Carbohydrate consumption, mood and anti-social behaviour

7 Carbohydrate consumption, mood and anti-social behaviour D. Benton, Swansea University, UK

Abstract: Although there is a widespread popular assumption that the consumption of refined carbohydrate rapidly increases blood glucose and therefore enhances mood, controlled studies do not support such a view. It is also commonly suggested that a marked increase in blood glucose is followed by a rapid fall, resulting in a hypoglycaemic reaction with associated anxiety-like symptoms. It is, however, uncommon for blood levels to fall to the levels required to diagnose clinical hypoglycaemia. There are, however, several reports of an association between a tendency for blood glucose to fall rapidly, but not to levels necessary to diagnose hypoglycaemia, irritability and aggression. The consumption of meals that are almost entirely carbohydrate can increase the levels of tryptophan in the blood with consequences for the synthesis of serotonin in the brain and hence an improvement in mood. The evidence is, however, that this mechanism is blocked by relatively small amounts of protein in the diet, such that it occurs very rarely when normal meals are consumed. Similarly, there is no support from well-controlled studies for the suggestion that sugar consumption causes hyperactivity in children. There is, however, evidence that pleasant tasting foods, for example chocolate, release endorphins with associated improvements in mood. Key words: anti-social behaviour, carbohydrate, chocolate, hypoglycaemia, mood, pre-menstrual syndrome, seasonal affective disorder, serotonin, tryptophan.

7.1 Introduction In the general population, there is a widespread assumption that the consumption of refined carbohydrate, in particular sugar, results in a rapid enhancement of mood and increased alertness. A ‘sugar rush’ is experienced. It is suggested that in children hyperactivity may be observed following the consumption of sugar. However, it is also suggested that this supposed short-term stimulating effect is followed by a downward swing so that you subsequently become fatigued, irritable and feel low. A similar

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pattern is suggested to follow the consumption of any highly refined carbohydrates, such as those found in white bread or pasta. A related idea is that we should attempt to eat a low-glycaemic diet; one that causes only small changes in the level of blood glucose. Another suggested consequence is that a diet high in refined carbohydrate will have been stripped of micronutrients to the extent that subclinical deficiencies result, with further consequences for behaviour. Some have even suggested that sugar is physically addictive (Avana et al., 2008), although this is disputed (Benton, 2010). The consequences for mood of carbohydrate consumption are therefore considered, although many of these ideas have gained little support when examined in well-controlled studies.

7.2 Carbohydrate metabolism and mood 7.2.1 Short-term effects of carbohydrate intake The consumption of a sugary drink or snack is a common response to feeling low or tired, but does mood reflect the level of blood glucose? The examination of the short-term influence of carbohydrate on mood has either contrasted sugar or starch with high-protein foods, or has compared sucrose- or glucose-containing drinks with a placebo. Benton (2002) reviewed studies that compared the response to carbohydrate-rich and protein-rich foods. Several hours after eating a high-carbohydrate rather than protein-containing food, there is a tendency to report feeling less energetic. The effect is calming rather than stimulating. In the first hour after drinking a sugar-containing drink, there are some reports of small increases in subjective energy, but others report no effect. The response is small and not easily demonstrated. For example, Benton and Owens (1993) reported a small increase in energy 15–30 minutes after combining several studies to produce a sample of 354. There was no evidence of a ‘sugar rush’. Benton (2002) concluded that a major variable is the time when mood was assessed. The majority of studies measured mood about two hours after the taking the drink or meal, something true of the studies that reported an association between decreased subjective energy and carbohydrate consumption. The studies that found that energy increased after a sugarcontaining drink measured mood after 15, 30 or 60 minutes. Benton and Owens (1993) stated that short-term increases in reported energy seemed a robust phenomenon; it was, however, a limited effect that could not be expected to be observed with a small sample size.

7.2.2 Mood under demanding conditions The above findings involved studies in which subjects sat quietly after consuming carbohydrate. In contrast, Owens et al. (1997) suggested that there

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would be a stronger association between mood and blood glucose levels when subject to cognitive demand. As the brain has a high metabolic rate, it was proposed that the supply of glucose would be more influential while performing demanding tasks. When mood was assessed while performing three cognitively demanding tasks, falling levels of blood glucose were associated with feeling less energetic. Similarly, Benton and Owens (1993) found that those whose blood glucose remained at lower levels reported feeling more tense, possibly reflecting the activation of the autonomic nervous system in an attempt to increase blood glucose values.

