Prolonged chewing at lunch decreases later snack intake

Appetite 62 (2013) 9195

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Appetite

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Research reportProlonged chewing at lunch decreases later snack intakeSuzanne Higgs , Alison JonesSchool of Psychology, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK

a r t i c l e i n f o

Article history:Received 24 August 2012Received in revised form 22 November 2012 Accepted 23 November 2012Available online 30 November 2012

Keywords: Chewing Satiety Food intake

a b s t r a c t

Prolonged chewing of food can reduce meal intake. However, whether prolonged chewing inuences intake at a subsequent eating occasion is unknown. We hypothesised that chewing each mouthful for 30 s would reduce afternoon snack intake more than (a) an habitual chewing control condition, and(b) an habitual chewing condition with a pauses in between each mouthful to equate the meal durations. We further hypothesised that this effect may be related to effects of prolonged chewing on lunch mem- ory. Forty three participants ate a xed lunch of sandwiches in the laboratory. They were randomly allo- cated to one of the three experimental groups according to a between-subjects design. Appetite, mood and lunch enjoyment ratings were taken before and after lunch and before snacking. Snack intake of can- dies at a taste test 2 h after lunch was measured as well as rated vividness of lunch memory. Participants in the prolonged chewing group ate signicantly fewer candies than participants in the habitual chewing group. Snack intake by the pauses group did not differ from either the prolonged or habitual chewing groups. Participants in the prolonged chewing group were less happy and enjoyed their lunch signi- cantly less than participants in other conditions. Appetite ratings were not different across groups. Rated vividness of lunch memory was negatively correlated with intake but there was no correlation with rated lunch enjoyment. Prolonged chewing of a meal can reduce later snack intake and further investigation of this technique for appetite control is warranted.

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Introduction

Given the continuing rise in levels of obesity in many countries there is an imperative to understand more about the factors that promote excess energy intake (Swinburn et al., 2011). One factor that has received some attention is the relationship between eating style, satiety and energy intake. It has been proposed that decreas- ing eating rate by eating more slowly or increasing chews per mouthful results in decreased food intake (Martin et al., 2007; Otsuka et al., 2006; Spiegel, Wadden, & Foster, 1991). Andrade and colleagues found that taking small bites, pausing between bites, and chewing food thoroughly decreased food intake and increased satiety compared with a condition in which the meal was eaten as fast as possible with no pauses between bites (Andrade, Greene, & Melanson, 2008). Similarly, Smit and colleagues investigated the effects of prolonged chewing for each mouthful of food on intake (Smit, Kemsley, Tapp, & Henry, 2011). They reported that chewing thirty-ve times before swallowing resulted in slower eating, longer meal duration and less food intake than chewing for ten times before swallowing.Few studies have attempted to isolate the specic components of eating style that might contribute to reduced energy intake.

Corresponding author.E-mail address: s.higgs.1@bham.ac.uk (S. Higgs).

There is some evidence that slowing down eating rate by providing obese children with feedback on their eating rate reduces food in- take (Ford et al., 2010), although in another study, slowed eating rate of a xed portion size was reported to have no effect on post- prandial appetite and intake of a subsequent meal (Karl, Young, & Montain, 2011). Other studies have focused on mastication and it has been reported that increased chewing of almonds is associated with a sustained reduction in rated appetite 2 h after consumption (Cassady, Hollis, Fulford, Considine, & Mattes, 2009). In addition, there is evidence that chewing per se without swallowing food suppresses appetite (Hetherington & Boyland, 2007; Nolan & Hetherington, 2009). To our knowledge no study to date has exam- ined the effect of prolonged chewing during consumption of a xed meal on food intake at the next eating opportunity.The mechanism underlying the effect of increased mastication on appetite and energy intake is unclear but there are several pos- sibilities. First, increased mastication might enhance cephalic phase responses and release of nutrients from food affecting release of gut hormones (Li et al., 2011). Second, a longer time of oral processing of food due to prolonged chewing might decrease intake due to in- creased sensory satiety (Zijlstra, de Wijk, Mars, Staeu, & de Graaf, 2009). Third, food palatability might be reduced by prolonged chewing or the experience might be so novel as to reduce enjoy- ment of eating and intake (Hill, Magson, & Blundell, 1984). Finally, cognitive factors might have a role to play, especially in inuencing

