Does flavour-nutrient inconsistency compromise energy regulation in humans?

Lead Research Organisation: University of Bristol
Department Name: Experimental Psychology

Abstract

The modern invention of processed foods has fundamentally changed our food environment. Retailers now stock an extremely wide range of foods. Even single types of food (e.g., pizza) are now available in numerous varieties that differ in size and the number of calories that they contain. For example, our data show that the number of calories in fish pie 'ready meals' can vary by up to 450% in the UK. In animals, this kind of 'variability' promotes overeating and an increase in body weight. For the first time, this project will explore whether this also happens in humans. There are two ways in which variability in our food environment might increase the number of calories that we consume. These are summarised below. In PHASE 1 we will look at our capacity to 'compensate' for calories in food. When we consume one meal shortly after another then good compensation occurs when the size of the first meal controls the size of the second meal (i.e., a larger first meal causes people to consume a smaller second meal). In animals, poor compensation has been linked to a degraded 'cephalic-phase response.' This anticipatory response governs appetite and represents a series of physiological changes (e.g., salivation and insulin release) that prepare the body for the consumption and digestion of food. Critically, merely looking at or smelling a food is sufficient to elicit a response that is proportional to the calories contained in a food. This shows that learning is involved and that responses are based on previous encounters with individual foods. In this phase we will determine whether the cephalic-phase response is reduced in highly variable foods and whether this promotes poor compensation leading to overconsumption. Cephalic-phase responses will be measured in a number of ways. In particular, we will develop a new method based on changes in skin temperature near to the liver. Previously, researchers have found that this 'thermogenic response' is particularly sensitive to different foods. In this interdisciplinary project we will work with an expert in sensor technology to develop this sensitivity still further. In PHASE 2 we will explore the idea that variability in our food environment makes it more difficult for us to predict the extent to which a particular food will stave off hunger. In 2002 a Nobel Prize was awarded for advances in the field of behavioural economics. This work shows that uncertainty tends to generate cautious and conservative responses and has been used extensively to predict animal behaviour and a range of decisions relating to gambling, financial trading, and risk taking. We find it surprising that 'prospect theory' has not been applied to understand dietary behaviour in humans. For the first time, we will draw on these principles to test the idea that our variable food environment causes uncertainty about the effects of consuming a food, which creates confusion and a concern that hunger might be experienced after it has been consumed. In response to this uncertainty we make conservative dietary decisions and select and then consume larger portions of food. In summary, this project will address important questions relating to variability in our dietary environment. Previously, this issue has been largely overlooked. Nevertheless, research in animals would suggest that variability has the potential to play an important role in promoting overeating and obesity. The beneficiaries of this project are wide ranging. For individual consumers, this might involve increased public awareness of the effects of variable foods. For children, guidelines and/or legislation might be introduced to limit exposure to highly variable foods. For obese individuals, interventions might be possible that re-train sensitivity to the calories contained in specific foods. As such, this work has considerable potential to impact a number of groups, including; health professionals, policy makers, educators, and the wider public.

Technical Summary

Over time, the orosensory properties of a food can serve as a cue (conditioned stimulus) that enables an individual to predict the caloric consequences of consuming a particular food. When these 'flavour-nutrient associations' are disrupted this promotes imprecise caloric regulation and weight gain in rats. In the UK, foods are now highly processed and their energy density is manipulated routinely. This increases exposure to inconsistent flavour-nutrient pairings. For the first time, this project will elucidate the effects of these inconsistent parings in humans. Specifically, it will explore two hypotheses. In Phase 1 we will test the hypothesis that inconsistent flavour-nutrient pairings disrupt learned cephalic-phase responses to food and that this compromises the ability to compensate for calories in food from meal to meal. As part of this research we will draw on expertise in 'sensing technology' to refine methods for measuring thermogenic responses to food. In Phase 2 we will test the hypothesis that inconsistent flavour-nutrient pairings have a direct effect on meal size, specifically, that they create 'uncertainty' (psychological) about the satiety that a food is expected to confer, and that this promotes the selection of larger meals. Despite its otherwise widespread application, this is the first time that 'prospect theory' will be used to make predictions about human dietary behaviour. In total, 11 studies will be conducted. Nine of these will be controlled laboratory experiments involving participants drawn from local staff and student populations. Four of these will use a 'preload' paradigm and two will establish causality by manipulating flavour-nutrient consistency directly. Two online studies will be conducted using custom software, written in Java script. This research will identify specific ways in which our modern food environment promotes obesity in the UK. As such, it will impact academics, the food industry, and the general public.