7.3 The incidence of hypoglycaemia In the general population, there is a widespread belief that raising blood glucose levels will give mood a short-term boost, although as discussed above this is a false belief. However, in addition there is a common belief that such short-term gains are at the expense of a longer term hypoglycaemic reaction. The suggestion is that following a highglycaemic meal, the associated release of high levels of insulin will cause blood glucose to fall to a level at which the functioning of the brain is adversely influenced. Nabb and Benton (2006) gave eight breakfasts that varied in the speed at which they released glucose into the blood stream. They found that those with better tolerance reported generally better mood and those eating breakfasts that contained more carbohydrate were in the late morning tired rather than energetic. Is it, however, reasonable to describe such a reaction as hypoglycaemic? Benton (2002) discussed this question. A series of homeostatic mechanisms attempt to maintain blood glucose in a range of 70–100 mg/dl. Raising levels of blood glucose stimulates the release of insulin that causes glucose to be taken up by muscle and stored in the liver. When levels fall below the optimal range, steps are taken to increase the level of glucose including the release of glucagon that acts broadly in an opposite manner to insulin, releasing stored glucose from the liver. However the release of catecholamines, growth hormone and glucocorticoids also plays a role. If catecholamines are released these result in sweating, palpitations, weakness and anxiety, something that occurs when blood glucose is about 40 mg/dl, although there are individual differences. As these symptoms are similar to anxiety, they are often interpreted by the patient as such. Harris (1924) observed in non-diabetic patients symptoms similar to those that result from insulin-induced hypoglycaemia. He coined the term spontaneous hypoglycaemia as these symptoms were a reaction to food consumption. There is also a distinction between ‘reactive hypoglycaemia’ where blood glucose values are low and ‘essential reactive hypoglycaemia’

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in which such values are associated with spontaneous symptoms. In some individuals, the consumption of high-glycaemic meals has been related to feeling tired, ill, inadequate, anxious, depressed and even to psychotic disorders, alcoholism and violence. The question is the frequency with which such reactions occur. The writers of many popular books have suggested that reactive hypoglycaemia occurs commonly, although such a view has not been supported by systematic study. A glucose tolerance test (GTT) can be used to assess an individual’s ability to control blood glucose levels. After fasting overnight, the blood glucose profile is monitored following the consumption of 75 g of glucose. When 650 normal subjects took a GTT, Lev-Ran and Anderson (1981) found a large range of glucose nadirs. The median lowest value was 65 mg/dl and the 2.5th percentile was 39 mg/dl. Superficially, this might suggest that one in 40 healthy individuals have a tendency to have a hypoglycaemic reaction to their diet. However, when 135 individuals who were believed to have reactive hypoglycaemia were considered, only four proved to have the disorder. Arguably a GTT, although valuable when diagnosing diabetes, tells us little about our reaction to a normal diet. The picture that emerges when the response to normal diets is monitored is one of relative glucose stability. Alberti et al. (1975) monitored 19 normally fed individuals and reported ‘. . . very little variation in glucose concentration during the day’. They found that the pattern of glucose was quite different to that obtained during a GTT. Hansen and Johansen (1970) found that blood glucose levels never fell below 71 mg/dl and Genuth (1973) that they were never below 80 mg/dl. Thus, in most normally fed healthy individuals blood glucose values rise following a meal and then fall, but not to the level required to diagnose clinical hypoglycaemia. Various professional bodies have issued public statements. The American Diabetes Association, The Endocrine Society and The American Medical Association jointly issued a statement on hypoglycaemia (Statement, 1973). They stated that the public had been led to ‘to believe that there is a widespread and unrecognized occurrence of hypoglycemia in this country. Furthermore, it had been suggested repeatedly that the condition is causing many of the common symptoms that affect the American population. These claims are not supported by medical evidence.’ It is clear that only rarely does a meal induce levels of blood glucose low enough to attract a diagnosis of clinical hypoglycaemia. In a normal diet, the presence of protein and fat will slow the rate at which glucose is released into the blood. Yet Nabb and Benton (2006) found that meals containing larger amounts of carbohydrate were associated with feeling tired in the late morning, although blood glucose levels were not low enough to attract a diagnosis of hypoglycaemia. It seems possible that the rate at which blood glucose falls, rather than the lowest level reached, may be important.

