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Texture and satiation: The role of oro-sensory exposure time
Physiology & Behavior 107 (2012) 496–501
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Texture and satiation: The role of oro-sensory exposure time Cees de Graaf ⁎ Division of Human Nutrition, Wageningen University, P.O. Box 8129, 6700 EV Wageningen, The Netherlands
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Article history: Received 16 February 2012 Received in revised form 6 May 2012 Accepted 8 May 2012 Keywords: Texture Food intake Cephalic phase response Satiation Satiety Appetite Sensory Taste
a b s t r a c t One of the characteristics of the current obesogenic food supply is the large availability of foods that can be ingested quickly. Controlled nutrition intervention studies have shown that the ingestion of simple energy containing beverages, which are consumed very quickly, do not lead to a lower compensatory intake of other foods. One of the theories behind this observation is that calories that are ingested quickly are not well sensed by the sense of taste, and do not lead to an adequate satiety response. This idea is confirmed by the results of a series of studies, where we have shown that the low satiation/satiety response of beverages can be largely attributed to their short oral residence time. Prolonging the oro-sensory exposure time to foods leads to earlier meal termination and/or a higher satiety response. The low satiation/satiety response to simple energy containing beverages is congruent with the observation from studies on the cephalic phase response to foods, i.e. the physiological response to sensory signals. Energy containing beverages do not lead to an adequate cephalic phase response. Various recent studies showed that slower eating leads to higher levels of satiety hormones. These results are in line with the idea that the sense of taste is a nutrient sensor which informs the brain and the gut about the inflow of nutrients. The sense of taste has an important contribution to the satiating effect of foods. One of the challenges in future research is to see whether or not these proofs of principles can be applied in longer term studies with regular commercial foods. This may make our obesogenic food supply more satiating, and may lead to a lower energy intake. © 2012 Published by Elsevier Inc.
1. Introduction The obesogenic food supply is characterized by a large variety of energy containing softly textured foods with large portion sizes that can be eaten quickly. These foods may promote a high energy intake, and on the long term a positive energy balance, leading to a higher body weight and a higher prevalence of obesity. In this paper it is argued that one of the psychobiological mechanisms behind these effects is related to oral processing characteristics such as a short oral residence time. Oral processing characteristics of foods that can be eaten or ingested quickly lead to a lack of adequate cephalic phase responses. Cephalic phase responses are the physiological response to sensory signals and inform the brain and gut about the inflow of nutrients. Inadequate sensory signaling with energy containing beverages results in an inadequate sensing of nutrients on the tongue producing an inadequate psychobiological satiation response. This paper starts with a short overview of long term studies that relate the consumption of of energy containing beverages (e.g. sugar sweetened soft-drinks) to energy balance and body weight. The central part of this paper consists of studies that assessed the effect of texture on satiation and satiety, and discusses a series of studies that looked at the causal mechanisms behind the effects of food
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texture on intake. The emphasis of the paper is on the effects of texture on satiation, i.e. meal termination. The term texture refers to the physical characteristics of a food, in this case specifically referring to the viscosity, varying from solid vs. liquid (beverage). A number of recent studies have studied the effect of slower or faster eating on the cephalic phase responses and physiological responses related to hunger and satiety. The discussion of this paper concerns a reflection of the main findings of the research area and a reflection on practical implications and future directions for research. 2. Calories from energy containing beverages, energy intake and body weight The results of various studies suggest that the consumption of energy containing beverages increases total daily energy intake, and on the long term body weight. Two classic intervention studies in this area are a study from Tordoff et al. [50] and a study from Raben et al. [38]. In the study of Tordoff et al. [50], 20 subjects consumed daily for 3 weeks either 1150 g of soda sweetened with aspartame, or 1150 g of soda sweetened with high fructose corn syrup. The results showed an increased energy intake and body weight in the sugar sweetened beverage group, and a stable energy intake and body weight in the aspartame group [50]. Average weight increase over three weeks in the high fructose corn syrup group was about 0.5 kg, whereas the aspartame group showed a statistically nonsignificant weight loss. In the study of Raben et al. [38], 21 overweight
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subjects consumed daily for 10 weeks about 150 g of sucrose mostly in the form of beverages, whereas another group of 20 subjects consumed the equivalent amount of products sweetened with artificial sweeteners. Also in this study, the sucrose group showed an increased energy intake and body weight, whereas in the artificial sweetener group, energy intake and body weight remained stable. Average body weight increased in the sucrose group by 1.3 kg, and decreased in sweetener group by 0.3 kg. In both studies, the energy from the liquid calories was added up to energy intake from other foods, and there was no decrease in the energy intake from other foods. Another by now classical study of DiMeglio and Mattes [12] investigated the effects of 4 weeks of daily ingestion of either a liquid or a solid carbohydrate preload (1.9 MJ; around 450 kcal) on food intake and body weight. The results of this study showed that liquid calories did not suppress the intake of other foods during the day, whereas solid calories did. Body weight changes in this study were congruent to the changes in total daily energy intake. A recently published randomized clinical trial from the same laboratory reported the effects of the provision of energy matched (400–550 kcal/20% of daily estimated energy needs) beverages or solid forms of fruits and vegetables during a period of 8 weeks in 34 subjects [21]. Dietary energy compensation was 53% in the beverage group and 78% in the solid group. The beverage treatment led to a weight gain of on average 1.95 kg of body weight, whereas the solid treatment led to an average weight gain of 1.36 kg [21]. A recently published study from Chen et al. [9] suggest that it also works the other way around, i.e. cutting out liquid calories also goes unnoticed, and therefore it leads to a decrease in energy intake and body weight. In a prospective behavioral intervention study of 18 months with 810 subjects, a reduction of liquid calories was related to a reduction in body weight. At 18 months, the highest tertile of reduction in sugar sweetened beverage intake had an average body weight loss of 5.2 kg, whereas the lowest tertile of reduction in sugar sweetened beverages had an average weight loss of 1.2 kg [9]. A reduction of liquid calories had a stronger effect on energy intake and body weight than the reduction of solid calories. The results of this study suggest that the liquid calories are not well sensed or noticed. The experimental data on the effect of sugar sweetened beverages on energy intake and body weight are generally supported by long term epidemiological cohort studies. For example, 8 years follow up from about 50,000 women from the Nurses' health Study II [42] suggested that increases in sugar sweetened beverages led to increases in body weight, whereas decreases in sugar sweetened beverages intake were associated with more stable weights. Systematic reviews on this issue arrive at a similar conclusion [22,31]. A word of caution is appropriate when we refer to liquid calories. The evidence with respect to the long term studies mainly refer to sugar sweetened beverages. Experimental data suggest that liquid calories that are consumed in the form of soup are more satiating than consumed as a drink (e.g. [34]; see Fig. 3). Flood and Rolls [14] showed that soup preloads in a variety of forms reduce meal energy intake. In a recently published study, Spill et al. [46] showed that serving large portion of vegetable soup at the start of a meal reduced meal energy intake in children. In a similar way, Hogenkamp et al. [19] showed that consuming a yoghurt drink with a spoon (resulting in a longer oro-sensory exposure time) leads to lower energy intake than consuming yoghurts with a straw, even after 10 exposures (see Fig. 5). These studies indicate that it is not the liquid texture per se that causes a low satiating efficiency of liquids; it is the high rate of consumption at which liquids are normally consumed [51] that is responsible for the low satiation/satiety effect. This idea is worked out below. 