Planned Impact

In response to the question 'Who are the beneficiaries of this research?' we have inserted five subheadings below. Under each subheading we have added text that identifies 'How will user groups benefit from this research?' 1. FOOD COMPANIES Multi-national food companies have long recognised that a competitive advantage can be gained by developing foods that confer health benefits. In particular, several companies (e.g., Unilever and Nestlé) develop and produce products that are specifically designed to aid weight loss by promoting satiety. This project will be of considerable benefit to these users because it will offer a methodology to evaluate their variability and the extent to which this impacts on the satiety that they confer. To this end, our measure of the thermogenic response has the potential to offer a highly informative, sensitive, and non-invasive assessment of the cephalic-phase response. To the applicants' knowledge, in the context of food variability, this has not been considered previously, in either an academic or an industry context. 2. HEALTH PROFESSIONALS/CLINICIANS If we are successful in establishing a relationship between food variability and overconsumption then this will offer an opportunity for health professionals and clinicians to develop appropriate intervention techniques that retrain sensitivity to the caloric content of foods in obese individuals. 3. POLICY MAKERS Research of this kind will assist policy makers because it has the potential to reveal a hitherto unknown relationship between our food environment and energy intake. In particular, this research will help to inform guidelines around healthy eating in adults. In children, it might also generate debate relating to whether children should be exposed to a variable food environment during their formative years. 4. NHS AND SOCIAL SERVICES The cost of obesity to the NHS and social services is considerable and it is expected to rise well above inflation over the next few decades. Not all countries have the same problem, and this is the case even after controlling for GDP. Therefore, it is important to carry out basic research that identifies ways in which specific aspects of our food environment contribute to overconsumption. If this can be achieved then changes to our food environment may be possible, offering an opportunity to implement cheap and effective solutions that reduce the burden of obesity on the NHS and related social services. 5. WIDER PUBLIC In addition to the above, the wider public will benefit from an opportunity to take individual and more informed control of the foods that they consume and the foods that they give their children.
 
Description The modern invention of processed foods has fundamentally changed our food environment. Retailers now stock an extremely wide range of foods. Even single types of food (e.g., pizza) are now available in numerous varieties that differ in size and the number of calories that they contain. In animals, this kind of 'variability' promotes overeating and weight gain. This project represents the first systematic translation of these findings to the study of obesity in humans.

Our research indicates that exposure to a wide variety of the same kind of food (e.g., pizza) promotes uncertainty about the energy content and expected satiation of that type of food. Specifically, we've shown that people tend to underestimate the expected satiation a food that they are uncertain about. For instance, we found that participants who had consumed a wide variety of pizzas (of various portion sizes and energy densities) believed that a portion of pizza would be less satiating compared to participants who had consumed fewer pizzas. Importantly, these expectations translated to real-life differences in food intake-when fed a portion of pizza and then given access to a second snack, the participants who had been exposed to a wide variety of pizzas ate more than the participants who had been exposed to fewer pizzas (Hardman et al., in prep). These findings suggest that dietary complexity reduces satiation and increases food intake, thereby contributing to weight gain.

Our research indicates that highly variable foods may also contribute to weight gain by reducing energy expenditure. One of the advantages of being able to accurately predict the energy content of food is that our body can generate anticipatory physiological responses which increase the efficiency of nutrient absorption. One of these 'cephalic phase responses' is thermogenesis-the increase in body heat which occurs before and during food intake. This increase in body temperature indicates an increase in energy expenditure; thus, decreases in cephalic phase thermogenesis could contribute to small but meaningful increases in body weight over time. Using a novel technique we developed for measuring thermogenesis in humans, we showed that cephalic phase responses were weaker in people who had highly variable dietary experiences compared to people with more limited and consistent dietary experience (Griggs et al., 2013; Coffey et al, 2013; Griggs et al., in prep.). This is the first demonstration that dietary complexity disrupts cephalic phase responses in humans, and identifies a second mechanism by which the current food environment might be contributing to obesity.

