Review article
Sugar rush or sugar crash? A meta-analysis of carbohydrate effects on mood

https://doi.org/10.1016/j.neubiorev.2019.03.016 Get rights and content

Highlights

  • Carbohydrates do not have a beneficial effect on any aspect of mood.

  • Carbohydrate consumption lowers alertness within 60 min after consumption.

  • Carbohydrates increase fatigue within 30 min post-consumption.

Abstract

The effect of carbohydrate (CHO) consumption on mood is much debated, with researchers reporting both mood improvements and decrements following CHO ingestion. As global consumption of sugar-sweetened products has sharply increased in recent years, examining the validity of claims of an association between CHOs and mood is of high importance. We conducted a systematic review and meta-analysis to evaluate the relationship between acute CHO ingestion and mood. We examined the time-course of CHO–mood interactions and considered the role of moderator variables potentially affecting the CHO–mood relationship. Analysis of 176 effect sizes (31 studies, 1259 participants) revealed no positive effect of CHOs on any aspect of mood at any time-point following their consumption. However, CHO administration was associated with higher levels of fatigue and less alertness compared with placebo within the first hour post-ingestion. These findings challenge the idea that CHOs can improve mood, and might be used to increase the public's awareness that the ‘sugar rush’ is a myth, inform health policies to decrease sugar consumption, and promote healthier alternatives.

Introduction

Over the last decades, consumption of sugar-sweetened soft drinks has increased dramatically. In the US alone, consumption of such drinks has increased by 135% from the 1970s to the early 2000s (Nielsen and Popkin, 2004). Similar findings have been reported in countries all over the world, including Germany, Spain and the United Kingdom (for a review, see Malik et al., 2010), with annual sales of energy drinks alone surpassing four billion EUR across Europe (490 million liters consumed; see Zucconi et al., 2013). Currently, soft drinks are a major contributor to daily energy intake, accounting for more than 7% of energy consumption and representing the largest single source of calories in people's diets (Block, 2004). The widespread appeal of sugar-sweetened and energy drinks is associated with the marketing of these products as a way of combating fatigue, increasing energy and promoting a euphoric feeling. As the main ingredient in such drinks is sugar, research has focused on understanding how sugar-sweetened drinks, and carbohydrates (CHOs) in general, might promote cognitive facilitation and emotional wellbeing (for reviews, see Benton, 2002, Benton and Donohoe, 1999a, Gibson and Green, 2002, Smith et al., 2011, Sünram-Lea and Owen, 2017).

Several influential studies have suggested that CHO ingestion might have mood-boosting properties. It has been observed that, compared with healthy populations, individuals suffering from affective conditions (e.g., seasonal affective disorder and depression) tend to ‘self-medicate’ by increasing their daily consumption of CHO-rich meals and beverages (Wurtman and Wurtman, 1989, Wurtman and Wurtman, 1995, Wurtman and Wurtman, 2018). On the other hand, recent studies have suggested that, on top of the metabolic health concerns associated with high levels of sugar consumption (e.g., Malik et al., 2006, Vartanian et al., 2007), high long-term consumption of CHOs has adverse effects on psychological wellbeing, even leading to higher rates of depression (Knüppel et al., 2017, Westover and Marangell, 2002). This ongoing debate has renewed the interest of researchers, media and the public in the relationship between sugar and mental wellbeing. As the trend for high consumption of sugary drinks shows no signs of abating, understanding the appeal of these products and the mental and physical health consequences of their consumption is of high priority.

Interestingly, despite researchers not having reached a consensus regarding the exact effects of sugar on mood, it seems that the public strongly believes in the idea that sugar improves mood (‘Why is sugar so addictive?’, 2013) and increases activity levels (especially in children; Furnham, 2018). Although it is difficult to pinpoint the exact pathways that have made the ‘sugar rush’ notion so widely influential in popular culture, the origins of this notion can be traced back to studies suggesting that consumption of CHOs may increase hyperactivity in children (Flora and Polenick, 2013, Rojas and Chan, 2005, Wolraich et al., 1994, Wolraich et al., 1995, Yu et al., 2016). Whereas it is generally accepted that children's ‘sugar rush’ is a myth (for a meta-analysis, see Wolraich et al., 1995), there is less agreement about the effect of sugar on mood. The purpose of the present review is to address the assertion that consumption of CHOs can affect mood. We begin by reviewing the theory behind the supposed neurobiological substrates of CHO–mood interactions, as well as the criticism that this framework has received over the years. We then present the current state of the field by discussing studies supporting and rejecting the claim that CHOs can improve mood, as well as how methodological differences among these studies could help explain these conflicting findings. Finally, we present a meta-analysis where we investigate the relationship between acute CHO administration and mood, while also considering the effect of moderator variables.