3. Two models of eating behavior, putting the effect of texture on food intake into perspective Fig. 1 shows a model by De Graaf and Kok [11], where eating behavior is guided by three separate factors. Sensory signals determine
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food choice; people choose/eat the foods they like, and avoid the foods that they dislike (e.g. [41]). Sensory signals are also responsible for the drive for variety in the diet through sensory specific satiety. For different aspects around the concept of sensory specific satiety the reader is referred to the original paper of [40], and the recently published papers of [6,16,17,36,39]. Metabolic signals, like satiety hormones, chemoreceptors and mechanoreceptors in the GI tract, are responsible for energy balance; they determine how much people eat (e.g. [55]). Every couple of hours, people get hungry, and go out to search for food. The most important part in this model is reflected in the central dimension, which refers to the learning component. Sensory signals from the food and from the environment get meaning in relation to the physiological, psychological and social consequences. For example, repeated exposure to chocolate will result in the “knowledge/cognition” that chocolate is a highly satiating food. After eating two sandwiches with cheese for breakfast for some time, one may “know” that two sandwiches with cheese is sufficient to stay satiated until lunch. In line with this idea, Hogenkamp et al. [20] recently showed that increasing viscosity/solidness in dairy products was associated with increasing expected satiety. Learning takes place at several levels; e.g. energy-taste conditioning results in an increased liking for tastes associated with higher energy levels in foods (e.g. [3,23,24]). Fig. 2 shows the satiety cascade from Blundell, of which various forms have been published in various papers (e.g. [4]). One of the principle characteristics of this cascade is that it nicely distinguishes between satiation, i.e. the processes that bring a meal to an end and satiety which refers to the processes between meals or eating occasions. One of the attractive features of this model is that it gives insight in the temporal pattern of hunger and satiety, and the related psycho-biological processes. From the model it is clear that sensory and cognitive factors will mainly play a role during satiation and the early satiety phase, whereas post-absorptive factors play a role later in time. Post-ingestive effects are intermediate in this respect. Texture may play a role in food intake through its effect on the oral residence time of taste substances on the tongue. The sense of taste functions as a sensor of nutrients, informing the brain and the gastrointestinal track about the inflow of nutrient. This effect of texture refers to the sensory factors in the model of Blundell, making it clear that this may act primarily on satiation. The cognitive factors as referred to in the previous paragraph are also mostly involved in satiation and early satiety. People may “know” that in general, more solid foods contain more energy than more liquid foods. In general, more solid foods will contain more energy delivering macronutrients than more liquid foods which will contain on average more water. The effect of texture may also work through its effect later on in the gastrointestinal track, e.g., through its effect on gastric emptying time, thereby affecting the exposure time of nutrients to nutrient sensors in the stomach and the gut. In this perspective, texture affects postingestive and post-absorptive factors (see e.g. [52]). The focus in this paper is on satiation. 4. Texture, satiation and food intake In a large series of recent studies, we showed that the fact that more solid foods lead to earlier meal termination than more liquid foods can be attributed to the length of oro-sensory exposure time. The concept of the role of oro sensory exposure time is well illustrated by an old study of Haber et al. [15], who compared the time to consume 500 g of apples or 500 g of apple juice. It took subjects about 10 × more time (17.5 min) to ingest 500 g of apples compared to the 1.5 min to ingest the apple juice. This implies that the contact time of taste substances to the taste system on the tongue is more than 10 × higher in case of the apples than in case of the apple juice. The apples appeared to be more satiating than the apple juice [15]. In a later elegant study, Mattes [34] compared the satiating efficiency
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Fig. 1. Factors effecting eating behavior. Sensory processes determine what we eat, and are also responsible for variety in the diet. Metabolic processes determine how much we eat. In the brain sensory signals during eating are linked to the metabolic consequences. These (largely unconscious) learning processes shape our nutrition pattern. The softbackground of foods represents our current day food environment (adapted from [11]).
of whole apples and apple juice to the satiating effect of apple soup. The apple soup was warm and eaten with a spoon. Fig. 3 shows that the whole apples and the apple soup had an equivalent hunger suppressing effect and this satiating effect was considerably higher than the satiating effect of the apple juice. In an attempt to find out why more solid foods are more satiating than more liquid foods, Zijlstra et al. carried out two studies. In a first real life study carried out in a cinema, Zijlstra et al. [59] showed that the ad libitum consumption of chocolate milk (>800 g) was about 30% higher than of chocolate custard (about 550 g) (see Fig. 4). The chocolate milk and custard had equivalent macronutrient compositions and they were similar with respect to liking. When asked how much they perceived to have ingested, subjects reported similar amounts for the milk and the custard. In a second laboratory study, the eating rates of the chocolate milk and chocolate custard were standardized with the help of a peristaltic pump (see Fig. 4). The peristaltic pump operated through a plastic tube that was filled with chocolate milk/custard, and subjects had only to open their mouth and swallow to ingest the chocolate milk/custard. The standardized eating rates of 40 g/min for men and 50 g/min for women for both the milk and the custard led to similar ad libitum food intakes. This study indicates that, just as in the study of Mattes [34] it is not texture per se that affects meal termination; it is the rate of eating that is important.
Fig. 2. Satiety cascade adapted from Blundell et al. [4]. The satiety cascade identifies different processes related to food intake. Satiation refers to the processes that bring a meal or eating occasion to an end; satiety refers to motivations to eat in between meals, it is usually low just after meal termination and high just before a meal. Sensory, cognitive, post-ingestive and post-absorptive factors play a role at different stages during the food intake cycle. Sensory and cognitive factors play a role during satiation and early satiety. Post-ingestive effects may play a role during satiation, but mainly during later stages of satiety. Post-absorptive effects concern later stages of satiety (adapted from [4]).
