Even brief exposure to the sight and smell of food has been shown to increase reported appetite, initiate ‘cephalic phase responses,’ and increase planned and actual consumption. This experiment tested the hypothesis that overweight individuals are especially sensitive to these established effects of food-cue exposure.
Overweight (n=52) and normal-weight (n=52) participants were exposed to the sight and smell of a ‘cued’ food (pizza) for 60 s. Before and after this period, we assessed salivation, prospective (planned) portion size, and desire to eat pizza and other ‘non-cued’ foods. Participants were then offered ad libitum access to pizza.
Consistent with previous studies, food-cue exposure increased rated hunger and desire to eat, increased prospective portion size of all savory foods, and increased salivation. In overweight individuals, cue exposure (i) elicited a significantly greater salivary response and, (ii) evoked a significantly greater increase in desire to eat both the cued food and another non-cued food.
After cue exposure, overweight individuals experience a greater motivation to consume food but do not desire or consume greater amounts of food. These findings are consistent with evidence that snacking and meal variability predict weight gain and they expose ‘cue reactiveness’ as a potential predisposing factor for overweight.
In the late 1960s, Schachter and co-workers proposed the ‘externality theory’ of human obesity.1, 2 By this account, obese individuals lack sensitivity to internal hunger and satiation signals, and are especially sensitive to external cues, including the sensory characteristics of food.3, 4, 5 Despite this early work, basic questions about the role of externality in overeating remain. Recently, studies have focused on the effects of exposure to the sight and smell of food.6, 7, 8, 9
In humans, ‘food-cue exposure’ can have a profound effect on our motivation and physiological preparedness to eat. Indeed, even brief exposure to the sight and smell of food increases reported hunger7, 8, 10, 11 and initiates ‘cephalic phase responses,’ including release of insulin and changes in salivation, heart rate, gastric activity and blood pressure.11, 12, 13, 14 Targeted clinical comparisons, such as those involving binge eaters and bulimics, show that individuals differ in their reactivity to food cues.15, 16, 17, 18, 19 Despite this, it remains unclear whether differences in cue reactivity represent a risk factor for overweight and obesity. We suggest that this issue merits attention because recent research indicates that cue exposure promotes the selection of larger portion sizes,7 and it increases the amount of food that is consumed in a meal.6, 7, 8
Previous research has explored associations between obesity and salivary reactivity. For example, Jansen et al.9 reported differences between overweight and lean children regarding food intake and the correspondence between food intake and salivation, after food-cue exposure. Also, overweight children are slower to show salivary habituation after repeated exposure to a food cue.20, 21 In adults, obese individuals salivate more in response to a food cue and are slower to develop salivary habituation.22, 23, 24, 25 However, these findings might otherwise be explained by differences in dietary restraint,26, 27, 28, 29, 30 which is correlated with body mass index (BMI).31, 32, 33 Indeed, some authors suggest that dietary restraint has a causal role in the development of heightened reactivity.6, 8
In a recent study, overweight and lean adults were exposed to a food cue (pizza) in a satiated state. The overweight participants reported a greater increase in desired pizza portion-size.34 However, only a modest sample of overweight participants (drawn from a student population) was tested and salivary response was not assessed. Furthermore, the cued food was not assessed relative to control (non-cued) foods. These controls are useful because they help to determine whether the effects of cueing are general or specific to the cued food. In an early study, the effects of cueing did not generalize to another non-cued food.8 However, the cued and non-cued foods were very different (sweet or savory). More recently, generalization has been observed across foods that share super-ordinate characteristics with the cued food.7
In this study we sought to resolve these issues. Specifically, we assessed differences between overweight and lean individuals using several measures of cue reactivity that we and others have previously found to be sensitive to the effects of cue exposure, relative to a control condition.7, 8, 10, 11, 12, 13, 14 In particular, we sought to determine whether there are overweight/lean differences in desire to eat and physiological reactivity (salivation) after food-cue exposure, and whether these differences are reflected in measures of prospective intake and the amount of food subsequently consumed. To control for overweight/lean differences in restrained eating, we also incorporated the Revised Restraint scale35 and the restraint subscale of the Dutch Eating Behaviour questionnaire.36 Both these measures were included in response to controversy over how to best assess dietary restraint.37 Finally, to explore the extent to which the effects of cue exposure are exclusive to a cued food (pizza), we also included assessments of a range of similar (savory) and dissimilar (sweet) non-cued foods.