Food variety is not the only source of uncertainty in today's environment- uncertainty regarding when and how much one plans to eat at their next meal could also bias people to overeat. In order to determine whether these sources of uncertainty are also problematic for weight control, we conducted experiments in which we explored how the time until the next meal (i.e., the inter-meal interval) influenced how much food participants chose to consume during a lunchtime meal. We observed that participants elected to consume more food at lunch when the post-meal interval was longer than when it was shorter; however, uncertainty about the time of the next meal did not bias participants to overeat. This finding suggests that the uncertainty about the energy content of a meal may be more problematic for weight control than uncertainty about meal timing.
Exploitation Route Our research highlights and extends knowledge about why the current food environment is proving so detrimental to food intake and weight control. Our research indicates that it is not only the increased access to food today that has led to obesity; it is also the increased variety of food available today which is problematic. We believe this work can be used by health professionals and policymakers to increase public awareness regarding the effects of highly variable foods-for instance, guidelines and/or legislation might be introduced to limit exposure to highly variable foods as preventative measures for obesity, especially in children. For obese individuals, this work highlights the necessity of developing new strategies for managing intake of highly variable foods other than those that rely on estimates of energy content or satiation. Food companies and manufacturers might benefit from our work by using our methods to evaluate the variability of their food products and the impact of this factor on satiety. Generally, the wider public will benefit from an opportunity to take more informed control of the foods that they consume and the foods that they give their children.
Sectors Agriculture

Food and Drink

Communities and Social Services/Policy

Healthcare

Other
URL http://www.bris.ac.uk/expsych/research/brain/nbu/currentprojects/bbsrcflav.html
 
Description Findings and methods developed as part of this award have been used in collaborative projects with two major food companies. In both projects our objective has been to explore opportunities to modify commercial products in ways that sustain consumer acceptance but deliver reduced energy intake. One of these projects explored the extent to which the energy-density of commercial food offering can be reformulated to reduce calorie content. Much of this research formed the basis for a follow-on project (EU Seventh Framework Programme [grant number 607310].). In this project, and building on work that stemmed from this BBSRC award, we showed that consumer acceptability of a reformulated food will depend on its initial energy density. Larger shifts changes in energy density can be achieved in products are are already especially energy dense. (https://www.ncbi.nlm.nih.gov/pubmed/29038018)
First Year Of Impact 2015
Sector Agriculture, Food and Drink
Impact Types Societal

Economic
 
Description FP7 EU consortium (Nudge-it)
Amount £567,528 (GBP)
Funding ID Grant Agreement 607310 (Nudge-it) 
Organisation European Commission 
Department Seventh Framework Programme (FP7)
Sector Public
Country European Union (EU)
Start 01/2014 
End 12/2018
 
Title Continuous assessment of diet-induced thermogenesis 
Description The consumption of food triggers a series of physiological responses that serve to optimise the digestion, absorption and use of the ingested nutrients. These responses can also be conditioned (cephalic phase responses) and, so, can be elicited by cues that have previously predicted food intake. Thermogenesis (i.e., the increase in body temperature which occurs immediately before and during eating) is one such cephalic phase response that can be conditioned by food cues. Typically, the stronger the association between a food cue and its associated caloric outcomes, the greater the magnitude of its cephalic phase response (i.e., the greater the thermogenesis). In order to establish links between food-cue reactivity, dietary variety, and cephalic phase responses, our research team collaborated with Dr. Mike Halliwell at the School of Clinical Sciences and Dr. Jeremy Burn at the School of Anatomy to develop a non-invasive method for measuring thermogenesis in humans. In rats, thermogenesis has been assessed by implanting temperature-sensitive recording devices in the abdomen, near the location of the liver. Our approach consists of placing temperature-sensitive recording devices (thermistors) on the outside of the abdomen in the location of the liver. Ultrasound scanning (sonography) is used to identify the precise location of the liver for each participant, and temperature recording is collected from three independent thermistors which provide second-to-second recordings of core temperature change. This method allows for the continuous monitoring of thermogenesis for groups of participants, simultaneously. 
Type Of Material Physiological assessment or outcome measure 
Provided To Others? No  
Impact Until now, methods for assessing core temperature in humans has been limited to procedures which are invasive (ingestible capsules; rectal probes) and quite expensive (indirect calorimetry via respiration chambers). Our technique capitalizes on what is already known about assessing thermogenesis in non-human animal models to provide a non-invasive, cost-effective method for monitoring core temperature in humans. This method does not require expensive / unwieldy equipment and, as such, recordings can be collected from multiple participants simultaneously and can be conducted outside of the laboratory. We expect this methodology will impact scientists by offering a relatively cheap, reliable, and flexible way of assessing thermogenesis in humans. 
 