In a later study, Zijlstra et al. independently manipulated bite size (5 g or 15 g) and oral residence time of each bite (3 s or 9 s) of chocolate custard. Again, subjects were instructed to eat until comfortably full. The results showed that increasing bit size led to higher ad libitum intakes, whereas increasing oral residence time led to a decrease of ad libitum intake. A second cinema study [60,61] with comparable environmental conditions as the first cinema chocolate milk/ custard study [62] was carried with solid foods with meat replacers, luncheon meat and hard candies. This led to much lower ad libitum intakes around 150–250 g (compared to 550–800 g for chocolate milk and custard). Also in this case, ad libitum intakes co varied with eating rate, with higher eating rates leading to higher ad libitum intakes. With the normal eating or regular consumption of food, eating rate negatively relates to oro-sensory exposure times. This makes it difficult to separate the effects from eating rate per se on ad libitum intake from the effect of oro-sensory exposure time per se on ad libitum intake. The experimental separation of these effects was done in two later studies, one of Weijzen et al. [53], and one of Bolhuis et al. [5]. In both studies, eating/ingestion rate was held constant (150 g/min in Weijzen et al. [53], and 60 g/min in Bolhuis et al. [5]), but the oro sensory exposure time was varied by manipulating the sip size. A higher sips size leads to lower oro-sensory exposure time; in both Weijzen et al. [53] and Bolhuis [5], the oro-sensory exposure time varied by a factor 2. Weijzen et al. [53] used orange flavoured lemonades, whereas Bolhuis et al. [5] used tomato soups. In both studies, doubling the oro-sensory exposure time led to a 30–35% lower ad libitum food intake.
Fig. 3. Hunger response before and after consuming 300 kcal of apples (508 g), apple juice (652 g) or apple soup (652 g) by 31 subjects. Apples and apple juice were served cold, the apple soup was served at 60 C. (Source: [34]).
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Fig. 5. Mean +/1 s.e.m. ad libitum intake of semi-solid (dotted line; n = 35) and liquid yoghurts (dashed, n = 34 and solid, n = 36 line) across 10 days for breakfast. The semisolid yoghurt was consumed with a spoon. The liquid yoghurt represented by the dashed line (upper curve) was consumed through a straw, and the liquid yoghurt with the dotted line was consumed with a straw. Eating rate with the liquid yoghurt with a straw was higher (on average 132 g/min) than the eating rates of liquid yoghurt eaten with a spoon (on average 105 g/min) and the semi-solid yoghurt (on averge 106 g/min). Source: [19].
repeated exposures. In a recently published study with custards that varied from liquid to solid [20], it was shown that expected satiation as introduced by Brunstrom et al. [7] was strongly dependent on the texture of the custard. The more solid a food is, the higher its expected satiation. A recently published study from Li et al. [29] varied the number of chews of each piece of food eaten. They showed both with a group of lean and with a group of obese subjects, that more chewing led to lower ad libitum intakes. As more chewing is directly related to a longer oro-sensory exposure time, this result is congruent with the results of the studies above. The results of several other studies also indicate that slower eating leads to a lower ad libitum intake [2,51]. Altogether, these studies suggest that texture has a large effect on satiation. More solid textures lead to lower ad libitum intakes. This effect of texture is mediated by the length of the oro-sensory exposure time. These results are congruent with the idea that the taste system is a nutrient sensing system that informs the brain and the GI tract about the inflow of nutrients. The sense of taste signals the inflow of nutrients or the inflow of energy, and thereby satiety. Fig. 4. Upper panel: Ad libitum intake in grams +/− sd and in energy intake (kJ) of the liquid, semi liquid and semi-solid chocolate dairy products in a cinema setting (n = 108; within subjects). Test products were similar in palatability, energy and macronutrient content, and consumed through a straw from 1.5 l carton boxes over a period of about 90 min. Intake from the semi-solid was 30% lesser than from the liquid testfood. Lower panel: Ad libitum intake in grams +/− sd and in energy intake (kJ) of the liquid and semi-solid chocolate dairy product in a laboratory setting (sensory cabin) (n = 49; within subjects) within a time frame of about 15 min. In the free eating rate, different effort, subjects consumed the products in the same way as in the cinema setting. In the free eating rate, no effort, subjects consumed the product from a tube making use of a peristaltic pump; in this condition subjects could adjust the rate of delivery. In the fixed eating rate, no effort condition, investigators set the rate of delivery of the test-products into the mouth of the subjects. (Source: [59]).
The results of three studies of Mars et al. [32] and Hogenkamp et al. [19,20] are also in line with the concept that it is the oro-sensory exposure time that is the crucial variable with respect to satiation. In two studies with low- and high energy dense semi-solid and liquid yoghurt(s) (drinks), it was shown that the liquid version of the yoghurt resulted in a higher ad libitum intake than the semi-solid version with equivalent energy densities and palatabilities [19,32]. However, in the latter study [19] when the liquid version of the yoghurt was eaten with a spoon, instead of drunken with straw, this resulted in an equivalent intake as the semi-solid version of the yoghurt which was also consumed with a straw. Fig. 5 shows that this effect was apparent not only at the first exposure, but also after
5. Why do fast liquid calories lead to a higher energy intake; the role of cephalic phase responses as an explanatory mechanism Cephalic phase responses reflect the initial anticipatory physiological response to the sensory signals coming from food. Even the thought of food can trigger this response [13,35,56]. Cephalic phase responses are conceived to inform the brain and the GI tract on the inflow of coming nutrients [43,58]. Initial cephalic phase responses to an attractive stimulus enhance hunger [57], but the continued cephalic phase response may have a significant contribution to satiation [43]. Cephalic phase responses are predominantly learned and include not only saliva flow, gastric acid release, digestive peptide release, but also pancreatic polypeptide, insulin and ghrelin release [58]. The role of the cephalic phase insulin response in glucose tolerance was nicely shown in a study of Teff and Engelman [47], who showed that oral glucose tolerance to a gastric load of 75 g of glucose improved when subject sham fed (chew and spit out) a peanut butter sandwich. Teff and colleagues [49] also investigated the cephalic phase response to sugars and artificial sweeteners. She concluded that drinks with either sucrose, glucose or aspartame did not elicit a cephalic phase response. However, apple pie did elicit a cephalic phase insulin response [49]. In a recently published study Teff et al. [48] investigated cephalic phase responses to simple sweet and salty tasting liquids,
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different types of chewing gum, and some real mixed solid foods. The results of this study suggested that the liquids and the chewing gum were not good elicitors of a cephalic phase response. Only the mixed solid foods led to a substantial cephalic phase response [48]. The results of another series of recently published studies suggest that longer oral sensory exposure times, either induced by sham feeding or by slower eating/more chewing elicit physiological and subjective responses that are congruent with higher satiety feelings. For example, Heath et al. [18] showed that modified sham feeding before an intragastric fat load led to a stronger decrease in ghrelin levels, and higher feelings of satisfaction. Two studies of Smeets et al. [44,45] suggest that modified sham feeding of fatty foods result in higher satiety response and/or lower ghrelin levels. Consuming a meal in 30 min compared to consuming the same meal in 5 min led to higher responses of the satiety hormones PYY and GLP1 [25]. Li et al. [29] showed that chewing food for longer compared to chewing food for shorter led to lower ad libitum intake and higher GLP-1 and PYY responses. One interesting question is this respect is how oral and gastric signals contribute to satiety. In an elegant study, Cecil et al. [8] showed that intragastric or intraduodenal loads of tomato soup led to modest decreases in hunger responses. When soup was consumed orally through the same tube as in the intra-gastric conditions, this led to significantly higher satiety responses (see Fig. 6). This study strongly suggests that there is a strong contribution of the oro-sensory signal to satiety. Wijlens et al. [54] independently manipulated gastric volume (0, 100 or 800 ml, through a naso-gastric tube) and oro-sensory exposure time (0, 1 and 8 min of modified sham feeding). In this study, 8 min sensory exposure had a stronger effect on subsequent satiety and ad libitum test‐meal intake than the 800 ml (100 kcal) intragastric load. Altogether, these studies show, that longer sensory exposure times lead to cephalic phase responses, that not only contribute to physiological homeostasis, but also significantly contribute to satiety. These results are in line with the concept of the sense of taste as a nutrient sensor, which inform the brain and the GI tract of the inflow of nutrients. 6. Discussion The results of numerous studies suggest that the effect of texture on food intake is mediated by the oro-sensory exposure time, or the
Fig. 6. The effect of soup given orally (filled black circles), overtly intragastricly (filled black squares), covertly intragastricly (open squares), and intraduodenally (open triangles) on hunger ratings. Values are expressed as mean +/−s.e.m. (n= 9). Source: [8].