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7.3.1 The control of blood glucose and mood The Quolla Indians in Peru and are known for their high murder rate and family feuds. Bolton (1973, 1979) noticed a strong craving for sugar and considered the possibility that their aggression reflected a tendency to develop low levels of blood glucose. He found in a GTT an association between a tendency for blood glucose to fall to low values and a history of being aggressive. Similarly, in Finland those with a history of violent crime have been found to develop low levels of blood glucose (Virkkunen, 1982; Virkkunen and Huttunen 1982; Virkkunen and Narvanem,1987). The study of Benton et al. (1998b) found a similar tendency in the normal population. In young adult males, those whose blood glucose levels fell more rapidly in a GTT were more likely to make aggressive comments when faced with a frustrating situation and were more likely to think that aggressive acts were justified. A similar study, using young adult females, found that those who had a tendency for blood glucose levels to fall to low levels during a GTT were more likely to display aggression (Donohoe and Benton, 1999). Gray and Gray (1983) suggested that an association between blood glucose levels and aggressiveness could not occur unless levels were low enough to be described clinically as hypoglycaemic. Donohoe and Benton (1999) illustrated that this was not the case. They found that a nadir of 63 mg/dl in a GTT was a value that distinguished those with greater tendency towards aggression; that is, blood glucose levels higher than those that can be described as hypoglycaemic are associated with irritability. As these relationships are only correlations, it is possible that a third factor might influence both aggression and blood glucose. However, there are reports in both children (Benton et al., 1987) and adults (Benton and Owens, 1993) that the giving of a sugar-containing drink reduced irritable behaviour; data suggesting a causal role for blood glucose values. In summary, the data, although limited, have shown an association between a tendency for blood glucose levels to fall rapidly, irritability or even aggression. In susceptible individuals, it will be of value to consider the effect on mood of the frequency that meals are eaten and the effect of their nutritional composition.

7.4 Serotonin synthesis after the consumption of carbohydrate A frequently quoted suggestion is that the intake of carbohydrate influences the rate at which the amino acid tryptophan is taken up into the brain, with consequences for the synthesis of the neurotransmitter serotonin and hence mood. There have been consistent reports that meals high in carbohydrate as opposed to protein increase the ratio of tryptophan to long-chain neutral amino acids (LNAA) in the blood (Lieberman et al., 1986a; Teff et al., 1989; Christensen and Redig, 1993) with potential consequences for

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serotonin synthesis in the brain. The question is the extent to which these findings have relevance when trying to understand normal food consumption. What does this laboratory observation tell us of our reaction to a typical diet? The rate at which the brain synthesizes serotonin depends on the availability of tryptophan, that is converted to 5-hydroxytryptophan by tryptophan hydroxylase, the rate limiting step. Subsequently, 5-hydroxytryptophan decarboxylase, with pyridoxal phosphate as a co-enzyme, forms 5-hydroxytryptamine, also known as serotonin. Thus, the availability of brain tryptophan, that in turn depends on the rate at which it is taken up by the brain, determines the rate at which serotonin is synthesized. A major theory of the aetiology of depression is that it reflects a low level of brain serotonin. Tryptophan in the blood competes with other LNAA, isoleucine, leucine, methionine, phenylalanine, tyrosine and valine, for transport across the blood–brain barrier. Normally, the proportion of tryptophan to these other LNAAs is relatively low. However, the consumption of carbohydrate and the consequent release of insulin influences the relative proportions of LNAAs. Insulin increases the rate at which most LNAAs are taken up into muscle. In contrast, tryptophan remains in the blood bound to albumin. The result is that the relative proportion of tryptophan in the blood increases and more crosses the blood–brain barrier where it is available for metabolism into serotonin. In contrast, a meal high in protein will decrease the plasma tryptophan ratio as less tryptophan than other competing LNAAs is provided. These phenomena have been demonstrated in many studies. For example, when rats ate a meal of carbohydrate and no protein, the ratio of tryptophan to the other LNAAs in the blood increased (Yokogoshi and Wurtman, 1986). However, the ability to increase the tryptophan/LNAA ratio was blunted by the addition of as little as 2.5 % protein, and either 5 % or 10 % protein failed to increase tryptophan levels. That is, although a meal without protein increased the availability of tryptophan, as little as 5 % protein prevented this phenomenon (Yokogoshi and Wurtman, 1986). Benton and Donohoe (1999) considered 30 human studies that had examined the influence of meals that differed in the energy coming from protein rather than carbohydrate. Although the consumption of exclusive carbohydrate increased the tryptophan/LNAA ratio, when protein provided as little as 5 % of the calories the phenomenon did not to occur. Wurtman et al. (2003) noted that there were few data associated with actual meals so they contrasted the response to two breakfasts. One, based on waffles, offered 80 % of calories as carbohydrate and only 6 % as protein. The other meal was based on turkey, eggs and cheese and provided 52 % of calories as protein and 17 % as carbohydrate. The two meals produced marked differences in the ratio of trypophan to LNAA, a response due more to the high-protein rather than high-carbohydrate meal. After four hours,