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92S. Higgs, A. Jones / Appetite 62 (2013) 9195

S. Higgs, A. Jones / Appetite 62 (2013) 919593

appetite in the inter-meal interval. Prolonged chewing might en- hance attention to and sensory processing of food, leading to en- hanced food memory. There is some evidence that satiety is inuenced by memories of recently eaten foods leading to the hypothesis that chewing enhances food memory, which enhances satiety (Higgs, 2002; Higgs, Robinson, & Lee, 2012).In the present study we manipulated the amount of time spent chewing per mouthful of a xed lunch meal and examined the ef- fect of this manipulation on later appetite and snack consumption. We hypothesised that prolonged chewing would decrease later snack intake. We were also interested in examining the potential mechanisms underlying any effects of prolonged chewing on later lunch intake. We hypothesised that prolonged chewing might have an effect on post-lunch snacking either via reduced mood due to low lunch palatability and/or an effect of prolonged chewing to en- hance lunch memory and inhibit later appetite.

Methods

Participants

Forty-three student volunteers (36 female, 7 males, mean age = 20.35, 2.82, mean BMI = 20.84, 2.10) were recruited through an online study registration website. Participation was in exchange for course credit. Participants met the recruitment crite- ria of: non-smoking, not actively dieting, healthy BMI, no food allergies or intolerances, not vegetarian or vegan, not diabetic and no current or ongoing dental problems. Scores for restrained eating (mean = 2.25, 0.89) and disinhibition (mean = 5.58, 3.03) were assessed using the restraint scale of the Dutch Eating Behav- iour Questionnaire (Van Strien, Frijters, Bergers, & Defares, 1986) and the disinhibition scale of the Three-Factor Eating Question- naire (Stunkard & Messick, 1985). Participants were asked to re- frain from eating for 2 h prior to arriving for the study. So that participants were not alerted to the purpose of the experiment, recruitment to the study was via an advertisement describing the experiment as a study on eating behaviour and mood. Ethical ap- proval was obtained from the University of Birmingham Ethical Re- view Committee and participants gave their written informed consent prior to taking part.

DesignA between-subjects experimental design was used, in which each participant was randomly assigned to one of three experi- mental conditions: Condition 1 (habitual chewing condition) was a control condition where participants were asked to eat as they usually would; Condition 2 (pauses condition), was another control condition in which participants chewed normally but with 10 s pauses between each mouthful; Condition 3 (prolonged chewing condition) was the experimental condition in which participants were asked to chew continuously for 30 s before swal- lowing. We chose to manipulate chewing time rather than number of chews as this allowed for easier control by the experimenter of the conditions and equating of meal duration. The timing of the prolonged chewing condition was based on a pilot study showing that 30 s was longer than usual chewing time but achievable with- out much discomfort. The timing of the pauses condition was sim- ilarly based on a pilot study and was chosen to try to ensure similar meal duration as the prolonged chewing condition but with usual chewing time. Previous studies have found that insert- ing pauses in between chewing increases concurrent intake, per- haps due to frustration at disruption of habitual chewing (Yeomans, Gray, Mitchell, & True, 1997). However, in the present study participants ate a xed lunch meal and so concurrent intake could not be altered by pausing. The between-subjects design was

used to minimise the possibility that participants guessed the aims of the study.

Test foodsThe lunch consisted of one and a half smoked ham and cheddar sandwich (Tesco, UK) with the crusts removed and cut equally into 24 triangular bite sized pieces. The lunch contained approximately 600 calories. The lunch was the same in all three conditions and participants were asked to consume all the meal. The afternoon snack consisted of one bowl containing 100 g of Skittles (The Wrig- ley Company Limited) and one bowl containing 100 g of Minstrels (Galaxy, Mars Incorporated). Skittles are chewy fruit candies and Minstrels are chocolate candies with a sugar shell. We provided two snacks in case the participants disliked one of them.