Title Measurement of food loss aversion 
Description Nobel-prize winning research in the field of behavioural economics has shown that uncertainty biases human decision making in highly predictable ways. 'Prospect theory' is now well established and is used extensively to predict animal behaviour and a range of decisions in humans including judgements relating to gambling, financial trading, and risk taking. However, these principles have not yet been applied to understand food choice and dietary behaviour. One measure that has been used to examine responses to uncertainty is 'loss aversion'. Loss aversion refers to the tendency to avoid choices that might result in a loss of some kind. This characteristic is typically measured with a gambling task where the participant is faced with uncertain odds and must decide on each trial whether to gamble (and risk losing, or gaining, a monetary reward). For the first time, we've adapted this task to assess how individual differences in risk taking (i.e., loss aversion) influence dietary decisions. Briefly, participants are presented with a portion of food that they are told will serve as their main meal. On each trial, however, the participant can choose to gamble in order to receive a different portion of food (i.e., one that is of a larger or smaller portion than his current portion). This task allows us to assess, a) whether individuals who show high levels of monetary loss aversion also make more cautious decisions when it comes to gambling for food (i.e., are more likely to gamble to increase their portion in an effort to avoid the adverse consequences of feeling hungry / experiencing the 'loss' of satiation) and, b) whether individual differences in the ability to tolerate food loss (i.e., eating more or less than one would prefer) predicts one's risk of overeating. 
Type Of Material Model of mechanisms or symptoms - human 
Provided To Others? No  
Impact We expect that this method will shed new light on how decision-making processes impact food choice and intake, and introduce a new way of understanding ingestive behaviour (i.e., via prospect theory). 
 
Description Field work with the Samburu tribe in Kenya 
Organisation Bucknell University
Department Department of Psychology
Country United States 
Sector Academic/University 
PI Contribution Professor Peter Rogers and Professor Jeff Brunstrom contributed their expertise in human dietary behaviour. In particular, Jeff Brunstrom contributed his knowledge of flavour-nutrient learning and its effect on appetite and food choice, and Peter Rogers contributed his knowledge of sugars and the role of sweet taste in appetite control.
Collaborator Contribution Dr Jon Holtzman is a cultural anthropologist from Western Michigan University who has studied the Samburu tribe for many years. He contributed his expertise in Samburu culture and served as a liason during our time in Kenya. Dr Kevin Myers is an expert in animal dietary behavior from Bucknell University. He contributed his expertise in learned food preferences and flavour-nutrient learning.
Impact This collaboration represents a novel interdisciplinary collaboration that fuses the comparative perspective of cultural anthropological approaches with rigorous empirical methods. The Samburu are an indigenous population of semi-nomadic pastoralists who live in a remote arid area of North Central Kenya. The Samburu are interesting to us because they have been exposed to a very narrow range of foods-- no 'processed' foods and certainly no 'diet' products or diet sodas. This makes them an ideal population to study because they can help us to understand the comparative effects of exposure to dietary variability and complexity in our own dietary environment (a central theme of our ongoing BBSRC-funded project). Through our research we have learned a lot about cultural differences in response to sugar and the role that sweetness and artificial sweeteners might play in the control of appetite (e.g., how Westernized environments may alter our learning about sweetness and appetite control). Several papers are in preparation based on this work.
Start Year 2014
 