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the eating of the high-protein meal decreased the ratio by 35 %, whereas after the high-carbohydrate meal it had increased by a more modest 10 %. If the proposed mechanism was working, then any difference between the meals should not be due to a negative response to a high-protein meal but rather a positive response to a high intake of carbohydrate. Although the authors claimed that these meals were similar to those consumed by Americans, there are reasons to question this statement. The findings reflected to a large extent the response to a high-protein meal, rather than the high-carbohydrate meal that was theoretically predicted to be influential. How often are meals with three different sources of protein consumed without bread, pasta or another source of starch? Arguably, these findings illustrate the improbability of typical meals producing significant differences in tryptophan availability, as the meals were highly prescribed and not typical of normal dietary patterns. In reality, it is rare to consume meals that contain so little protein that the provision of tryptophan will increase. When the proportion of dietary energy provided by protein has been calculated, it has been found to be relatively constantly in the range of 13 +/−2 % of daily calories. The ratio of carbohydrates to protein eaten is similarly fairly constant, typically, there are four or five time the amount of carbohydrate as protein (de Castro et al., 1987; Kim et al., 1987). A diet of this nature will not generally increase the availability of tryptophan to the brain. Most foods that would be described as being high in carbohydrate provide sufficient protein to ensure that tryptophan availability in the blood is not increased. For example, white bread offers 14 % of calories as protein, the figure for potatoes and rice is 7 %, yet the phenomenon described by Wurtman occurs only when a meal is consumed that is almost entirely carbohydrate. Nevertheless, protein must be eaten at some stage as tryptophan is an essential amino acid and hence must be consumed for the mechanism to function. Another problem is that a diet that is exclusively of carbohydrate would be unpalatable and unbalanced. In fact, a chronic lack of protein in the diet would decrease rather than increase levels of tryptophan, as protein consumption is the only source of tryptophan. Ultimately, we need to consider brain serotonin synthesis rather than the amino acid profile of peripheral blood. In animals, after a carbohydraterich/protein-poor meal, enhanced serotonin synthesis occurred only following a meal that was almost entirely carbohydrate (Fernstrom, 1988). In fact, there is some doubt as to whether data from rats can be extrapolated to humans, as in humans changes in plasma tryptophan following high-carbohydrate meals may be less. Ashley et al. (1985) gave a breakfast containing only 1.6 % of the energy as protein and found only a 16 % increase in the tryptophan/LNAA ratio. In rats the ratio between tryptophan and LNAAs needed to at least double if an increase in serotonin synthesis was to be demonstrated (Fernstrom and Wurtman, 1972). Importantly, in humans the consumption of a meal entirely made up of carbohydrate failed to increase the level of tryptophan in cerebral spinal fluid (Teff et al., 1989).

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In conclusion, although there is good evidence that a meal that is almost exclusively carbohydrate will increase the tryptophan/LNAA ratio, there is little reason to believe that this is a mechanism that is relevant other than on rare occasions when food items that are entirely carbohydrate are consumed.

7.4.1 Carbohydrate consumption and depression Wurtman and Wurtman (1989) suggested that one way of addressing depression was to increase the intake of carbohydrate, a view based on those suffering with pre-menstrual syndrome (PMS), seasonal affective disorder (SAD) or carbohydrate-craving obesity. As discussed above, it was proposed that the consumption of carbohydrate increases the level of serotonin in the brain and reduces depression. Pre-menstrual syndrome (PMS) One symptom of PMS is an increased appetite towards the end of the monthly cycle. Sayegh et al., (1995) found that a carbohydrate-rich drink (48 g carbohydrate/no protein) in a double-blind study decreased the depression, anger and confusion of those with PMS. The generality of this response should, however, be questioned as a meal containing no protein would rarely if ever be consumed. Although Christensen (1996) concluded that ‘individuals with PMS increase their carbohydrate consumption in the pre-menstrual stage’, we need to consider whether carbohydrate intake specifically increases or, alternatively if there is a more general increase in food intake? A study of dietary intake found that carbohydrate consumption increased in the pre-menstrual stage (Wurtman et al., 1989). Although these data were used as evidence that carbohydrate intake is greater in those with PMS, there was in fact an increase in both the intake of fat and carbohydrate. As the increased intake was not specifically carbohydrate, it may well have reflected an increased consumption of palatable foods in general, irrespective of the macronutrient composition. When Wurtman et al. (1989) offered high-carbohydrate meals (4 % of energy as protein), the mood of those with PMS improved. However, the levels of protein offered were sufficiently high to question whether the provision of tryptophan would have been increased and, consistent with this view, the amino acid profile in the blood did not change. Importantly, improved mood had been found even though the level of blood tryptophan did not increase. In addition, as most meals contain more than 4 % protein, even if the levels of blood amino acids had differed, the observation would not generalise to the consumption of a more typical meal. Is there evidence that the diets of those with PMS are distinctive? Surveys tend to report that the pre-menstrual stage is associated with cravings for sweet items, particularly chocolate, but there is also a general increase in