Female staff from the University of Bristol (UK) were recruited through email and poster advertisements. None had assisted with previous experiments in our laboratory. On the basis of an initial screening of their self-reported body weight, and after taking measures of their actual height and weight, 52 participants were classified as overweight (mean BMI=30.1, s.d.=5.4) and 52 were classified as normal weight (mean BMI=22.6, s.d.=1.6). Participants were classified as overweight if their BMI was 25.0. The mean age of the overweight and the normal-weight group was 35.4 (s.d.=12.5) and 34.9 (s.d.=13.1) years, respectively. Participants were excluded if they were vegetarian or vegan, had any food allergies or intolerances, or if they reported a strong dislike of pizza. All participants were offered £10 (Sterling) in remuneration for their assistance. Ethical approval was granted by the University of Bristol Faculty of Science Human Research Ethics Committee.
Visual analog scales. Desire to eat was measured using a 100-mm visual-analog rating scale headed ‘How strong is your desire to eat (food name inserted) right now?’ Similar scales were also used to assess hunger, fullness and liking for the test foods. All of the scales were anchored with the phrases ‘Not at all’ and ‘Extremely.’
Salivation. Salivation was measured using a modified version of the Strongin–Hinsie Peck procedure.38 Participants were given a pre-weighed bag containing a single dental roll and were asked to place the roll under their tongue for 30 s. After this period, the participants removed the dental roll and returned it to the plastic bag, which was then weighed a second time. This technique has been used successfully in other studies in our laboratory,28, 39 is relatively noninvasive, and provides a sensitive single measure of whole-mouth saliva volume.
Prospective portion-size task
On the basis of previous work,7 prospective portion size was assessed using a computerized task. We used hot pizza as the cued food and cake; ‘chocolate buttons;’ ‘chicken tikka masala;’ ‘pasta and tomato sauce;’ and ‘scrambled eggs, chips and beans’ as non-cued foods. Each food was photographed 41 times (numbered 1–41) on the same white plate (255-mm diameter). For each food, picture-21 corresponded with a ‘standard’ (average portion size in the UK). Information about typical portion sizes was obtained from Gregory et al.40 or from the nutritional information on the product packaging (see Table 1). For cake and chocolate buttons, picture-1 and picture-41 represented 0.25 and four times the weight of the standard, respectively. For the other foods this range was limited by the amount of food that could physically be placed on the plate—picture number-1 represented 0.3 times the weight of the standard and picture-41 was three times the standard. Across the range of pictures the portion sizes increased in equal logarithmic steps. All of the pictures were taken using a high-quality digital camera that was mounted directly overhead, with fixed lighting. Particular care was taken to ensure identical lighting and arrangement of the plate across foods and portion sizes.
Images (255 mm × 190 mm) were shown on a 19″ TFT-LCD monitor. A horizontal scrollbar was presented at the bottom of the screen. When a participant used the mouse to move the scrollbar, the computer presented a new image that corresponded to the new position of the scrollbar. Moving the scrollbar to the left caused the portion size to decrease (a smaller picture number was shown). Moving it to the right caused the opposite. The pictures were loaded with sufficient speed so that steady movements on the scrollbar gave the appearance that the change in portion size was ‘animated.’ For each food, the participants provided two estimates of prospective portion size. The first and the second estimate started with the scrollbar located at the bottom (smallest portion size) and top of its range (largest portion size), respectively. Participants were instructed to select the portion size that they would like to eat at that moment in time. For each food, a measure of prospective portion size was derived from the mean of both responses. For each participant, the test foods were presented in a different randomized order. The code for this task was written in Visual Basic (version 6.0).
Other measures. Previously, it has been suggested that restrained and unrestrained eaters respond differently to food cues.26, 27, 28, 29, 30 To assess and control for dietary restraint we asked the participants to complete the Revised Restraint Scale35 and the restraint section of the Dutch Eating Behaviour Questionnaire (DEBQ36). The Revised Restraint scale is a 10-item questionnaire that measures two factors, concern for dieting (CD) and weight fluctuation (WF). Each question elicits a response to 4 or 5 options. The DEBQ-R scale asks participants to endorse items concerning deliberate planned weight control. This scale comprises 10 items, each eliciting a response to five alternative options.
Participants were told that the purpose of the study was to investigate the effects of mood on appetite for food. All attended a single 60-min session, held between 1130 and 1430 hours. Before their appointment, the participants were asked to abstain from eating for a 3-h period. On arrival, they provided written consent and completed baseline hunger, fullness, and liking visual-analog scales. Consistent with the cover story, they were then asked to fill out the positive affect negative affect scale (PANAS).41 Before exposure, the participants provided a measure of baseline saliva and completed ratings of hunger, fullness, and desire to eat. They then completed our prospective portion-size task.