oral residence time of food in the mouth. The studies on the cephalic phase response, and the studies on oral and gastric contributions to satiety show that one needs a considerable amount of time of food in the mouth before the sensory signals lead to a substantial physiological/subjective satiety response. These data are in line with the notion that the sense of taste monitors the inflow of nutrients, and has an important contribution to satiety. With simple liquid foods like sugar sweetened beverages, this system is bypassed, and the calories enter the body more or less unoticed. Within this context it is good to notice, that the short term behavioral studies on the lack of a compensatory response to simple liquid caloric beverages (e.g. [33]) are in line with longer term nutrition intervention studies [12,38,50]. The results of the intervention studies are in line with the epidemiological literature on the effects of sugar sweetened beverages on the prevalence of obesity [31,42]. These findings are reinforced by the notion of the lack of cephalic phase stimulation with liquids [48]. The effect of texture on food intake seems more clear when studying satiation compared to studying satiety. For example, Zijlstra et al. [59] showed that the ad libitum intake of a liquid flavoured dairy product was about 30% higher than the ad libitum intake of the semi solid version of the same product. In a subsequent study, Zijlstra et al. [61] showed that the fixed intake of 300–400 g of the liquid and semo-solid version led to about similar changes in hunger responses during the 90-min after ingestion. For texture effect on satiety one may need considerable differences in structure like the difference between a solid and a liquid version of a food (see [15,27]). The idea that texture has a stronger effect on satiation than satiety fits with the satiety cascade of Blundell [4], which show that cognitive and sensory effects have a major impact on satiation and less so on satiety (see also [10]). The notion that texture effects are more obvious with satiation than with satiety does not mean that texture has no impact on satiety. It does. Recent systematic reviews on the effects of dietary fire on satiety and food intake show that food with fibres that are more viscous/more gelling lead to higher satiety responses and a lower subsequent food intake than foods that are less viscous/gelling [26,52]. This suggests that the volume or contact time of foods with nutrient sensors in the stomach and gut have a signifiant impact on satiety. In this way, in relation to the satiety cascade of Blundell, texture affects satiety also through post-ingestive and post-absorptive effects. Liquids vs. semi-solid foods lead to substantial differences in satiation and satiety. One key question is whether or not not this also holds for comparable solid products. Do products that are chewed or consumed for longer also lead to significant differences in intake? The results of Zijlstra et al. [62] showed that also for solid foods, a higher eating rate was related to a higher ad libitum intake. However, within pairs of similar foods with slightly different textures she could not demonstrate a difference in intake [62]. Li et al. [29] showed that increasing the number of chews from 15 to 40 chews led to a lower ad libitum intake. This suggests that one needs conserable differences in eating rate/oral residence time to signifiantly lower food intake. One important research question that remains to be answered is whether or not texture differences in realistic foods that can be exchanged for each other in the commercial market place lead to lower intake. Can commercial food companies use the proofs of principles of the effects of texture on satiety to design food that promote earlier satiation and/or a longer satiety response? Several food companies are working and/or have been working on this [1,30,37]. Within the context of the present paper on the effects of texture on satiation, it should first be shown that a regularly consumed meal with longer oral processing time leads to a lower ad libitum intake. Next, one would like to have evidence that the lower intake is not compensated later on the day. Recent data from Levitsky & Pacanowski [28] suggest that people are unlikely to compensate for
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moderate lower decreases in food intake during one meal. The final challenge will be to test these proofs of principles in longer term studies. In the end, such studies may contribute to a food supply that is less obesogenic. Another important research area in the future is the characterization of cephalic phase responses. As is clear from the results of various studies, cephalic phase responses have a substantial contribution to satiation and satiety. It seems also well established that one needs solid foods with a substiantal oral residence time to produce a cepahlic phase response. However, it is not yet clear how different tastes and different macronutrient may contribute to a cephalic phase response, and therefore also contribute to satiety.