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appetite. Vlitos and Davies (1996) found 13 studies that reported an increase in energy intake during the luteal phase that varied from 87 to 674 kilocalories a day. For example, a survey of 384 women found that in 58 % there was an increase in appetite in the pre-menstrual period, in particular a raised liking for sweet foods (Friedman and Jaffe, 1985). The findings are sufficiently consistent for food cravings and changes in food intake to be seen as symptoms of PMS. Does this increased liking for sugary items result in a changed overall profile of macronutrient intake? Does the intake of carbohydrate increase as predicted? An isolated study supported the hypothesis. Dalvit-McPhillips (1983) reported that protein and fat intake was similar in the pre- and postmenstrual stages, whereas the intake of carbohydrate increased from 133 to 257 g. However, when Vlitos and Davies (1996) reviewed the topic, they found seven other studies that did not find a selective increase in carbohydrate intake. The weight of evidence does not support the suggested selective increase in carbohydrate intake in the pre-menstrual stage. There are reports of an increased eating of sweets, cake and chocolate (Davies et al., 1993) and a greater preference for chocolate-containing foods while bleeding (Tomelleri and Grunewald, 1987). As the foods that are craved are pleasant tasting and are high in fat and carbohydrate, there is little support for the hypothesis that the intake of carbohydrate is selectively enhanced. In addition, the amount of protein in chocolate (4–6 % of energy), cakes (4–10 %) and cookies (5–6 %) will ensure that there will not be an increased availability of tryptophan in the blood. Although the suggestion of Wurtman and Wurtman (1989) was that the change in the pattern of food consumption was an attempt to influence mood, there is also substantial evidence of changes in basal metabolic rate over the menstrual cycle (Buffenstein et al., 1995). For example, Webb (1986) found that eight out of ten women showed a rise of between 8 % and 16 % in basal metabolic rate between the first and second halves of the menstrual cycle. Thus, there are parallels between increased pre-menstrual appetite, increased energy intake and increased metabolic rate: the change in food consumption may simply reflect an increased need for energy rather than an attempt to manipulate mood. In summary there is no consistent evidence of a selective increase in carbohydrate consumption in the pre-menstrual stage. There is, however, evidence that appetite, metabolic rate and caloric intake all rise and that the consumption of pleasant tasting foods increases, foods that contain high levels of both fat and carbohydrate. Seasonal affective disorder (SAD) Wurtman and Wurtman (1989) also proposed that a distinguishing feature of those suffering with SAD is a specific hunger for carbohydrate, a desire to decrease depression by increasing serotonin synthesis. Consistent with this view, a survey found that those suffering with SAD in the winter con-

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sumed more carbohydrate-rich foods, such as pasta and rice, although the intake of high-protein foods such as meat and fish did not vary with the seasons (Krauchi and Wirz-Justice, 1988). It should, however, be noted that the high-carbohydrate foods contained enough protein to prevent an increased level of blood tryptophan. Rosenthal et al. (1989), however, found in those with SAD that a carbohydrate-rich protein-poor meal improved mood, although the meal contained high levels of both carbohydrate (105 g) and fat (43 g). As the meal contained only 0.7 g protein (0.4 % of energy), the expected increase in the level of blood tryptophan occurred. It is, however, clear that this was a very unusual meal and the findings cannot be generalised to more normal dietary patterns that include protein consumption. To distinguish the relative contribution of carbohydrate as such from palatability, it would be instructive to offer those suffering with SAD snacks that were equally palatable, although they differed in their carbohydrate content. An obvious hypothesis is that there is differential response to palatability rather than carbohydrate content; that it is the taste rather than carbohydrate content that is important. The mood modifying properties of chocolate are discussed below. Carbohydrate craving depression Wurtman and Wurtman (1989) in addition suggested that there is a sub-set of obese patients whose weight problems are characterised by depression and uncontrolled carbohydrate consumption. Again it was proposed that carbohydrate intake reflected a supposed psychopharmacological action. Lieberman et al., (1986b) distinguished obese individuals who ate almost entirely high-carbohydrate snacks from those who consumed high-fat/highcarbohydrate snacks. Two hours after eating a high-carbohydrate lunch, the mood of the two groups differed. Those who crave carbohydrate felt less depressed and the non-carbohydrate cravers were less alert, more fatigued and sleepy. It is possible to calculate from the data supplied the nutritional composition of the snacks on offer. The five so-called high-carbohydrate snacks provided on average 45 % of the total energy as carbohydrate, 5 % as protein and 50 % as fat. Only one snack contained a level of protein low enough (2.5 % of energy) to even suggest that if eaten exclusively the level of blood tryptophan would have risen. In fact, it is very improbable that a particular snack would have been eaten exclusively and therefore protein from other food items would have limited the provision of tryptophan. In fact, the existence of ‘carbohydrate craving’ obesity has been questioned. Toornvliet et al. (1997) gave three types of snack to ‘carbohydrate craving’ and ‘non-carbohydrate craving’ obese patients. The snacks variously offered energy as 100 % carbohydrate; 70 % carbohydrate, 29 % fat and 1 % protein; 35 % carbohydrate, 3 % fat and 62 % protein. As predicted, the level of tryptophan in the blood was greater after the high-carbohydrate and high-fat/high-carbohydrate meals. Mood was, however, similar after all

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three snacks. The responses of the ‘carbohydrate craving obese’ were similar to others. They concluded that ‘from a therapeutic point of view it was useless to maintain the concept of carbohydrate craving . . . the existence of carbohydrate craving patients has never been established. . . .’ That the only two studies of this topic produced different findings may reflect the methodology. Lieberman et al. (1986b) offered palatable cookies whereas the Dutch study gave liquids of a similar taste and appearance. As the response to food is known to be influenced by its palatability, this may be more important than the actual macronutrient composition. Studies of the influence of macronutrient composition need to control for taste and palatability if they are to establish a role for nutrition.