ProcedureEach participant completed a pre-study questionnaire prior to taking part to ensure that they met the study requirements. If suit- able for the study, they were randomly assigned to one of the three conditions and informed that they were required to attend two sessions on the same day. The rst session (lunch) took place at 12:00, 12:30 or 13:00 and lasted approximately 30 min. On arrival, participants were individually taken into a quiet test room and asked to complete a demographics questionnaire and a series of line rating scales assessing mood and appetite. The following items were rated using a 100 mm unmarked line rating scale: hungry, full, desire to eat, happy, sad, stressed, relaxed, irritable, nervous, excited. The anchors at the end of the line were Not at all and Extremely. The question was in the format How XXX do you feel right now? and the text was centred above the line. Ratings were obtained by measuring the distance in mm from the left extremity of the lines. After completing the ratings, participants were given written instructions informing them of how they should eat their lunch, that they should nish all of the lunch and that the research- er would remain in the room. The researcher was seated to the side of the participant and not in the direct line of sight of the partici- pant. In the pauses condition and the prolonged chewing condi- tion, the researcher instructed the participants when to chew and when to pause using a stopwatch. In the habitual chewing con- dition, the researcher remained in the room but gave no instruc- tions. On completion of the lunch, participants were given a second series of 100 mm rating scales assessing post-lunch appe- tite, mood and enjoyment of their lunch. They were thanked for their time and reminded not to eat before returning for the second session.The second session (snack) took place 2 h after the lunch (for example if the lunch session was at 12:00 they returned at 14:00) and took place in the same room. On arrival, participants were asked to complete a set of 100 mm rating scales assessing appetite and mood. Once nished, participants were given another set of 100 mm rating scales assessing mood accompanied by the snack. Participants were told that a printing error had occurred and they needed to be left for 10 min whilst it was corrected. Par- ticipants were asked to complete the rating scales whilst waiting and were informed that they could eat as much or as little of the snack as they liked. The snack bowls were weighed before and after to measure the amount consumed during the 10 min interval.When the researcher returned, the snack was removed and a 100 mm rating scale asking how vivid is your memory of your lunch was presented. This question was used to assess the mem- ory of the lunch. A nal paper-based question asked the participant to guess and briey describe the purpose of the study, as well as providing the opportunity for any additional comments. Height and weight measurements were taken and participants then com- pleted the restraint scale of the Dutch Eating Behaviour Question- naire (Van Strien et al., 1986) and the disinhibition scale of the

Three-Factor Eating Questionnaire (Stunkard & Messick, 1985). They were debriefed, thanked for their time and asked not to dis- cuss the study with anybody else.

AnalysisTwo participants were excluded from the analysis. The rst par- ticipant did not eat the afternoon snack due to personal taste pref- erences and the second participant was taking medication known to affect appetite. Forty-one participants (34 female, 7 males, mean age = 20.29, 2.82, mean BMI = 20.87, 2.14) were included in the nal analysis. Results were analysed using a multivariate ANOVA with condition (chewing/pauses/habitual chewing) as a factor. Sex was included as a factor but no signicant interactions were observed and so the results are presented as the overall group means. Analyses were conducted using SPSS 17.0.

Results

Participant characteristics

The groups did not differ in terms of age (F (2, 38) = 1.35,p = 0.27), BMI (F (2, 38) = 1.33, p = 0.28), restraint (F (2, 38) =0.69, p = 0.51) or disinhibition (F (2, 38) = 2.07, p = 0.14). See Table1.

Pre-lunch appetite and moodA multivariate analysis revealed no signicant differences be- tween the groups on any of the pre-lunch measures of appetite and mood (all p > 0.1) apart from pre-lunch desire to eat where there was a marginal effect of group (F (2, 38) = 2.59, p = 0.09) and the pauses group had a slightly greater desire to eat compared with the chewing group. See Table 2.