The rationale behind the assertion that CHOs improve mood has a strong physiological basis. Consumption of pure CHOs is associated with an increase in neurotransmitter synthesis and uptake in the brain. Specifically, the availability of neurotransmitters such as glutamate, acetylcholine and gamma-aminobutyric acid appears to be modulated by exogenous glucose supply (for a review, see Messier, 2004). For example, in mice, even small doses of glucose have been found to increase acetylcholine synthesis and release in the hippocampus (Durkin et al., 1992) and facilitate cognitive performance (Kopf et al., 2001). Additionally, the effects of glucose on gamma-aminobutyric acid release are also accompanied by alterations in dopaminergic activity (Levin, 2000), further strengthening the assertion that glucose is an important precursor to neurotransmitter synthesis (also see Yeghiayan et al., 2004). The serotoninergic system in particular is susceptible to CHO manipulations, and it has been suggested that the supposed effects on mood are related to fluctuations in serotonin availability following CHO ingestion (for reviews, see Gibson, 2007, Markus, 2008, Spring et al., 1987). It is well-established that serotonin and mood are intrinsically related, with the serotoninergic system being implicated in the etiology of a number of mood disorders, including depression, mania, seasonal affective disorders, anxiety and aggression (for reviews, see Chaouloff et al., 1999, Jenkins et al., 2016, Marek et al., 2003, Sandyk, 1992). Studies manipulating levels of tryptophan (a precursor to serotonin) using tryptophan depletion protocols have found low mood, increased irritability and aggression in human volunteers. However, restoring tryptophan levels has been shown to have antidepressant qualities and can reduce levels of aggression in human volunteers (for reviews, see Jenkins et al., 2016, Young and Leyton, 2002).

It has been observed that both CHO administration and insulin injections in rats are followed by a marked increase in tryptophan (large neutral amino acid; LNAA) in the plasma as well as higher levels of serotonin and tryptophan concentrations in the brain (Fernstrom and Wurtman, 1971, Fernstrom and Wurtman, 1972). Similar findings have been reported in humans, with CHO consumption leading to higher tryptophan availability in the periphery (Fernstrom, 1990, Markus, 2007, Markus et al., 1998, Markus et al., 1999, Rosenthal et al., 1989), accompanied by increased levels of brain tryptophan and a surge in serotonin synthesis (Carpenter et al., 1998, Markus, 2008, Nishizawa et al., 1997, Williams et al., 1999). Whereas protein consumption has been found to decrease tryptophan availability (Fernstrom et al., 2013), ingestion of pure CHOs leads to a higher tryptophan:LNAA ratio, despite CHOs being devoid of tryptophan (Fernstrom and Wurtman, 1971, Markus, 2007). This is because insulin secretion following a meal high in CHOs results in all LNAAs except for tryptophan to be taken up by tissue (e.g., muscle) and, consequently, tryptophan levels remain high compared to other LNAAs (Cangiano et al., 1983; for a review, see Bellisle et al., 1998). As tryptophan competes with other amino acids to cross the blood-brain barrier, such higher tryptophan:LNAA ratio increases tryptophan influx in the brain, resulting in higher brain tryptophan concentrations and increased serotonin synthesis (for reviews, see Gibson, 2007, Markus, 2008, Spring et al., 1987, Wurtman and Wurtman, 2018).

As such, the supposed effects of CHO on mood are posited to be related to the increase in serotoninergic activity following CHO ingestion. It should be noted that this serotonin surge (or, at the very least, the increase in tryptophan availability in the brain) is observed only when CHOs are consumed alone and not when ingested in combination with other macronutrients. Specifically, CHO meals and beverages containing as little as 5% protein do not increase tryptophan concentrations (Yokogoshi and Wurtman, 1986; for a review, see Benton and Donohoe, 1999b). Some studies have failed to observe increases in tryptophan and serotonin availability following CHO ingestion (Teff et al., 1989), suggesting that the CHO–tryptophan relationship could be mediated by other factors, including CHO dose or the presence of protein in the stomach from a previous meal, which can attenuate the effect. Although the real-life applicability of the CHO–serotonin–mood relationship has been challenged because meals typically contain enough protein to suppress a CHO-related increase in tryptophan (for reviews, see Benton, 2002, Benton and Donohoe, 1999a, Benton and Nabb, 2003, Spring et al., 1987), the majority of commercially available soft drinks do not contain any macronutrients other than CHOs. Considering the global increase in the consumption of CHO-rich soft drinks, investigating the extent to which sugar affects mood is an important step in understanding and managing the appeal of these products.