Description Field work with the Samburu tribe in Kenya 
Organisation Western Michigan University
Country United States 
Sector Academic/University 
PI Contribution Professor Peter Rogers and Professor Jeff Brunstrom contributed their expertise in human dietary behaviour. In particular, Jeff Brunstrom contributed his knowledge of flavour-nutrient learning and its effect on appetite and food choice, and Peter Rogers contributed his knowledge of sugars and the role of sweet taste in appetite control.
Collaborator Contribution Dr Jon Holtzman is a cultural anthropologist from Western Michigan University who has studied the Samburu tribe for many years. He contributed his expertise in Samburu culture and served as a liason during our time in Kenya. Dr Kevin Myers is an expert in animal dietary behavior from Bucknell University. He contributed his expertise in learned food preferences and flavour-nutrient learning.
Impact This collaboration represents a novel interdisciplinary collaboration that fuses the comparative perspective of cultural anthropological approaches with rigorous empirical methods. The Samburu are an indigenous population of semi-nomadic pastoralists who live in a remote arid area of North Central Kenya. The Samburu are interesting to us because they have been exposed to a very narrow range of foods-- no 'processed' foods and certainly no 'diet' products or diet sodas. This makes them an ideal population to study because they can help us to understand the comparative effects of exposure to dietary variability and complexity in our own dietary environment (a central theme of our ongoing BBSRC-funded project). Through our research we have learned a lot about cultural differences in response to sugar and the role that sweetness and artificial sweeteners might play in the control of appetite (e.g., how Westernized environments may alter our learning about sweetness and appetite control). Several papers are in preparation based on this work.
Start Year 2014
 
Description Modelling the effects of dietary complexity on body weight and adiposity 
Organisation University of Bristol
Department Modelling Animal Decisions (MAD) group
Country United Kingdom 
Sector Academic/University 
PI Contribution Professor Jeff Brunstrom, Professor Peter Rogers and Dr Danielle Ferriday provided theoretical background for the project and were integrally involved in deciding the assumptions to be tested within the model. All have been involved in interpreting the data from the model and in preparing a manuscript for submission to the International Journal of Obesity.
Collaborator Contribution Professor Alasdair Houston and Dr Andrew Higginson used their extensive expertise in state-dependent dynamic programming models to program and run a model exploring the effects of; i) increases in energy density and ii) uncertainty about energy density on adiposity and body weight. Both have been involved in interpreting the data from the model and in preparing a manuscript for submission to International Journal of Obesity.
Impact Various empirical studies using rodents implicate flavour-nutrient inconsistency as something that is detrimental - inconsistency causes animals to gain weight and to lack an ability to 'compensate' for calories. Intuitively, this makes sense. The prevailing view is that flavour-nutrient (F-N) learning is an important component of dietary control. Therefore, disrupting this ability should have 'negative' consequences. For the first time, this multi-disciplinary collaboration (between Experimental Psychologists and Theoretical Biologists) tested the logic behind this hypothesis. Our modelling has shown that F-N inconsistency only generates an increase in energy reserves if particular assumptions are held. When other assumptions are made, energy reserves actually decrease. These various outcomes are interesting, because they generate a set of grounded and novel hypotheses about F-N inconsistency and the effect this has on food intake and bodyweight. We are currently preparing a manuscript for submission to the International Journal of Obesity later this year based on these findings. The findings from this collaboration will be presented to the University of Bristol 'Decision-making Research' group on the 20th November 2014.
Start Year 2012
 
Description Advisory panel for @Bristol Science and Discovery Center 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Professor Jeffrey Brunstrom and Dr Danielle Ferriday were members of a scientific advisory panel for a local science and discovery centre (@Bristol). Their specific role was to assist in scientific fact checking and idea generation for interactive displays in the development of their Food! exhibit. This exhibit aims to be an educational yet fun and interactive exhibit for children and their guardians to learn about where their food comes from and the science behind food development/food choice. Brunstrom and Ferriday attended meetings to assist in the development of interactive displays and shared current scientific findings to assist the team @Bristol. They also assisted in the development of online materials for interested parties. The exhibit launched on 23rd July 2014.