Post-lunch appetite, mood and meal ratingsFor the post meal ratings, a multivariate analysis revealed a sta- tistically signicant effect of condition on rated happiness (F (2,38) = 3.9, p = 0.03) and post hoc tests revealed that the mean scoresfor the chewing group were signicantly lower than the pauses

Table 1

group (p = 0.01). The habitual chewing group did not differ signif- icantly from the chewing group (p = 0.49) but was marginally low- er than the pauses group (p = 0.06).A multivariate analysis also revealed a statistically signicant effect of condition on ratings of relaxed (F (2, 38) = 5.39, p = 0.01) and post hoc comparisons revealed that the mean scores were sig- nicantly lower for the chewing group (p < 0.01) and the habitual chewing group (p = 0.03) than the pauses group. The chewing group and the habitual chewing group did not differ from each other (p = 0.36).There was no effect of condition on any of the other post-lunch ratings (all p > 0.1). See Table 2.

Pre-snack appetite and moodA multivariate ANOVA revealed no signicant differences be- tween groups for the pre-snack appetite and mood ratings. There was a marginal effect for rated happiness whereby there was a ten- dency for the pauses group to be more happy than the habitual chewing and chewing groups (F (2, 38) = 2.54, p = 0.1), which was similar to the pattern observed post-lunch. See Table 2.

Evaluation of lunchA multivariate ANOVA also revealed a signicant effect of con- dition on enjoyment of eating the lunch (F (2, 38) = 9.48, p < 0.01). Post hoc comparisons revealed that the chewing group enjoyed eating their lunch signicantly less than the habitual chewing group (p < 0.01) and the pauses group (p < 0.01). The habitual chewing and pauses groups did not statistically differ from each other in this respect (p = 0.38). There was a signicant effect of condition for pleasantness of the texture of the lunch (F (2, 38) = 5.56, p = 0.01) and post hoc tests revealed that the chew- ing group found the texture of their lunch signicantly less pleas- ant than the habitual chewing group (p < 0.01) and the pauses group (p < 0.04). Again, this measure was not signicantly different between the habitual chewing and pauses groups (p = 0.22). See Table 3.

Table 3Lunch ratings according to group. Values are expressed as means (SD).

Participant characteristics according to group. Values are expressed as means (SEM).

Rating 0100 mmHabitual chewing(N = 13)

Pauses(N = 14)

Chewing(N = 14)

Age (years)19.85 (1.77)19.71 (0.83)21.29 (2.82)Tastiness of the lunch6.12 (1.68)6.32 (2.31)6.49 (1.86)BMI (kg)20.4 (2.8)20.56 (1.85)21.61 (1.58)Pleasantness of the texture7.00 (1.76)5.91 (2.79)4.12 (2.10)*,+Restraint (05) (DEBQ)2.18 (0.97)2.1 (0.82)2.48 (0.88)of the lunchHabitual chewing (N = 13)

Pauses (N = 14)

Chewing (N = 14)

Enjoyment of eating the lunch

5.42 (2.36)4.75 (1.72) 2.34 (1.73)

*,+

Disinhibition (016) (TFEQ)

6.92 (4.11)5.5 (2.74)4.57 (1.87)

* Refers to signicant difference at p < 0.05 compared to habitual chewing group.

+ Refers to the signicant difference at p < 0.05 compared to pauses group.

Table 2Rated appetite and mood as a function of time and group. Data presented as mean (SEM).

Rating (0100 mm)Habitual chewing (n = 13)Pauses (n = 14)Chewing (n = 14)Before lunchAfter lunchBefore snackBefore lunchAfter lunchBefore snackBefore lunchAfter lunchBefore snack

Hunger6.43 (1.89)0.86 (1.73)2.79 (1.82)6.92 ( 1.43)1.20 ( 1.15)2.57 ( 1.66)5.56 (2.03)1.05 (1.43)2.29 (1.58)

Fullness2.12 (1.84)8.33 (1.54)6.21 (2.26)2.34 (1.35)8.02 (1.60)6.59 (2.00)2.63 (1.82)8.00 (2.09)6.06 (2.13)

Desire to eat5.95 (2.64)1.25 (1.69)3.40 (1.85)7.06 (1.29)1.89 (2.26)2.52 (1.82)5.31 (2.09)0.81 (1.29)2.10 (1.38)

Happy5.81 (1.80)5.77 (2.33)6.20 (1.05)6.49 (1.38)7.20 (1.27)7.26 (1.62)6.03 (1.68)5.25 (2.01)+6.11 (1.79)

