Effects of Different Breakfast Cereals on Alertness and Wellbeing

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Introduction
There has been extensive research on the associations between eating breakfast and wellbeing (see Smith, 2018 for a review). In many of these studies the nature of breakfast has varied considerably, and it is often unclear whether breakfast is beneficial or whether skipping breakfast has negative effects. Smith (2018) examined the behavioural effects of eating a high carbohydrate breakfast cereal, namely cornflakes. The aim of this research was to identify sensitive outcome measures that could then be used to assess the effect of breakfast type and characteristics of the person eating it. The main objective of the present study was to extend this research by investigating the effects of two other breakfast cereals and comparing them to a no breakfast condition. A second aim was to compare the two cereals to determine whether their ingredients led to different behavioural effects. One line of research has focused on the fibre content of RTEC (Smith, Bazzoni, Beale, Elliott-Smith, & Tiley, 2001). The results demonstrated that consumption of cereals high in fibre led to increased mental energy. A two week intervention study showed that eating high fibre breakfast cereal led to reduced fatigue. It was suggested that these results reflected improved digestion. Smith (2010aSmith ( , 2011 carried out secondary analyses of a large general population database (Smith, Johal, Wadsworth, Davey Smith, & Peters, 2000) and found that digestive symptoms were related to reduced wellbeing (Smith, 2010a(Smith, , 2011. These results are consistent with research that has shown impaired cognitive function in people with irritable bowel syndrome (Berrill et al., 2013;Kennedy et al., 2014). Further analyses demonstrated that the benefits of consuming a high fibre diet did not reflect fewer digestive problems (Smith, 2010a). Another possible mechanism was that wheat bran stimulates good bacteria in the colon which might then produce behavioural changes. However, the hypothesis that wheat bran is a prebiotic has not been supported (Smith, Deaville, & Gibson, 2018) but this research led to investigation of established prebiotics (e.g. inulin) which are often added to other food products.
Inulin is found in many plants such as onions, leeks, garlic, artichokes and chicory. It is added to certain foods to replace carbohydrates or fats, increase fibre, or as a prebiotic (Gibson, Beatty, Wang, & Cummings, 1995;Roberfroid, 2007). It is often combined with oligofructose, and research has often used this combination. Oligofructose-enriched inulin (Orafti®Synergy1) consists of chicory-derived inulin enriched by a specific fraction of oligofructose, produced by partial hydrolysis of chicory inulin in about a 50/50 ratio. Smith (2005) conducted a two week intervention study using 10g of oligofructose-enriched inulin compared to a maltodextrin placebo. Inulin did not improve mood, well-being or performance but was associated with an increase in digestive problems (wind, feeling bloated and stomach cramps). It is likely that any beneficial prebiotic effects may have been negated by the increased digestive problems. Smaller doses (2g) are added to food and there is evidence that these smaller doses may have beneficial behavioural effects especially when combined with carbohydrate. Smith, Sutherland and Hewlett (2015) compared the effects of 5g inulin combined with food with placebo and found beneficial effects on digestion, memory and mood over a 4 hour testing period. Another study (Smith, 2019) used a larger dose (13g) of inulin over a longer time period (12 hours). The results showed increased digestive symptoms, a more negative mood and impaired memory after ingesting inulin.
In order to eliminate negative effects due to increased digestive problems, the present study examined the effects of an inulin supplement (2g) in a commercially available breakfast cereal. This test cereal was compared with "Rice Krispies" which had a similar nutritional composition and a "no breakfast" condition. The design of this second study was similar to that used by Smith (2005) and the duration was 14 days which is a long enough time period to demonstrate effects of any changes in gut flora. The outcome measures consisted of questionnaires used by Smith et al. (2001) and Smith (2010b) to examine the effects of wheat bran and other types of breakfast cereal. In addition, ratings of alertness were made using visual analogue scales before and after breakfast. The study of wheat bran and other research on the effects of breakfast showed that alertness is increased by regular consumption of high fibre breakfast, as seen in pre-breakfast ratings, and acutely by breakfast consumption, as revealed by post-breakfast ratings.
The main objective of the present study was to compare RTEC meals with a no breakfast condition, and to identify cereal-specific differences. This was done using adults and children and effects were investigated over time. Measures included general wellbeing and ratings of alertness at specific times. This approach aimed to identify behavioural changes which could then form the basis for further research identifying underlying mechanisms and where microbiological assays of gut flora are required, and other indicators of prebiotic metabolites measured.

Methods
The study was approved by the ethics committee, School of Psychology, Cardiff University, and carried out with the informed consent of the volunteers. Consent was given by the Head Teacher who agreed that the school would take part before any parents were approached. Consent was then obtained from each adult from each family and from one adult from each family on behalf of their child or children.

Design
A between groups design was used with the volunteers consuming the different breakfast cereals (or no breakfast) for two weeks. All members of the same family were assigned to the same breakfast condition.