The participants were then exposed to the sight and smell of a freshly cooked ‘Goodfellas deeply delicious loaded cheese pizza’ for 1 min (supplied by Green Isle Foods Limited, Naas, Co. Kildare, Ireland). After this period, they provided a second measure of salivation, a second set of ratings (hunger, fullness, desire to eat), and completed the prospective portion-size task once again.
Participants were then given free access to a 546 g (5755 kJ) portion of pizza. The pizza was presented in bite-size pieces and the participants were instructed to eat until they no longer wished to do so. Afterwards, they completed a final set of hunger and fullness ratings. At the end of the session the participants completed the dietary-restraint questionnaires and a measure of height and weight was taken.
All data were analyzed using SPSS version 12.0.1 (SPSS Inc., Chicago, IL, USA). Independent-samples t-tests were used to explore differences between normal-weight and overweight groups in baseline hunger, fullness, and liking for the six test foods.
To determine whether cueing had a significant effect on reported hunger and fullness, a two (exposure: before cueing, after cueing) × two (weight status: normal weight, overweight) analysis of covariance (ANCOVA) was conducted. In our analyses of these and other dependent variables, pre-exposure liking for pizza was included as a covariate where it significantly correlated with a dependent variable (see Table 2 for correlations between the covariate and the dependent variables). When we found a significant interaction between weight status and exposure we included each measure of restraint as a covariate (DEBQ-restraint & Revised Restraint), but only when it correlated significantly with the dependent variable. We adopted this approach because dietary restraint tends to be associated with both BMI31, 32, 33 and heightened reactivity.26, 27, 28, 29, 30 In each case the homogeneity of regression slopes assumption was met.
To determine whether cueing had a significant effect on prospective portion size, a six (food type: cake; ‘chocolate buttons;’ ‘chicken tikka masala;’ ‘pasta and tomato sauce;’ pizza; ‘scrambled eggs, chips and baked beans’) × two (exposure: before cueing, after cueing) × two (weight status: normal weight, overweight) ANCOVA was conducted. For each food, we then conducted a separate ANCOVA. This strategy was also applied to analyze the desire-to-eat ratings.
To determine whether cueing had a significant effect on salivation, a two (exposure: before cueing, after cueing) × two (weight status: normal weight, overweight) ANCOVA was conducted. ANCOVA was also used to explore differences between the consumption of pizza (g) in overweight and normal-weight individuals.
Initially, we were interested to determine whether significant differences exist between normal-weight and overweight individuals in baseline ratings of hunger, fullness, and liking for the test foods. Table 3 shows the means and standard deviations associated with these variables. Values are provided for overweight and normal-weight individuals separately. Independent-samples t-tests revealed no reliable differences between these groups.
Analysis of the relationship between responses to items on the Revised Restraint scale35 and the restraint subscale of the DEBQ36 showed that these measures had good internal consistency within our sample. In particular, for the Revised Restraint scale, the Cronbach's alpha coefficients were 0.763, 0.719 and 0.835 for the six-item CD scale, the four-item WF scale and the whole scale, respectively. The Cronbach's alpha coefficient for the restraint subscale of the DEBQ was 0.901. These alpha values are consistent with previous published statistics.42 The mean DEBQ-restraint score for the overweight and the normal-weight group was 3.07 (s.d.=0.72) and 2.95 (s.d.=0.79), and the mean Revised Restraint score for the overweight and the normal-weight group was 17.78 (s.d.=6.16) and 12.26 (s.d.=4.78), respectively.
Effects of cueing on hunger and fullness
Table 4 shows the unadjusted means and standard deviations for ratings of hunger and fullness before and after exposure to the food cue. Participants experienced a significant increase in hunger (F1,102=50.20, P<0.001) and a significant decrease in fullness (F1,101=14.41, P<0.001) after exposure to the food cue. For both hunger (F1,102= 1.49, P>0.05) and fullness (F1,101=1.67, P>0.05), the interaction between weight status and cueing failed to reach significance.
Effects of cueing on prospective (planned) portions of pizza and non-cued foods
Table 5 shows the mean (standard deviation) estimates of prospective portion-size before and after exposure to the food cue. Prospective portion size was significantly greater after exposure to the food cue (F1,102=17.05, P<0.001). However, this main effect was qualified by an interaction with food type (F3.47, 353.66=7.30, P<0.001). To explore this interaction further, we considered the effect of exposure in each food separately.
After cue exposure, the participants reported a significantly greater prospective portion-size for ‘scrambled egg, chips and baked beans’ (F1,102=9.46, P=0.003); ‘chicken tikka masala’ (F1,102= 16.57, P<0.001); and ‘pasta and tomato sauce’ (F1,102=9.55,P=0.003). With cake (F1,102=0.05, P>0.05) and chocolate buttons (F1,102=0.30, P>0.05), the effects of exposure were not significant.