Sad2.22 (1.92)2.69 (2.80)2.08 (1.56)1.76 (1.87)1.06 (1.38)1.10 (1.69)2.16 (2.11)2.56 (2.24)1.61 (2.15)

Stressed2.68 (1.66)2.85 (2.28)2.78 (2.41)2.69 (2.22)2.05 (1.81)2.13 (2.11)3.49 (2.38)3.81 (2.71)3.41 (2.13)

Relaxed6.51 (1.97)5.17 (2.61)+5.57 (2.90)6.26 (2.14)7.19 (1.48)6.99 (1.89)5.28 (2.06)4.31 (2.83)+5.61 (2.10)

Irritable1.81 (1.81)1.95 (1.65)1.72 (1.45)1.89 (2.25)1.23 (1.11)1.07 (1.22)1.61 (1.54)2.51 (2.38)1.97 2.00)

Nervous1.55 (1.17)1.80 (1.74)1.55 (1.54)1.5 (1.75)0.94 (1.21)1.74 (1.98)2.11 (1.82)2.34 (2.63)1.71 (1.75)

Excited3.61 (2.58)3.08 (1.65)3.54 (2.09)4.2 (1.68)3.84 (2.90)5.16 (2.31)3.91 (2.1)3.64 (2.52)4.85 (1.81)

+ Refers to the signicant difference at p < 0.05 compared to pauses group.

70

60

Candy intake (g)50

40

30

20

10

0ControlPausesChewingCondition

Fig. 1. Afternoon snack intake (candies) according to experimental group. Data are expressed as mean intake (g) + SEM.

Snack intakeANOVA revealed a signicant effect of condition for the total amount of the afternoon snack consumed (F (2, 38) = 3.49, p = 0.04). Post hoc tests revealed that the chewing group ate signif- icantly less of the afternoon snack than the habitual chewing group (p = 0.01). There were no signicant differences between the pauses group and either habitual chewing (p = 0.3) or chewing groups (p = 0.1). See Fig. 1.

Vividness ratingsThe means for rated vividness of the lunch (chewing = 8.13 0.94, pauses = 7.39 1.94, habitual chewing = 7.78 1.04) did not differ (F (2, 38) = 0.98, p = 0.39) as revealed by a one-way ANOVA.

Correlations between intake, memory, lunch enjoyment and mood scoresWe hypothesised that snack intake might be related to either lunch enjoyment measures and/or memory of lunch and so we cor- related the intake measure with lunch measures that were signif- icantly affected by the manipulation and the memory measure. Pearsons correlation showed that there was a signicant negative correlation between total snack intake and memory vividness (r = -0.31, p = 0.05) but not between snack intake and rated enjoy- ment of lunch (r = 0.12, p = 0.5) or between snack intake and lunch pleasantness (r = 0.05, p = 0.8). Similarly, there was no correlation between post-lunch mood measures of happiness (r = 0.2, p = 0.14) and relaxed and later intake (r = 0.03, p = 0.8).

Post-study questionnaireWhen asked to guess the purpose of the study, the majority of participants reported the study to be about food and mood. Six par- ticipants believed the study to be about food presentation and memory and four participants believed the study to be about the lunch duration. Only two participants mentioned chewing as a fac- tor but believed the study to be about chewing and mood. There was no indication that any participant was aware of study hypotheses.

Discussion

The results of this study provide further evidence that pro- longed chewing of a lunchtime food can reduce later snack intake. Participants who chewed each mouthful of lunch continuously for 30 s ate half as many candies later that afternoon as participants