Recruitment Procedure
Recruitment consisted of an advertisement for participants in school newsletters. Those who responded and fulfilled the inclusion and exclusion criteria (see below) were recruited. Recruitment continued until the required number of participants were obtained. The participants were recruited from primary schools in Cardiff. Parent and child volunteers were assigned to either the Rice Krispies (food name: toasted rice cereal), Multigrain (food name: Sweetened Multi-grain cereal shapes with natural prebiotic), or the no breakfast condition. They received an honorarium of £50 per individual taking part, and each school also received a single honorarium of £150.
At the start of the study, each family was given an opportunity to try the available cereals. Nobody taking part in the study was expected to eat a cereal or abstain from breakfast if that was not acceptable to them. Those interested in taking part completed a simple screening questionnaire over the telephone to check the exclusion/inclusion criteria before being entered into the study.

Exclusion Criteria
Exclusion criteria were: (a) existing disease or use of long term medication (b) heavy smoking (>10 cigarettes a day -this applied to adult participants only) (c) alcohol consumption above 20 units a week (for female adults) and above 30 units a week (for male adults), and (d) relevant food allergies.

Inclusion Criteria
Participants had to either be (a) willing to consume the allocated breakfast cereal every day for two weeks or (b) willing to abstain from eating breakfast for two weeks. In addition, children had to attend primary school, and each participating family had to consist of at least one eligible adult and one eligible child. Table 1 shows the number of adults and children in each condition and gender and age characteristics.

The Two Cereals
The ingredients of the two cereals are shown in Table 2.

Outcome Measures
Adult volunteers completed a baseline questionnaire (about themselves and their children). Adult and child participants then consumed the chosen breakfast cereal or no breakfast (if that was usual for the child) for two weeks. Adult participants rated their own and their child or children"s wellbeing by completing questionnaires every week (see supplementary material). These questionnaires were used because of their prior use in studies of the effects of breakfast cereal (Smith et al., 2001) and other types of cereal (Smith, 2010(Smith, , 2018. They also rated their own and their children"s alertness levels before and after breakfast at baseline and days 7 and 14 using a visual analogue scale (see supplementary material).

Testing Schedule
The details of the study and how to complete the questionnaires were explained carefully and in full at initial meetings with the families. At these meetings they were given the opportunity to try the available cereals). Adult participants were given the participant information sheet and completed the consent forms and the baseline questionnaire (see supplementary information). At the end of the meeting families were given a 14 day supply (each serving being 30g) of their chosen breakfast cereal (if appropriate) and the two weekly questionnaires (see supplementary information). They were also given a reminder sheet summarising when they should complete each part of the study. The weekly questionnaires were completed at home by the adult participants.

Statistical Analysis
Following data collection an anonymised database was created. All names and other identifying details were removed so that no data could be linked back to any individual or to any school. The baseline characteristics of the cereal/no-breakfast groups were compared using ANOVA and Chi-squared analyses. There were no significant gender differences between the breakfast conditions for either adults (p = 0.97) or children (p = 0.54).
The ages of the adults in the groups were also similar (p = 0.18), but the children in the no-breakfast group were slightly older than those in the other three conditions (p = 0.01). The final database was used in analyses of co-variance. The initial factors in the model were the baseline covariates. Cereal and no-breakfast conditions were then compared. The amount of missing data was small and the accuracy of data input high.

Effects of Breakfast on Wellbeing
Those in the breakfast cereal conditions had lower scores than the no breakfast group for depression, anxiety, cognitive difficulties, emotional distress, somatic symptoms, fatigue, general health and digestive symptoms (see Table 3; all p values < 0.001). These effects appeared consistent across the different cereals, across both adults and children, and were significant at both week 1 and 2 (after adjusting for baseline scores).

Breakfast, Inulin and Alertness
The wellbeing measures showed big differences between the no-breakfast and the cereal conditions but little difference between the Rice Krispie and Multi-grain groups. However, the alertness ratings at day 14 revealed significant differences not only between the cereal conditions and no-breakfast condition, but also between the Rice Krispie and Multi-grain groups. These results are described in Table 4 and it can be seen that the cereal with inulin (the Multi-grain group) was associated with significantly higher alertness scores than the Rice Krispie group. The differences between the cereal conditions were observed for both adults and children.

General Effects of RTEC:
The results from this study confirm that consumption of breakfast cereal is associated with better wellbeing. However, there was no evidence of significant differences in the effect on wellbeing between the two cereals.