Contrary to previous findings,7, 34 we failed to find a significant effect of cue exposure on the prospective portion-size of the cued food (pizza) (F1,02=1.51, P>0.05). Inspection of raw data showed that some participants selected a whole pizza both before and after cueing, perhaps reflecting a disposition to select a highly familiar portion size. To test this idea, we repeated the analysis excluding all participants who chose a whole pizza (this resulted in 17 participants being excluded from the analysis). This post hoc analysis showed a significant increase in prospective portion-size for pizza after cueing (F1,85=5.42, P=0.02). Weight status did not moderate this pattern of results.
Effects of cueing on desire to eat pizza and non-cued foods
Figure 1 shows the mean (s.e.m.) change in the ratings of desire to eat before and after food-cue exposure. Separate values are shown for overweight and lean participants, and for each test food. Desire to eat was significantly greater after exposure to the food cue (F1,101=8.54, P=0.004). However, this main effect was qualified by an interaction with food type (F4.557,460.284=10.52, P<0.001). To explore this interaction, we considered the effect of exposure in each food separately.
Participants reported a significant increase in desire to eat ‘pasta and tomato sauce’ (F1,102= 10.00, P=0.002); ‘chicken tikka masala’ (F1,101=10.06, P=0.002); pizza (F1,102=28.38, P<0.001); and ‘scrambled egg, chips and baked beans’ (F1,102= 9.54, P=0.003) after exposure to a food cue. Significant differences were not observed for cake (F1,102= 2.28, P>0.05) or chocolate buttons (F1,102= 2.02, P>0.05). Importantly, we found a significant interaction between weight status and change in desire to eat pizza (F1,102=5.18, P=0.025) and a significant interaction between weight status and desire to eat ‘scrambled egg, chips and beans’ (F1,102=4.78, P=0.031). Overweight individuals experienced larger changes in their desire-to-eat pizza and ‘scrambled egg, chips and beans’ (see Figure 1). Neither the DEBQ-restraint scale nor the Revised Restraint scale correlated significantly with the change in desire to eat either pizza (r103=0.06, P>0.05; r93=0.07, P>0.05) or ‘scrambled egg, chips and beans’ (r103=0.00, P>0.05; r93=0.02, P>0.05).
Effects of cueing on salivation
The difference between the amount of saliva produced before and after cue exposure narrowly missed significance (F1,101=3.57, P=0.062). However, there was a significant interaction between the effects of food-cue exposure on salivation and weight status (F1,101=4.17, P=0.044). Overweight individuals produced significantly more saliva after exposure to a food cue (see Figure 2). Differences in the amount of saliva produced before and after cue exposure were unrelated to DEBQ-Restraint or Revised Restraint scores (r103=0.01, P>0.05; r93=−0.00, P>0.05).
Pizza intake in overweight and lean individuals
On average, overweight individuals ate 256.6 g pizza (s.d.=83.8) and normal-weight individuals ate 293.1 g pizza (s.d.=96.2) in the ad libitum meal. Liking for pizza (a covariate in the analysis) was significantly related to pizza intake (F1,101=20.23, P<0.001). However, the amount of pizza (g) that overweight and normal-weight individuals consumed did not differ significantly (F1,101=1.84, P=0.178).
Consistent with previous studies, we found that food-cue exposure increases (i) rated desire to eat, (ii) prospective (planned) portion size of a cued food (pizza) and (iii) salivation (albeit non-significant, P=0. 06).6, 7, 8, 10, 11 In two of these measures, we found heightened food-cue reactivity in overweight individuals.