who chewed normally. The effect is unlikely to be due to aspects of the controlled chewing procedure such as the instructions given regarding consumption of the lunch because both the pauses and prolonged chewing group received similar instructions and the re- sults of our pilot study indicated that the conditions were unlikely to differ in meal duration. Between group differences in eating characteristics, age and BMI were also ruled out as possible expla- nations since the groups did not differ on these measures.No signicant effect of chewing on rated appetite was observed after lunch or before snacking but we did observe signicant ef- fects of prolonged chewing on rated mood and lunch enjoyment. Participants in the prolonged chewing group were less happy after lunch and had reduced ratings of lunch enjoyment and pleasant- ness of the texture of lunch compared with the other conditions. These effects may be due to both the novelty of the prolonged chewing compared with usual chewing and reduced palatability of the food due to increased oral processing. These data suggest that some previously reported effects of increased mastication on concurrent consumption may be explained at least in part by aver- siveness to the procedure (Cassady et al., 2009). It would be infor- mative to evaluate whether repeated exposure to prolonged chewing would ameliorate any reduced enjoyment of eating. Pro- posed mechanisms by which this could be achieved include mere exposure and/or positive reinforcement through longer and im- proved avour release with improved mastication.We did not nd signicant effects of pausing in between chew- ing on mood and appetite ratings, although there was a tendency for the pauses group to have higher rated happiness than the other groups after lunch and before snacking. These data contrast with the ndings of Yeomans et al. (1997) who found that participants found a meal less satisfying with the introduction of within meal pauses. It is possible that methodological differences between the studies account for the contrasting results. For example, in the present study, intake at lunch was xed whereas in the study of Yeomans et al. (1997) participants could eat as much food as they liked. In addition, participants in the present study were not required to make ratings in the pauses as they were in the Yeo- mans et al. (1997) study.The reduction in intake of snacks after prolonged chewing could be due to a number of factors. One possibility is that there was a carry-over of the negative effects of prolonged chewing at lunch on later snacking. Because the participants did not particularly en- joy the lunch experience, this may have affected decisions about how many candies to eat later. However, the negative effect of chewing on mood had dissipated by the time participants returned for the snack tasting session suggesting that this interpretation is unlikely. Furthermore, we found no relationship between ratings of the lunch experience and later snack intake, suggesting that any effect of chewing on food palatability and mood was short- lived. Participants may have found the prolonged chewing at lunch fatiguing which might have carried over to later intake but since the snack session took place 2 h after the lunch it would be ex- pected that there would have been recovery from any fatigue. An alternative explanation is that prolonged chewing enhanced encoding of the lunch memory which then reduced snack intake. In support of this idea, we have previously reported that enhancing memory of lunch by focusing on the sensory properties of food while it is eaten decreases later snacking, whereas disrupting memory for lunch has the opposite effect (Higgs & Donohoe, 2011; Higgs & Woodward, 2009). However, in the present study we found no differences between the groups in lunch memory rat- ings, which argues against this explanation. It may have been that the measure used to assess lunch memory was not sensitive en- ough to detect between group differences or that ceiling effects were operating. Nevertheless, we did nd that rated vividness of lunch memory was negatively correlated with snack intake

suggesting that the effect of chewing to decrease intake may be due in part to enhanced lunch memory encoding. In future studies it would be informative to use a more sensitive memory measure that asks participants to rate their memory for specic food items rather than the lunch as a whole.A limitation of the present study is the small sample size. We were able to detect signicant effects of our chewing manipulation on intake but it will be important to validate our ndings in follow- up studies. Future studies might also examine the effect of pro- longed chewing on later intake in obese versus lean populations to ascertain whether chewing interventions might be useful in treating obesity. In addition, it would be important to examine whether effects of chewing on satiety are sustained in the longer term and reduce intake of later meals as well as snacks. Given that food form affects oral exposure and satiety (Zijlstra, Mars, de Wijk, Westerterp-Plantenga, & de Graaf, 2008), it would also be interest- ing to examine the effect of chewing on different food types, partic- ularly since the amounts eaten in the present study may have been affected by the fact that some people limit their intake of sweets for health motivations. It would also be useful to assess level of gut derived hormones such as CCK, GLP-1 and PYY since there is evidence that both increased mastication and slow eating are asso- ciated with increased levels of these hormones (Kokkinos et al., 2010). Given the effect of prolonged chewing to decrease lunch pleasantness, it remains to be determined whether prolonged chewing can be established as a habit in adults. An implication of the present results might be that an eating style involving thor- ough chewing of food should be encouraged in children before habits are established.In summary, the present ndings suggest that prolonged chew- ing reduces later food intake although the underlying mechanism remains unclear. Further investigation of enhanced chewing of food as a tool for appetite control is warranted.

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