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Sucrose compared with artificial sweeteners: different effect on ad libitum food intake and body weight after 10 wk of supplementation in overweight subjects. Am J Clin Nutr 2002;76:721–9. [39] Remick AK, Polivy J, Pliner P. Internal and external moderators of the effect of variety on food intake. Psychol Bull 2009;135:434–51. [40] Rolls BJ, Rowe EA, Rolls ET, Kingston B, Megson A, Gunary R. Variety in a meal enhances food intake in man (1981. Physiol Behav 1981;26:215–21. [41] Rozin P, Vollmecke TA. Food like and dislikes. Annu Rev Nutr 1986;6:433–56. [42] Schulze MB, Manson JE, Ludwig DS, Colditz GA, Stampfer MJ, Willet WC, et al. Sugar-sweetened beverages, weight gain, and incidence of type 2 diabetes in young and middle-aged women. J Am Med Assoc 2004;292:927–34. [43] Smeets PAM, Erkner A, de Graaf C. Cephalic phase responses and appetite. Nutr Rev 2010;68:643–55. [44] Smeets AJ, Lejeune MP, Westerterp-Plantenga MS. Effects of oral fat perception by modified sham feeding on energy expenditure, hormones and appetite profiles in the postprandial state. Br J Nutr 2009;101:1360–8. [45] Smeets AJPG, Westerterp-Plantenga MS. Satiety and substrate mobilization after oral fat stimulation. Br J Nutr 2006;95:795–801. [46] Spill MK, Birch LL, Roe LS, Rolls BJ. Serving large portions of vegetable soup at the start of a meal affected children's energy and vegetable intake. Appetite 2011;57: 213–9. [47] Teff KL, Engelman K. Oral sensory stimulation improves glucose tolerance: effects on post-prandial glucose, insulin, C-peptide and glucagon. Am J Physiol 1996;270: R1371–9. [48] Teff KL. Cehalic phase pancreatic polypeptide response to liquid and solid stimuli in humans. Physiol Behav 2010;99:317–23. [49] Teff KL, Devine J, Engelman K. Sweet taste: effect on cephalic insulin release in men. Physiol Behav 1995;57:1089–95. [50] Tordoff MG, Alleva AM. 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The control of food intake: behavioral vs. molecular approaches. Cell Metab 2009;9:489–98. [56] Wooley SC, Wooley OW. Salivation to the sight and thought of food: a new measure of appetite. Psychosom Med 1973;35:136–42. [57] Yeomans MR. Palatability and the micro-structure of feeding in humans: the appetizer effect. Appetite 1996;27:119–33. [58] Zafra MA, Moilia F, Puerto A. The neural/cephalic phase reflexes in the physiology of nutrition. Neurosci Biobehav Rev 2006;30:1032–44. [59] Zijlstra N, Mars M, de Wijk RA, Westerterp-Plantenga MS, de Graaf C. The effect of viscosity on ad libitum food intake. Int J Obes 2008;32:676–83. [60] Zijlstra N, de Wijk RA, Mars M, Stafleu A, de Graaf C. Effect of bite size and oral processing time of a semisolid food on satiation. Am J Clin Nutr 2009;90:269–75. [61] Zijlstra N, Mars M, de Wijk RA, Westerterp-Plantenga MS, Holst JJ, de Graaf C. Effect of viscosity on appetite and gastro-intestinal hormones. Physiol Behav 2009;97:68–75. 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Texture and satiation: The role of oro-sensory exposure time Cees de Graaf ⁎ Division of Human Nutrition, Wageningen University, P.O. Box 8129, 6700 EV Wageningen, The Netherlands
a r t i c l e
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Article history: Received 16 February 2012 Received in revised form 6 May 2012 Accepted 8 May 2012 Keywords: Texture Food intake Cephalic phase response Satiation Satiety Appetite Sensory Taste
a b s t r a c t One of the characteristics of the current obesogenic food supply is the large availability of foods that can be ingested quickly. Controlled nutrition intervention studies have shown that the ingestion of simple energy containing beverages, which are consumed very quickly, do not lead to a lower compensatory intake of other foods. One of the theories behind this observation is that calories that are ingested quickly are not well sensed by the sense of taste, and do not lead to an adequate satiety response. This idea is confirmed by the results of a series of studies, where we have shown that the low satiation/satiety response of beverages can be largely attributed to their short oral residence time. Prolonging the oro-sensory exposure time to foods leads to earlier meal termination and/or a higher satiety response. The low satiation/satiety response to simple energy containing beverages is congruent with the observation from studies on the cephalic phase response to foods, i.e. the physiological response to sensory signals. Energy containing beverages do not lead to an adequate cephalic phase response. Various recent studies showed that slower eating leads to higher levels of satiety hormones. These results are in line with the idea that the sense of taste is a nutrient sensor which informs the brain and the gut about the inflow of nutrients. The sense of taste has an important contribution to the satiating effect of foods. One of the challenges in future research is to see whether or not these proofs of principles can be applied in longer term studies with regular commercial foods. This may make our obesogenic food supply more satiating, and may lead to a lower energy intake. © 2012 Published by Elsevier Inc.
1. Introduction The obesogenic food supply is characterized by a large variety of energy containing softly textured foods with large portion sizes that can be eaten quickly. These foods may promote a high energy intake, and on the long term a positive energy balance, leading to a higher body weight and a higher prevalence of obesity. In this paper it is argued that one of the psychobiological mechanisms behind these effects is related to oral processing characteristics such as a short oral residence time. Oral processing characteristics of foods that can be eaten or ingested quickly lead to a lack of adequate cephalic phase responses. Cephalic phase responses are the physiological response to sensory signals and inform the brain and gut about the inflow of nutrients. Inadequate sensory signaling with energy containing beverages results in an inadequate sensing of nutrients on the tongue producing an inadequate psychobiological satiation response. This paper starts with a short overview of long term studies that relate the consumption of of energy containing beverages (e.g. sugar sweetened soft-drinks) to energy balance and body weight. The central part of this paper consists of studies that assessed the effect of texture on satiation and satiety, and discusses a series of studies that looked at the causal mechanisms behind the effects of food
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texture on intake. The emphasis of the paper is on the effects of texture on satiation, i.e. meal termination. The term texture refers to the physical characteristics of a food, in this case specifically referring to the viscosity, varying from solid vs. liquid (beverage). A number of recent studies have studied the effect of slower or faster eating on the cephalic phase responses and physiological responses related to hunger and satiety. The discussion of this paper concerns a reflection of the main findings of the research area and a reflection on practical implications and future directions for research. 2. Calories from energy containing beverages, energy intake and body weight The results of various studies suggest that the consumption of energy containing beverages increases total daily energy intake, and on the long term body weight. Two classic intervention studies in this area are a study from Tordoff et al. [50] and a study from Raben et al. [38]. In the study of Tordoff et al. [50], 20 subjects consumed daily for 3 weeks either 1150 g of soda sweetened with aspartame, or 1150 g of soda sweetened with high fructose corn syrup. The results showed an increased energy intake and body weight in the sugar sweetened beverage group, and a stable energy intake and body weight in the aspartame group [50]. Average weight increase over three weeks in the high fructose corn syrup group was about 0.5 kg, whereas the aspartame group showed a statistically nonsignificant weight loss. In the study of Raben et al. [38], 21 overweight