7.5 Anti-social behaviour and refined carbohydrate consumption Refined carbohydrate intake has been repeatedly related to the hyperactivity of children. In particular, there is a widespread popular belief that sugar induces hyperactivity. In the US simply advertising for parents who believed that sugar consumption causes their child to become hyperactive has on many occasions readily provided an experimental sample. In fact, there are few topics in this area that have been subject to more well-designed doubleblind trials. Following a meta-analysis of these trials, Wolraich et al. (1995) concluded that sugar does not adversely influence the behaviour of children. As an illustrative example, Wolraich et al. (1994) provided the meals for three weeks for families living in their own home. They found that the behaviour of children was similar, irrespective of whether meals were sweetened with either sucrose or artificial sweeteners. There are, however, many in the general population who are so convinced that an adverse reaction to sugar occurs that they have tried to explain away the failure to support their preconceptions. It may be that the adverse response only occurs in a sub-set of children who are sugar reactive; only those with a particular clinical diagnosis might respond; the reaction may occur in those who are younger as there is a tendency for some adverse reactions to food to decline with age. Benton (2008) using meta-analysis considered these types of suggestion but again was unable to find any evidence of an adverse reaction to sugar. Although there is no evidence of a general or even a common adverse response to sugar, there is evidence that on occasions an individual might respond adversely. Benton (2007) used meta-analysis to integrate studies of the impact of food intolerance on hyperactivity and found a significant influence in samples pre-chosen because parents believed their child responded to one food item or another. The response was idiosyncratic and no two children responded in the same way. Of the many dozens of foods to which at least one child reacted, the problems resulted most commonly

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from cows milk, chocolate, grapes and wheat. Although some children respond to sucrose, there were 13 other foods that were more likely to induce a reaction (Egger et al., 1985). In fact, there are reports that a sugar-containing drink can improve the behaviour of children. In the afternoon, Benton and Stevens (2008) gave children, aged 9–11 years, either a glucose-containing drink or a placebo. After the glucose-containing drink, the children’s memories were better and they spent more time on task when working in class. As in childhood the brain uses relatively more glucose than when adult, children may be particularly susceptible to the provision of blood glucose. Compared to the size of the body, children have relatively larger brains than adults. In addition, a given weight of brain tissue from a child uses more glucose than if it came from an adult (Kalhan and Kilic, 1999). From birth to 4 years of age the use of glucose by the brain increases greatly, such that by 4 years of age it uses twice as much glucose as a similar amount of adult brain (Chugani, 1998).This high rate of usage continues until 9–10 years after which it gradually declines to reach adult levels in the late teenage years.

7.5.1

Micronutrient status, anti-social behaviour and refined carbohydrate consumption Typically, parents report that their child responds to sugar within an hour of consumption and therefore the short-term reaction to a single drink is a valid test. Although it has been shown repeatedly that in these circumstances sugar is without effect (Wolraich et al., 1995), such studies do not preclude the possibility that a diet high in sugar might have a longer term influence. One mechanism by which the consumption of refined carbohydrate has been suggested to influence anti-social behaviour is by decreasing micronutrient status. The ‘empty calorie’ hypothesis suggests that the consumption of refined carbohydrates leads to micronutrient deficiencies. There are several well-controlled studies that have found that micronutrient supplementation decreases violence. Schoenthaler et al. (1997) studied anti-social behaviour in imprisoned juveniles. Over three months, the incidence of violence was 28 % less in those who received a multivitamin/mineral supplement rather than placebo. Similarly, Gesch et al. (2002) in a double-blind trial found that the disciplinary record of young offenders improved following supplementation with vitamins/minerals and fatty acids. The greatest reduction occurred in more serious violent offences. It was, however, unclear whether this sample was responding to vitamins, minerals or fatty acids, although it has been suggested that the dose of fatty acids was too low to have been influential. Zaalberg et al. (2010) replicated the finding using young Dutch prisoners who received nutritional supplements containing vitamins, minerals and essential fatty acids and found that the incidence of aggressive and rule-breaking behaviour decreased by 34 %.

