treatment and pectin addition on beta-lactoglobulin allergenicity. Journal of Agricultural and Food Chemistry, 54(15), 5643e5650. Ramnani, P., Chitarrari, R., Tuohy, K., Grant, J., Hotchkiss, S., Philp, K., et al. (2012). In vitro fermentation and prebiotic potential of novel low molecular weight polysaccharides derived from agar and alginate seaweeds. Anaerobe, 18, 1e6. Robinson, T. M. (2004). Dietary hydrocolloids, fibre, and satiety. In P. A. Williams, & G. O. Phillips (Eds.). Gums & stabiliser for the food industry, Vol. 12 (pp. 571e580). London: Royal Society of Chemistry. Rolls, B. J., Bell, E. A., & Waugh, B. A. (2000). Increasing the volume of a food by incorporating air affects satiety in men. The American Journal of Clinical Nutrition, 72, 361e368. Schuring, E., Quadt, F., Kovacs, E. M. R., Meullenet, J.-F., Wiseman, S., & Mela, D. J. (2012). A quantitative method for estimating and comparing the duration of human satiety responses: statistical modeling and application to liquid meal replacers. Appetite, 59(2), 601e609. Schwizer, W., Steingötter, A., Fox, M., Zur, T., Thumshirn, M., Bösiger, P., et al. (2002). Non-invasive measurement of gastric accommodation in humans. Gut, 51, i59ei62. Slavin, J. (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. Slavin, J. L., Savarino, V., Paredes-Diaz, A., & Fotopoulos, G. (2009). A review of the role of soluble fiber in health with specific reference to wheat dextrin. Journal of International Medical Research, 37, 1e17. So, P.-W., Yu, W.-S., Kuo, Y.-T., Wasserfall, C., Goldstone, A. P., et al. (2007). Impact of resistant starch on body fat patterning and central appetite regulation. PLoS ONE, 2(12), e1309. Spiegelman, B. M., & Flier, J. S. (2001). Obesity and the regulation of energy balance. Cell, 104, 531e543. Spill, M. K., Birch, L. L., Roe, L. S., & Rolls, B. (2011). Serving large portions of vegetable soup at the start of a meal affected children’s energy and vegetable intake. Appetite, 57, 213e219. 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. Stewart, M. L., & Slavin, J. L. (2006). Molecular weight of guar gum affects shortchain fatty acid profile in model intestinal fermentation. Molecular Nutrition and Food Research, 50, 971e976. Ström, A., Boers, H. M., Koppert, R., Melnikov, S. M., Wiseman, S., & Peters, H. P. F. (2009). Physico-chemical properties of hydrocolloids determine their appetite effects. In P. A. Williams, & G. O. Phillips (Eds.). Gums and stabilisers for the food industry, Vol. 15 (pp. 341e355). Cambridge: Royal Society of Chemistry. Temelli, F. (2008). All fibres are not equal: the importance of viscosity. Agro Food Industry Hi-tech, 19(6), 6e8. Tester, R., & Hooper, D. (2007). Gastric raft composition comprising preferably processed starches for inducing satiety. Patent WO2007104905.

154

S. Fiszman, P. Varela / Food Hydrocolloids 32 (2013) 147e154

The Commission of the European Communities (2008). Commission directive 2008/ 100/EC annex II of 28 October 2008. Titoria, P. M. (2011). Hydrocollods 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. Tyler, D. J., Moore, R. J., Marciani, L., & Gowland, P. A. (2004). Rapid and accurate measurement of transverse relaxation times using a single shot multi-echo echo-planar imaging sequence. Magnetic Resonance Imaging, 22, 1031e1037. 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. Welch, R. W. (2011). Satiety: have we neglected dietary non-nutrients? Proceedings of The Nutrition Society, 70(2), 145e154. Wilkinson, L. L., & Brunstrom, J. M. (2009). Conditioning ‘fullness expectations’ in a novel dessert. Appetite, 52, 780e783. 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.

Wolf, B. W., Blidner, B. B., Garleb, K. A., Lai, C.- S., & Schenz, T. W. (2002). Dual induced viscosity fiber system and uses thereof. Patent WO2002096223. Yamamoto, F., & Cunha, R. L. (2007). Acid gelation of gellan: effect of final pH and heat treatment conditions. Carbohydrate Polymers, 68, 517e527. Yang, H.-F., & Chen, H.-L. (2008). Utilization of gum dietary fibers by the human fecal inoculum in the static fermentation culture system. Taiwanese Journal of Agricultural Chemistry and Food Science, 46(4e5), 183e189. Yeomans, M. R., & Chambers, L. (2011). Satiety-relevant sensory qualities enhance the satiating effects of mixed carbohydrateeprotein preloads. American Journal of Clinical Nutrition, 94, 1410e1417. Yeomans, M. R., Weinberg, L., & James, S. (2005). Effects of palatability and learned satiety on energy density influences on breakfast intake in humans. Physiology & Behavior, 86, 487e499. Zijlstra, N., de Wijk, R. A., Mars, M., Stafleu, A., & de Graaf, C. (2009). Effect of bite size and oral processing time of a semisolid food satiation. The American Journal of Clinical Nutrition, 90, 269e275. Zijlstra, N., Mars, M., de Wijk, R. A., Westerterp-Plantenga, M. S., & de Graaf, C. (2008). Effect of viscosity on appetite and gastro-intestinal hormones. Physiology & Behavior, 97, 68e75.