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subjects consumed daily for 10 weeks about 150 g of sucrose mostly in the form of beverages, whereas another group of 20 subjects consumed the equivalent amount of products sweetened with artificial sweeteners. Also in this study, the sucrose group showed an increased energy intake and body weight, whereas in the artificial sweetener group, energy intake and body weight remained stable. Average body weight increased in the sucrose group by 1.3 kg, and decreased in sweetener group by 0.3 kg. In both studies, the energy from the liquid calories was added up to energy intake from other foods, and there was no decrease in the energy intake from other foods. Another by now classical study of DiMeglio and Mattes [12] investigated the effects of 4 weeks of daily ingestion of either a liquid or a solid carbohydrate preload (1.9 MJ; around 450 kcal) on food intake and body weight. The results of this study showed that liquid calories did not suppress the intake of other foods during the day, whereas solid calories did. Body weight changes in this study were congruent to the changes in total daily energy intake. A recently published randomized clinical trial from the same laboratory reported the effects of the provision of energy matched (400–550 kcal/20% of daily estimated energy needs) beverages or solid forms of fruits and vegetables during a period of 8 weeks in 34 subjects [21]. Dietary energy compensation was 53% in the beverage group and 78% in the solid group. The beverage treatment led to a weight gain of on average 1.95 kg of body weight, whereas the solid treatment led to an average weight gain of 1.36 kg [21]. A recently published study from Chen et al. [9] suggest that it also works the other way around, i.e. cutting out liquid calories also goes unnoticed, and therefore it leads to a decrease in energy intake and body weight. In a prospective behavioral intervention study of 18 months with 810 subjects, a reduction of liquid calories was related to a reduction in body weight. At 18 months, the highest tertile of reduction in sugar sweetened beverage intake had an average body weight loss of 5.2 kg, whereas the lowest tertile of reduction in sugar sweetened beverages had an average weight loss of 1.2 kg [9]. A reduction of liquid calories had a stronger effect on energy intake and body weight than the reduction of solid calories. The results of this study suggest that the liquid calories are not well sensed or noticed. The experimental data on the effect of sugar sweetened beverages on energy intake and body weight are generally supported by long term epidemiological cohort studies. For example, 8 years follow up from about 50,000 women from the Nurses' health Study II [42] suggested that increases in sugar sweetened beverages led to increases in body weight, whereas decreases in sugar sweetened beverages intake were associated with more stable weights. Systematic reviews on this issue arrive at a similar conclusion [22,31]. A word of caution is appropriate when we refer to liquid calories. The evidence with respect to the long term studies mainly refer to sugar sweetened beverages. Experimental data suggest that liquid calories that are consumed in the form of soup are more satiating than consumed as a drink (e.g. [34]; see Fig. 3). Flood and Rolls [14] showed that soup preloads in a variety of forms reduce meal energy intake. In a recently published study, Spill et al. [46] showed that serving large portion of vegetable soup at the start of a meal reduced meal energy intake in children. In a similar way, Hogenkamp et al. [19] showed that consuming a yoghurt drink with a spoon (resulting in a longer oro-sensory exposure time) leads to lower energy intake than consuming yoghurts with a straw, even after 10 exposures (see Fig. 5). These studies indicate that it is not the liquid texture per se that causes a low satiating efficiency of liquids; it is the high rate of consumption at which liquids are normally consumed [51] that is responsible for the low satiation/satiety effect. This idea is worked out below. 3. Two models of eating behavior, putting the effect of texture on food intake into perspective Fig. 1 shows a model by De Graaf and Kok [11], where eating behavior is guided by three separate factors. Sensory signals determine
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food choice; people choose/eat the foods they like, and avoid the foods that they dislike (e.g. [41]). Sensory signals are also responsible for the drive for variety in the diet through sensory specific satiety. For different aspects around the concept of sensory specific satiety the reader is referred to the original paper of [40], and the recently published papers of [6,16,17,36,39]. Metabolic signals, like satiety hormones, chemoreceptors and mechanoreceptors in the GI tract, are responsible for energy balance; they determine how much people eat (e.g. [55]). Every couple of hours, people get hungry, and go out to search for food. The most important part in this model is reflected in the central dimension, which refers to the learning component. Sensory signals from the food and from the environment get meaning in relation to the physiological, psychological and social consequences. For example, repeated exposure to chocolate will result in the “knowledge/cognition” that chocolate is a highly satiating food. After eating two sandwiches with cheese for breakfast for some time, one may “know” that two sandwiches with cheese is sufficient to stay satiated until lunch. In line with this idea, Hogenkamp et al. [20] recently showed that increasing viscosity/solidness in dairy products was associated with increasing expected satiety. Learning takes place at several levels; e.g. energy-taste conditioning results in an increased liking for tastes associated with higher energy levels in foods (e.g. [3,23,24]). Fig. 2 shows the satiety cascade from Blundell, of which various forms have been published in various papers (e.g. [4]). One of the principle characteristics of this cascade is that it nicely distinguishes between satiation, i.e. the processes that bring a meal to an end and satiety which refers to the processes between meals or eating occasions. One of the attractive features of this model is that it gives insight in the temporal pattern of hunger and satiety, and the related psycho-biological processes. From the model it is clear that sensory and cognitive factors will mainly play a role during satiation and the early satiety phase, whereas post-absorptive factors play a role later in time. Post-ingestive effects are intermediate in this respect. Texture may play a role in food intake through its effect on the oral residence time of taste substances on the tongue. The sense of taste functions as a sensor of nutrients, informing the brain and the gastrointestinal track about the inflow of nutrient. This effect of texture refers to the sensory factors in the model of Blundell, making it clear that this may act primarily on satiation. The cognitive factors as referred to in the previous paragraph are also mostly involved in satiation and early satiety. People may “know” that in general, more solid foods contain more energy than more liquid foods. In general, more solid foods will contain more energy delivering macronutrients than more liquid foods which will contain on average more water. The effect of texture may also work through its effect later on in the gastrointestinal track, e.g., through its effect on gastric emptying time, thereby affecting the exposure time of nutrients to nutrient sensors in the stomach and the gut. In this perspective, texture affects postingestive and post-absorptive factors (see e.g. [52]). The focus in this paper is on satiation. 4. Texture, satiation and food intake In a large series of recent studies, we showed that the fact that more solid foods lead to earlier meal termination than more liquid foods can be attributed to the length of oro-sensory exposure time. The concept of the role of oro sensory exposure time is well illustrated by an old study of Haber et al. [15], who compared the time to consume 500 g of apples or 500 g of apple juice. It took subjects about 10 × more time (17.5 min) to ingest 500 g of apples compared to the 1.5 min to ingest the apple juice. This implies that the contact time of taste substances to the taste system on the tongue is more than 10 × higher in case of the apples than in case of the apple juice. The apples appeared to be more satiating than the apple juice [15]. In a later elegant study, Mattes [34] compared the satiating efficiency
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Fig. 1. Factors effecting eating behavior. Sensory processes determine what we eat, and are also responsible for variety in the diet. Metabolic processes determine how much we eat. In the brain sensory signals during eating are linked to the metabolic consequences. These (largely unconscious) learning processes shape our nutrition pattern. The softbackground of foods represents our current day food environment (adapted from [11]).
of whole apples and apple juice to the satiating effect of apple soup. The apple soup was warm and eaten with a spoon. Fig. 3 shows that the whole apples and the apple soup had an equivalent hunger suppressing effect and this satiating effect was considerably higher than the satiating effect of the apple juice. In an attempt to find out why more solid foods are more satiating than more liquid foods, Zijlstra et al. carried out two studies. In a first real life study carried out in a cinema, Zijlstra et al. [59] showed that the ad libitum consumption of chocolate milk (>800 g) was about 30% higher than of chocolate custard (about 550 g) (see Fig. 4). The chocolate milk and custard had equivalent macronutrient compositions and they were similar with respect to liking. When asked how much they perceived to have ingested, subjects reported similar amounts for the milk and the custard. In a second laboratory study, the eating rates of the chocolate milk and chocolate custard were standardized with the help of a peristaltic pump (see Fig. 4). The peristaltic pump operated through a plastic tube that was filled with chocolate milk/custard, and subjects had only to open their mouth and swallow to ingest the chocolate milk/custard. The standardized eating rates of 40 g/min for men and 50 g/min for women for both the milk and the custard led to similar ad libitum food intakes. This study indicates that, just as in the study of Mattes [34] it is not texture per se that affects meal termination; it is the rate of eating that is important.