@Bristol receives hordes of visitors each year and the Food! exhibit has already received lots of positive feedback/interest. Through the explore more website, any parent/child who is interested can find out further information.
Year(s) Of Engagement Activity 2012,2013,2014
URL http://www.at-bristol.org.uk/2337
 
Description BBC Radio 4 Food Programme 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Participation in radio broadcast which sparked discussion about food cravings and preferences.

Increased public awareness regarding the factors which contribute to food choice.
Year(s) Of Engagement Activity 2012
URL http://www.bbc.co.uk/programmes/p00yyr41
 
Description Café Scientifique meeting, Explore at-Bristol 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Talk generated a Q&A afterwards which was followed by informal discussions with several members of the public.

One member of the audience asked me about job opportunities and access to a career in science.
Year(s) Of Engagement Activity 2012
 
Description Interactive demonstration @Bristol science and discovery centre 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Christina Potter (Ph.D. student) designed an interactive demonstration with project staff at At-Bristol for visitors at the Science centre. In the demo, we presented various portion sizes of a snack food (wine gums). The wine gums were presented in different portion sizes on 9 plates, ranging from 2g (one wine gum) up to 386g (a full plate of wine gums). Children had the option to try a wine gum to eat. As a visual feedback, we displayed bar charts where children could place a sticker underneath a portion size which corresponds to their ideal portion as well as their maximum portion.

As many of our computerised tasks involve portion size selection, we felt that this educational activity paired well with the research task and helped to illustrate the difference between "ideal" portions and "maximum" portions. The researchers then used conversation cues for child/family groups, while being careful to avoid any assertive message about eating. These cues were implemented to generate a discussion with the family. Further, any questions that parents or children had about the research tasks, such as explaining the more scientific concepts of our measures (i.e. expected satiety), were answered by the research staff on site.

Example cues:
'How do you know when you're full?' This cue lead to conversations about physical and mental sensations of fullness and hunger.
'What do you think happens to food once it's inside your body?' This cue lead to conversations about your body using food to give you energy to do move/play, to allow you to grow, to help your body to recover if you're ill or hurt yourself.
"What is the most you could possibly eat?"
"What is your perfect amount to eat"

The overall feedback from both parents and children who took part in the activity was extremely positive. Many parents commented that they hadn't ever considered several of the topics that we discussed with their child (such as portion tolerance) and they were interested to learn more. The activity often lead to conversations about how children, particularly those younger in age, have "eyes bigger than their stomach" when selecting both their ideal and maximum potion sizes.
Year(s) Of Engagement Activity 2013,2014
 
Description Media interest (Beverages influence meal planning) 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Our results were disseminated to several regional and international news sources, as well as social networking sites.

The press coverage of our research sparked debate about the dangers of caloric beverages, specifically sugar-containing soft drinks, in appetite and weight control.
Year(s) Of Engagement Activity 2014
URL http://www.bristol.ac.uk/news/2014/july/soft-drinks-and-meal-planning.html
 
Description Media interest (Portion size, expected satiety, and the role of dietary variability) 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact Current research projects were highlighted on BBSRC website.

Web coverage of our projects highlighted our current lines of research, attracting new interest in our research team.
Year(s) Of Engagement Activity 2013
URL http://www.bbsrc.ac.uk/news/health/2013/130204-f-would-you-like-to-supersize-that.aspx
 
Description Stall at Food Matters Live 2016 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Industry/Business
Results and Impact More than 13,500 experts from across the food, health and nutrition sectors attended Food Matters Live 2016. The Nutrition and Behaviour Unit hosted a stall at this event and featured a Powerpoint projection which detailed current research projects/ideas, methodologies, facilities. Recent scientific publications were also available for distribution. This stall sparked interest, conversations and requests for further information.
Year(s) Of Engagement Activity 2016
URL https://www.foodmatterslive.com/