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The finding of Schoenthaler and Bier (2000) suggested that these findings might generalise to samples other than those with a criminal history. They considered school-children who had been disciplined at least once over an eight-month period. During a subsequent four-month intervention, those receiving a multivitamin/mineral supplement infringed rules significantly less often than those taking a placebo. Although these findings suggest that a decline in micronutrient status is a possible mechanism by which a high sugar might influence anti-social behaviour, how plausible is it to suggest that such a diet will result in micronutrient deficiencies? Benton (2008) reviewed studies of the relationship between the amount of sugar in the diet and micronutrient status and found that micronutrient intake was more closely associated with total energy rather than sucrose intake. Typically, the amount of sucrose in the diet does not lead to micronutrient deficiency. Gibney et al. (1995) used the rule of thumb that an intake of two thirds of the RDA gives grounds for concern and found ‘that a greater proportion of those consuming low amounts of sugars did not meet at least two-thirds of the RDA for some micronutrients compared with consumers of moderate amounts’. Thus it was a low rather than high intake of sugar that caused potential problems. If a low amount of energy was consumed by those consuming low levels of sugar then micronutrient deficiencies could occur; a reflection of the low energy rather than sucrose intake. As one specific example, Forshee and Storey (2001) considered data from the 1994–1996 USDA Continuing Survey of Food Intakes. They found that children who ate more added sugars consumed more, not less, vitamin C, iron and folate, whereas adolescents consumed more iron and vitamin C. Perhaps the most important conclusion was that any positive or negative associations with sugar intake were ‘always so small as to be of no clinical significance’. To illustrate this point, the greatest negative relationship observed was a negative association between the amount of sugar added to the diet and the intake of fruit. Although this could be portrayed as undesirable, you needed 119 extra teaspoons of sugar to account for the consumption of one less piece of fruit. The associations between sugar intake and micronutrient status were even weaker. The UK Department of Health (1989) considered diets low in energy. They found if you controlled for energy intake, a higher intake of sugar was associated with a lower micronutrient intake. However, those who eat a lot of sugar also tend to eat more in general. Total energy consumption is a better predictor of micronutrient status than the level of sugar and, as those who consume higher levels of sugar generally eat more, they therefore have a higher energy intake.Thus micronutrient intake tends not to be a concern. Logically, with this analysis a group that gives grounds for concern are those with a low energy intake. The UK Department of Health (1989) concluded that ‘in people who eat only small amounts, dietary sugars may compete with other nutrients.’ Simple mathematics suggests that a lowenergy diet that obtains a high percentage of its energy from refined

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carbohydrate may result in sub-optimal deficiencies of micronutrients. However, if such instances occur, the problem is likely to reflect the lowenergy rather than sugar intake. There is a risk that if pleasant tasting sweet food is removed from the diets of those who are only prepared to eat a limited range of food items, the quality of the diet may further decline. To the extent that a pleasant sweet taste can be used to encourage the eating of foods, that would not otherwise be consumed, it could even be part of the solution.

7.6 Chocolate – macronutrients or palatability? In several places it has been suggested that the response to aspects of diet might reflect palatability rather than the macronutrient composition. In various studies referred to above, that considered so-called highcarbohydrate foods, an increased intake of chocolate occurred. Although attention was directed to the macronutrient composition, and in particular the carbohydrate content, should we be focusing solely on macronutrients? The palatability of chocolate needs to be considered as it is uniquely attractive, with an appeal unmatched for many by any other food item. Many will admit readily to craving chocolate (Weingarten and Elston, 1991) and some even claim to be addicted (Hetherington and MacDiarmid, 1993). The example of chocolate will illustrate various points about attempts to simplistically relate changes in mood to macronutrients, rather than looking at the entire experience of eating. In a popular rather than scientific book Waterhouse (1995) stated ‘Chocolate can cause a rush of both serotonin and endorphins into your brain cells . . . it has been called the most effective non-drug anti-depressant . . . the “prozac of plants.” ’ It was claimed that the sugar in chocolate increases the synthesis of serotonin and that the fat in chocolate released endorphins, inducing a sense of wellbeing. The improbability of carbohydrate influencing serotonin synthesis is discussed above. However, as we will see, it may induce the release of endorphins. In addition to macronutrients, chocolate supplies substances such the phenylethylamine, a chemical related to amphetamine, theobromine that acts in a similar manner to caffeine and anandamide, an endogenous cannabinoid neurotransmitter. These have all been suggested to account for the attractiveness of chocolate. Benton (2004), however, argued that chocolate cannot be consumed in amounts sufficient to offer a physiologically active dose of any of these substances. There is good evidence that chocolate, or in fact any highly palatable food, will be consumed when mood is low, you are fatigued or under stress. A desire for chocolate has been reported to be associated with depression (Lester and Bernard, 1991). Benton et al. (1998a) found that those who craved chocolate did so when under emotional stress. A colloquial way of