First, after cue exposure, the overweight participants reported a greater increase in their desire to eat both a cued food (pizza) and other non-cued foods (‘scrambled egg, chips and beans’). Second, cue exposure elicited a stronger salivary response in overweight individuals. Furthermore, and consistent with a recent study,34 we found little evidence that variance in these dependent measures (change in salivation and change in desire to eat) can be explained by differences in dietary restraint. Finding heightened salivary reactivity in overweight individuals is consistent with previous research demonstrating that overweight adults and children are slower to achieve salivary habituation after repeated exposure to a food cue.20, 21, 25
In relation to energy intake, food-cue exposure can have two consequences; it can prime an individual to engage in eating behavior and it can increase the amount of food that is selected and subsequently consumed.7 We found overweight/lean differences only in the former. Specifically, overweight individuals reported a greater increase in their motivation to consume food after exposure. This is potentially important, because this sensitivity may encourage snacking behavior and variability in eating habits, and it may promote disinhibited eating, all of which are associated with increased energy intake, overweight and weight gain.43, 44, 45, 46 In relation to our failure to find differences in intake, one explanation is that the overweight group consciously limited their eating because they felt scrutinized under laboratory conditions. However, the prospect that cue exposure promotes the initiation of a meal and not its size is consistent with the observation that everyday portion sizes are not predicted by BMI.47
Given the overweight/lean differences that were observed in the effects of cueing on desire to eat and salivation, it is perhaps surprising that these were not reflected in measures of rated hunger. In this regard it may be relevant that we tested hungry participants. One possibility is that hunger ratings were high at baseline, leaving little opportunity for further increases after exposure (a ceiling effect). In addition, effects of food-cue exposure on self-reported hunger may be greater in non-deprived participants.48 The extent to which this affected our opportunity to identify overweight/lean differences remains unresolved.
Research of this kind prompts two types of question: can we infer that heightened reactivity causes an increase in BMI, and what causes heightened reactivity in the first place? In relation to the first of these questions, the answer is, at present, no. However, consistent with this proposition, several studies report a positive association between self-reported externality and BMI.49, 50 Indeed, Burton et al.50 have shown that this relationship is mediated by a specific tendency to experience food cravings for high-energy-dense foods. Objective assessments of externality have also been considered. Consistent with self-report measures, Rodin and Slochower51 measured external responsiveness in 9- to 15-year-old girls during the first week of summer camp. Externality was a good predictor of weight gain at the end of the summer camp. Conversely, enforced overeating and weight gain is not associated with increased responsiveness to external cues.51 Thus, we suspect that externality is more likely to precede overweight and to have a causal role in promoting behaviors associated with weight gain.
In relation to the second question (what causes heightened reactivity?), both deterministic and environmental explanations might be invoked. Consistent with a deterministic account, in children, there would seem to be a significant genetic component to variability in BMI52 and this appears to be partly explained by variation in parental reports of food-cue responsiveness.53 The reason for this genetic variation remains open to debate. One suggestion is that in our ancestral past body fat was regulated by upper and lower ‘intervention limits’.54 The lower intervention limit was set by the risk of starvation and the upper intervention limit was set by the risk of predation. This ‘drifty gene’ hypothesis proposes that as social communities developed, humans were released from the risk of predation and the upper limit on body fat became subject to random genetic drift.54 For now, the behavioral correlates of this drift remain to be identified. We suggest that heightened reactivity might serve to defend against a digression below a genetic ‘ideal’ bodyweight. Thus, it may be this departure from ideal (and not absolute) bodyweight that explains variation in food-cue reactivity.
An alternative explanation is that cue reactivity is learned in childhood. Jansen et al.9 propose that reactivity results from an association that forms between a food cue and subsequent eating behavior, and that these classically conditioned associations are stronger in overweight children because their parents encourage ‘plate cleaning’. This prospect remains to be explored. However, it may be relevant that obese children eat relatively faster and with larger bites, and they accelerate their eating rate toward the end of the meal, but only in the presence of a parent.55
Other findings from this study also warrant discussion. We found evidence that the effects of cueing on desire to eat and prospective portion size are not specific to the cued food (pizza). Cue exposure also increased prospective portion size and desire to eat non-cued foods, including; ‘chicken tikka masala’, ‘pasta and tomato sauce’ and ‘scrambled egg, chips and beans’. By contrast, cue exposure had little effect on desire to eat and prospective portion size for ‘chocolate buttons’ or ‘cake’. Consistent with our previous work,7 and contrary to previous reports,8 the effects of cueing appear to generalize to other non-cued foods, but only those that share common super-ordinate characteristics. In our study, overweight individuals reported a relatively greater increase in their desire to eat one of the non-cued foods (‘scrambled eggs, chips and beans’). In future, it would be interesting to pursue the hypothesis that the effects of food-cue exposure are more generalized in overweight participants.
In conclusion, the results from this study suggest that overweight individuals are especially sensitive to the effects of food-cue exposure on the motivation to consume food. Specifically, in overweight individuals, food-cue exposure (i) elicited a stronger salivary response and (ii) evoked larger changes in desire to eat pizza and a non-cued food (‘scrambled egg, chips and beans’). These findings are consistent with evidence that snacking and meal variability predict weight gain43, 44, 45, 46 and they expose ‘cue reactiveness’ as a potential predisposing factor for overweight.
This research was supported by a grant from the Economic and Social Research Council (RES-000-22-1745) on individual differences and food-cue reactivity, awarded to JMB.
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Scientific Reports (2017)