Differences between Cereals:
Inulin has been used to supplement breakfast cereal and this study involved a 14 day intervention and compared effects of no breakfast, Rice Krispies and a Multi-grain cereal fortified with 2g inulin. This was part of a programme of research which examined effects of breakfast cereal on adults and children (Smith, 2010b) with a special emphasis on the alerting effects of consuming ready-to-eat breakfast cereals (Smith, 2018). The results from this study confirmed the wide ranging benefits of consuming breakfast. The effects of adding inulin to the cereal were more specific, with alertness increasing only after 14 days of consumption. This is similar to the result found in an earlier wheat bran intervention study (Smith et al., 2001). However, this alerting effect was not found in a similar intervention study with a higher dose of inulin (Smith, 2005). It is possible that the negative effects of a larger dose of inulin counteract longer term prebiotic effects that may occur with smaller doses eaten with carbohydrate. Smith (2005) put forward two possible mechanisms that could underlie effects of inulin on alertness. The first involves fibre being fermented by gut flora to produce short chain fatty acids. The subsequent use of short-term fatty acids can then provide a major contribution to a person"s energy needs. Acetate leads to ATP being generated, and, in addition, short-term fatty acids have been shown to have neuro-active properties (Sampson & Mazmanian, 2015). The second mechanism is detoxification. Clostridia form neurotoxins and these come from protein metabolism rather than from carbohydrate or fibre. Fibre stimulates bifidobacteria and lactobacilli that do not give rise to toxins. The detoxification that follows ingestion of prebiotics is a slow process and the energising effects of short-term fatty acids would appear to be better able to account for the alerting effects of the inulin seen in the present study.
The present research has a number of limitations. A first limitation of the study was the type of cereal used. The Multi-grain and Rice Krispie conditions had very similar macro-nutrient composition. However, the Multi-grain cereal included flour from other cereals that may have prebiotic effects which means that one cannot definitely attribute differences between the cereals to the supplementation of inulin. Another limitation was the lack of appropriate physiological measures to identify underlying mechanisms. The study of pre-biotic effects has largely been based on faecal sampling but in the future it will be important to also use other invasive techniques to investigate changes in the microbiota in the upper gut (Desmedt et al., 2019). In order to examine the gut-brain axis it will be important to use a multi-method approach including metagenomics, metatranscriptonomic and metaproteonomic analysis (Desmedt et al., 2019). Gas or liquid chromatography, in combination with mass spectroscopy, could measure changes of key metabolites. Imaging mass spectroscopy could present a clearer profile of the interaction between the brain and gut microbes. Using this scale, we"d like to ask you about some physical symptoms that people often experience. For each symptom we would like you to indicate how much that problem has bothered or distressed you during the past seven days, including today. For each, we"d like you to answer by circling "not at all", "a little bit", "moderately", "quite a bit" or "extremely".
In the past seven days how often were you bothered by : Over the last week please indicate how many bowls of breakfast cereal you consumed each morning for breakfast (please round up to the nearest half bowl). Also would you indicate how much you enjoyed the cereal on a scale of 0 to 10 where 0 = not at all and 10 = very much indeed. If you were not supplied with breakfast cereal please put 0 bowls consumed for each day.

Number of bowls consumed each day How much did you enjoy it (0-10)? Monday Tuesday Wednesday Thursday Friday Saturday Sunday
Thank you for completing this section of the booklet. Now please make sure that a separate section is completed for each member of your family taking part in the study.
This section of the booklet is for the first child who is taking part in the study. It should be completed on DAY 7 by an adult on behalf of the child. If more than one adult from your family is involved in the study, either or both of them can complete this section. It should take up to an hour to fill in.
The questions in this section are worded in exactly the same way as they were in the section about you. This may make one or two of them seem unusual to ask about a child. We have done it like this so that we can compare the information with our previous work on adults.
It is important that you complete the questions on behalf of your child. There is no need to directly ask him or her any of the questions. We are simply trying to get an overall impression of your opinion about him or her. To make things easier, each person"s section is colour coded: 1 st adult = green; 2 nd adult = yellow; oldest child = blue; 2 nd child = purple; 3 rd child = pink; 4 th child = orange; 5 th child = cream. It is very important for us that you stick to these colours for each person for ALL of the study! This questionnaire starts with some questions about how alert each person is feeling. As we explained when we met you, you need to complete these questions on DAY 1 of the study, BEFORE and then again AFTER each person has breakfast. If you have not been supplied with breakfast cereal please complete these questions soon after each person gets up and again about an hour later.
The questions about alertness may take about 30 minutes to complete altogether. To make things easier, each person"s sections are colour coded as before: 1 st adult = green; 2 nd adult = yellow; oldest child = blue; 2 nd child = purple; 3 rd = pink; 4 th child = orange; 5 th child = cream. It is very important for us that you stick to these colours for each person for all of the study!

ALERTNESS RATING DAY 1 BEFORE BREAKFAST
ADULT 1 On each of the following lines please draw a cross between the two extremes which best represents how you are feeling now. ADULT 1 / ADULT 2 On each of the following lines please draw a cross between the two extremes which best represents how your child is feeling now.

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