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describing this phenomenon is that it is ‘comfort eating’. That a low mood causally increases chocolate consumption was demonstrated by Willner et al. (1998) who induced differences of mood by playing either happy or miserable music. After the sad music, subjects were prepared to work harder to receive chocolate. The question arises as to the mechanism by which chocolate enhances mood. Rather than influencing tryptophan levels, it seems plausible that the mechanism involves endorphins, the family of endogenous peptides that act in the brain in a similar way to morphine. In animals, the intake of sweet solutions is increased by an opiate agonist and decreased by an opiate antagonist such as naloxone or naltrexone (Reid, 1985). The consumption of chocolate by rats releases beta-endorphin (Dum et al., 1983). Palatability is important; naloxone decreased the eating of chocolate-chip cookies rather than standard rat food (Giraudo, et al. 1993). The suggestion that opiate mechanisms selectively influence the pleasure associated with palatable food was supported by a study in which human males were given nalmefene, a long-lasting opioid antagonist (Yeomans et al., 1990). Nalmefene did not influence the intake of particular macronutrients, but rather it influenced the intake of palatable foods, for example high-fat cheese such as brie. The choice was between various savoury food items; chocolate and sweet foods were not on offer. In a similar study, naloxone differentially decreased the intake of palatable high-fat/high-sugarcontaining foods (Drewowski et al., 1989). In summary, a major theory is that the eating of palatable foods is associated with the release of endorphins. The blocking of the action of endorphins with drugs such as naloxone or naltrexone selectively decreases the intake of palatable foods. The response is to palatability rather than macronutrient composition. However, the attractiveness of foods reflects many factors other than macronutrient composition.

7.6.1 A psychological or physiological reaction? One study has compared the relative contributions of the psychological and physiological mechanisms that underlie chocolate consumption (Michener and Rozin, 1994). The approach taken was to see which of the various constituents of chocolate satisfies craving. Cocoa butter is the fat that when removed from chocolate liquor leaves cocoa powder. The known pharmacological ingredients are all in the cocoa powder. Therefore, if you eat white chocolate, made from the cocoa butter, you have the fat and sugar intake of chocolate but not the pharmacological constituents. If you consume cocoa powder you take the pharmacological ingredients but not the fat and sugar. In the event, only chocolate satisfied chocolate craving. Capsules containing the possible pharmacological ingredients had a similar effect to taking nothing. The adding of cocoa-containing capsules to white chocolate

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did not increase the less than optimal response to white chocolate. The obvious conclusion was that it was the sensory experience associated with eating chocolate, rather than macronutrient profile or pharmacological constituents, that was important. In conclusion, what seems to be important is that chocolate tastes good. Animals, including humans, prefer foods that are both sweet and high in fat. When we eat something that tastes pleasant endorphin mechanisms in the brain are stimulated. The attractiveness of chocolate reflects its taste and mouth feel; for many, it offers a near optimally pleasant taste that potently stimulates endorphin release. There is also a range of learnt and cultural factors associated with particular foods that influence their desirability.

7.7 Future trends Various themes that would benefit from further study have gained support from this review. Meals high in carbohydrate, with a high glycaemic load, depress mood several hours after consumption. The opportunity arises to develop food items to ‘keep you going’ for longer periods. The approach might be to manipulate the relative amounts of the various macronutrients or to ensure that the carbohydrate used was released slowly into the blood stream. In carrying out such work, it should be remembered that highly palatable foods enhance mood and that any novel food item needs to be palatable if it is to become part of a freely chosen diet. The modification of the pattern of meals and snacks is another approach that could be taken, although any advice to eat ‘little and often’ should not become ‘a lot and often’ with consequences for weight gain. Although snacks have the opportunity to prevent a fall in blood glucose levels, they are often highly palatable and should not offer high levels of fat.

7.8 Sources of further information and advice The topics discussed can be considered in further detail in a series of reviews: • Benton D (2002) Carbohydrate ingestion blood glucose and mood. Neuroscience and Biobehavioral Reviews, 26, 293–308. • Benton D and Nabb S (2003) Carbohydrate memory and mood. Nutrition Reviews, 61, S68–S74. • Benton D (2007) The impact of diet on anti-social behaviour. Neuroscience Biobehavioral Reviews, 31, 752–774. • Benton D (2008) Sucrose and behavioural problems. Critical Reviews in Food Science and Nutrition, 48, 385–401.

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• Benton D (2010) The plausibility of sugar addiction and its role in obesity and eating disorders. Clinical Nutrition, 29, 288–303. Those wanting an overview of glycaemic load should consult the Glycemic Index and GI Database created at the University of Sydney by Jenny Brand-Miller: http://www.glycemicindex.com. As well as an overview of the topic, and good general advice, a comprehensive database of the glycaemic index of a wide variety of foods is provided.

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