Fig. 2. Satiety cascade adapted from Blundell et al. [4]. The satiety cascade identifies different processes related to food intake. Satiation refers to the processes that bring a meal or eating occasion to an end; satiety refers to motivations to eat in between meals, it is usually low just after meal termination and high just before a meal. Sensory, cognitive, post-ingestive and post-absorptive factors play a role at different stages during the food intake cycle. Sensory and cognitive factors play a role during satiation and early satiety. Post-ingestive effects may play a role during satiation, but mainly during later stages of satiety. Post-absorptive effects concern later stages of satiety (adapted from [4]).
In a later study, Zijlstra et al. independently manipulated bite size (5 g or 15 g) and oral residence time of each bite (3 s or 9 s) of chocolate custard. Again, subjects were instructed to eat until comfortably full. The results showed that increasing bit size led to higher ad libitum intakes, whereas increasing oral residence time led to a decrease of ad libitum intake. A second cinema study [60,61] with comparable environmental conditions as the first cinema chocolate milk/ custard study [62] was carried with solid foods with meat replacers, luncheon meat and hard candies. This led to much lower ad libitum intakes around 150–250 g (compared to 550–800 g for chocolate milk and custard). Also in this case, ad libitum intakes co varied with eating rate, with higher eating rates leading to higher ad libitum intakes. With the normal eating or regular consumption of food, eating rate negatively relates to oro-sensory exposure times. This makes it difficult to separate the effects from eating rate per se on ad libitum intake from the effect of oro-sensory exposure time per se on ad libitum intake. The experimental separation of these effects was done in two later studies, one of Weijzen et al. [53], and one of Bolhuis et al. [5]. In both studies, eating/ingestion rate was held constant (150 g/min in Weijzen et al. [53], and 60 g/min in Bolhuis et al. [5]), but the oro sensory exposure time was varied by manipulating the sip size. A higher sips size leads to lower oro-sensory exposure time; in both Weijzen et al. [53] and Bolhuis [5], the oro-sensory exposure time varied by a factor 2. Weijzen et al. [53] used orange flavoured lemonades, whereas Bolhuis et al. [5] used tomato soups. In both studies, doubling the oro-sensory exposure time led to a 30–35% lower ad libitum food intake.
Fig. 3. Hunger response before and after consuming 300 kcal of apples (508 g), apple juice (652 g) or apple soup (652 g) by 31 subjects. Apples and apple juice were served cold, the apple soup was served at 60 C. (Source: [34]).
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Fig. 5. Mean +/1 s.e.m. ad libitum intake of semi-solid (dotted line; n = 35) and liquid yoghurts (dashed, n = 34 and solid, n = 36 line) across 10 days for breakfast. The semisolid yoghurt was consumed with a spoon. The liquid yoghurt represented by the dashed line (upper curve) was consumed through a straw, and the liquid yoghurt with the dotted line was consumed with a straw. Eating rate with the liquid yoghurt with a straw was higher (on average 132 g/min) than the eating rates of liquid yoghurt eaten with a spoon (on average 105 g/min) and the semi-solid yoghurt (on averge 106 g/min). Source: [19].
repeated exposures. In a recently published study with custards that varied from liquid to solid [20], it was shown that expected satiation as introduced by Brunstrom et al. [7] was strongly dependent on the texture of the custard. The more solid a food is, the higher its expected satiation. A recently published study from Li et al. [29] varied the number of chews of each piece of food eaten. They showed both with a group of lean and with a group of obese subjects, that more chewing led to lower ad libitum intakes. As more chewing is directly related to a longer oro-sensory exposure time, this result is congruent with the results of the studies above. The results of several other studies also indicate that slower eating leads to a lower ad libitum intake [2,51]. Altogether, these studies suggest that texture has a large effect on satiation. More solid textures lead to lower ad libitum intakes. This effect of texture is mediated by the length of the oro-sensory exposure time. These results are congruent with the idea that the taste system is a nutrient sensing system that informs the brain and the GI tract about the inflow of nutrients. The sense of taste signals the inflow of nutrients or the inflow of energy, and thereby satiety. Fig. 4. Upper panel: Ad libitum intake in grams +/− sd and in energy intake (kJ) of the liquid, semi liquid and semi-solid chocolate dairy products in a cinema setting (n = 108; within subjects). Test products were similar in palatability, energy and macronutrient content, and consumed through a straw from 1.5 l carton boxes over a period of about 90 min. Intake from the semi-solid was 30% lesser than from the liquid testfood. Lower panel: Ad libitum intake in grams +/− sd and in energy intake (kJ) of the liquid and semi-solid chocolate dairy product in a laboratory setting (sensory cabin) (n = 49; within subjects) within a time frame of about 15 min. In the free eating rate, different effort, subjects consumed the products in the same way as in the cinema setting. In the free eating rate, no effort, subjects consumed the product from a tube making use of a peristaltic pump; in this condition subjects could adjust the rate of delivery. In the fixed eating rate, no effort condition, investigators set the rate of delivery of the test-products into the mouth of the subjects. (Source: [59]).
The results of three studies of Mars et al. [32] and Hogenkamp et al. [19,20] are also in line with the concept that it is the oro-sensory exposure time that is the crucial variable with respect to satiation. In two studies with low- and high energy dense semi-solid and liquid yoghurt(s) (drinks), it was shown that the liquid version of the yoghurt resulted in a higher ad libitum intake than the semi-solid version with equivalent energy densities and palatabilities [19,32]. However, in the latter study [19] when the liquid version of the yoghurt was eaten with a spoon, instead of drunken with straw, this resulted in an equivalent intake as the semi-solid version of the yoghurt which was also consumed with a straw. Fig. 5 shows that this effect was apparent not only at the first exposure, but also after
5. Why do fast liquid calories lead to a higher energy intake; the role of cephalic phase responses as an explanatory mechanism Cephalic phase responses reflect the initial anticipatory physiological response to the sensory signals coming from food. Even the thought of food can trigger this response [13,35,56]. Cephalic phase responses are conceived to inform the brain and the GI tract on the inflow of coming nutrients [43,58]. Initial cephalic phase responses to an attractive stimulus enhance hunger [57], but the continued cephalic phase response may have a significant contribution to satiation [43]. Cephalic phase responses are predominantly learned and include not only saliva flow, gastric acid release, digestive peptide release, but also pancreatic polypeptide, insulin and ghrelin release [58]. The role of the cephalic phase insulin response in glucose tolerance was nicely shown in a study of Teff and Engelman [47], who showed that oral glucose tolerance to a gastric load of 75 g of glucose improved when subject sham fed (chew and spit out) a peanut butter sandwich. Teff and colleagues [49] also investigated the cephalic phase response to sugars and artificial sweeteners. She concluded that drinks with either sucrose, glucose or aspartame did not elicit a cephalic phase response. However, apple pie did elicit a cephalic phase insulin response [49]. In a recently published study Teff et al. [48] investigated cephalic phase responses to simple sweet and salty tasting liquids,
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different types of chewing gum, and some real mixed solid foods. The results of this study suggested that the liquids and the chewing gum were not good elicitors of a cephalic phase response. Only the mixed solid foods led to a substantial cephalic phase response [48]. The results of another series of recently published studies suggest that longer oral sensory exposure times, either induced by sham feeding or by slower eating/more chewing elicit physiological and subjective responses that are congruent with higher satiety feelings. For example, Heath et al. [18] showed that modified sham feeding before an intragastric fat load led to a stronger decrease in ghrelin levels, and higher feelings of satisfaction. Two studies of Smeets et al. [44,45] suggest that modified sham feeding of fatty foods result in higher satiety response and/or lower ghrelin levels. Consuming a meal in 30 min compared to consuming the same meal in 5 min led to higher responses of the satiety hormones PYY and GLP1 [25]. Li et al. [29] showed that chewing food for longer compared to chewing food for shorter led to lower ad libitum intake and higher GLP-1 and PYY responses. One interesting question is this respect is how oral and gastric signals contribute to satiety. In an elegant study, Cecil et al. [8] showed that intragastric or intraduodenal loads of tomato soup led to modest decreases in hunger responses. When soup was consumed orally through the same tube as in the intra-gastric conditions, this led to significantly higher satiety responses (see Fig. 6). This study strongly suggests that there is a strong contribution of the oro-sensory signal to satiety. Wijlens et al. [54] independently manipulated gastric volume (0, 100 or 800 ml, through a naso-gastric tube) and oro-sensory exposure time (0, 1 and 8 min of modified sham feeding). In this study, 8 min sensory exposure had a stronger effect on subsequent satiety and ad libitum test‐meal intake than the 800 ml (100 kcal) intragastric load. Altogether, these studies show, that longer sensory exposure times lead to cephalic phase responses, that not only contribute to physiological homeostasis, but also significantly contribute to satiety. These results are in line with the concept of the sense of taste as a nutrient sensor, which inform the brain and the GI tract of the inflow of nutrients. 6. Discussion The results of numerous studies suggest that the effect of texture on food intake is mediated by the oro-sensory exposure time, or the
Fig. 6. The effect of soup given orally (filled black circles), overtly intragastricly (filled black squares), covertly intragastricly (open squares), and intraduodenally (open triangles) on hunger ratings. Values are expressed as mean +/−s.e.m. (n= 9). Source: [8].
oral residence time of food in the mouth. The studies on the cephalic phase response, and the studies on oral and gastric contributions to satiety show that one needs a considerable amount of time of food in the mouth before the sensory signals lead to a substantial physiological/subjective satiety response. These data are in line with the notion that the sense of taste monitors the inflow of nutrients, and has an important contribution to satiety. With simple liquid foods like sugar sweetened beverages, this system is bypassed, and the calories enter the body more or less unoticed. Within this context it is good to notice, that the short term behavioral studies on the lack of a compensatory response to simple liquid caloric beverages (e.g. [33]) are in line with longer term nutrition intervention studies [12,38,50]. The results of the intervention studies are in line with the epidemiological literature on the effects of sugar sweetened beverages on the prevalence of obesity [31,42]. These findings are reinforced by the notion of the lack of cephalic phase stimulation with liquids [48]. The effect of texture on food intake seems more clear when studying satiation compared to studying satiety. For example, Zijlstra et al. [59] showed that the ad libitum intake of a liquid flavoured dairy product was about 30% higher than the ad libitum intake of the semi solid version of the same product. In a subsequent study, Zijlstra et al. [61] showed that the fixed intake of 300–400 g of the liquid and semo-solid version led to about similar changes in hunger responses during the 90-min after ingestion. For texture effect on satiety one may need considerable differences in structure like the difference between a solid and a liquid version of a food (see [15,27]). The idea that texture has a stronger effect on satiation than satiety fits with the satiety cascade of Blundell [4], which show that cognitive and sensory effects have a major impact on satiation and less so on satiety (see also [10]). The notion that texture effects are more obvious with satiation than with satiety does not mean that texture has no impact on satiety. It does. Recent systematic reviews on the effects of dietary fire on satiety and food intake show that food with fibres that are more viscous/more gelling lead to higher satiety responses and a lower subsequent food intake than foods that are less viscous/gelling [26,52]. This suggests that the volume or contact time of foods with nutrient sensors in the stomach and gut have a signifiant impact on satiety. In this way, in relation to the satiety cascade of Blundell, texture affects satiety also through post-ingestive and post-absorptive effects. Liquids vs. semi-solid foods lead to substantial differences in satiation and satiety. One key question is whether or not not this also holds for comparable solid products. Do products that are chewed or consumed for longer also lead to significant differences in intake? The results of Zijlstra et al. [62] showed that also for solid foods, a higher eating rate was related to a higher ad libitum intake. However, within pairs of similar foods with slightly different textures she could not demonstrate a difference in intake [62]. Li et al. [29] showed that increasing the number of chews from 15 to 40 chews led to a lower ad libitum intake. This suggests that one needs conserable differences in eating rate/oral residence time to signifiantly lower food intake. One important research question that remains to be answered is whether or not texture differences in realistic foods that can be exchanged for each other in the commercial market place lead to lower intake. Can commercial food companies use the proofs of principles of the effects of texture on satiety to design food that promote earlier satiation and/or a longer satiety response? Several food companies are working and/or have been working on this [1,30,37]. Within the context of the present paper on the effects of texture on satiation, it should first be shown that a regularly consumed meal with longer oral processing time leads to a lower ad libitum intake. Next, one would like to have evidence that the lower intake is not compensated later on the day. Recent data from Levitsky & Pacanowski [28] suggest that people are unlikely to compensate for
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moderate lower decreases in food intake during one meal. The final challenge will be to test these proofs of principles in longer term studies. In the end, such studies may contribute to a food supply that is less obesogenic. Another important research area in the future is the characterization of cephalic phase responses. As is clear from the results of various studies, cephalic phase responses have a substantial contribution to satiation and satiety. It seems also well established that one needs solid foods with a substiantal oral residence time to produce a cepahlic phase response. However, it is not yet clear how different tastes and different macronutrient may contribute to a cephalic phase response, and therefore also contribute to satiety.
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