Over the years, evidence has been accumulating in support of the premise that CHOs can improve mood. For instance, Benton and Owens (1993) found that an increase in blood glucose levels after the consumption of 50 g of CHOs is associated with decreased levels of tension (also see Smit et al., 2004). CHO administration has also been related to increased ratings of activation and arousal (Backhouse et al., 2007), higher alertness following a 2-h fast (Owen et al., 2012), higher levels of subjective positive affect (Backhouse et al., 2005, Peacock et al., 2012), lower levels of confusion (Lieberman et al., 2002) and tension (Lieberman et al., 2002, Markus, 2007), higher levels of clear-headedness (Smit et al., 2004), and less fatigue (Markus, 2007, Reay et al., 2006). Furthermore, CHO ingestion has been shown to be related to increased calmness (Spring et al., 1982), particularly following a long period of fasting (i.e., overnight fast; Owen et al., 2012).

The literature on CHO effects on cognition suggests that CHOs can improve cognitive functioning, particularly under circumstances where participants are asked to perform cognitively demanding rather than easy tasks (Mantantzis et al., 2017, Scholey et al., 2009, Sünram-Lea et al., 2002). In a similar manner, studies have found the protective effects of CHOs on mood to be more robust when participants perform demanding physical and cognitive tasks. In fact, whereas participants in control groups experience higher levels of tiredness after performing a cognitively demanding task, consumption of CHOs seems to protect subjective ratings of energy against a potential drop-off after high cognitive exertion (Benton and Owens, 1993, Owens et al., 1997). Additionally, exogenous energy supply in the form of CHOs has been shown to increase vigor and reduce fatigue under conditions of increased physical stress (Ali et al., 2017, Lieberman et al., 2002, Markus, 2007, Welsh et al., 2002) and cognitive demands (Owens et al., 1997, Smit et al., 2004). Therefore, it has been hypothesized that, similar to cognition, mood improvement following CHO administration is stronger when participants have to perform demanding cognitive or physical tasks (for a review, see Benton, 2002).

Furthermore, consumption of CHO-rich foods (i.e., meals with a high CHO-to-other-macronutrients ratio) has been found to have a protective effect against increases in subjective ratings of depression and performance-related declines in vigor, specifically in individuals prone to stress (Markus et al., 1999, Markus et al., 1998). Meals high in CHOs can also decrease levels of fatigue compared with meals high in protein (Lloyd et al., 1996). Additionally, whereas consumption of low-CHO diets over long periods increases depression, tension, anger and fatigue (Deijen et al., 1989), CHO-rich diets can lead to lower hypothalamic–anterior pituitary–adrenocortical axis stress response (Anderson et al., 1987, Blass, 1987, Drewnowski et al., 1992), suggesting that CHOs might have a protective effect against stress and depression (Dallman et al., 2003, Wurtman and Wurtman, 1989, Wurtman and Wurtman, 1995). Similarly, it has been found that self-reported levels of daily CHO intake are negatively associated with depression ratings (de Castro, 1987; for a review, see Soh et al., 2009). Researchers have hypothesized that the relationship between CHO-rich meals, serotonin and mood is so potent that CHO meals are consumed as ‘comfort foods’ by individuals suffering from mood or affective disorders in an effort to improve their mood (for a review, see Wurtman and Wurtman, 2018).

Despite the intuitive appeal of the serotoninergic hypothesis and the literature reporting CHO effects on several mood aspects, there are also studies investigating CHO–mood interactions that have reported conflicting findings. Over the last three decades, an increasing number of empirical reports have suggested that ingestion of CHOs does not lead to any pronounced increases in subjective mood and overall affect, but can even have detrimental effects on mood (Adan and Serra-Grabulosa, 2010, Brody and Wolitzky, 1983, Duckworth et al., 2013, Giles et al., 2012, Harte and Kanarek, 2004, Howard and Marczinski, 2010, Jones et al., 2012, Jones and Sünram-Lea, 2008, Meikle et al., 2004, Miller et al., 2013, Miller et al., 2014, O’Neal et al., 2013, Owen et al., 2013, Qin et al., 2017, Reid and Hammersley, 1995, Reid and Hammersley, 1998, Riby et al., 2004, Scholey et al., 2009, Scholey et al., 2014, Scholey and Fowles, 2002, Scholey and Kennedy, 2004, Seo et al., 2014, Stollery and Christian, 2013, Sünram-Lea et al., 2011, Ullrich et al., 2015, van der Zwaluw et al., 2014, Zacchia et al., 1991). Researchers have acknowledged the complicated nature of the results and have challenged the reliability of CHO effects on mood (Benton, 2002, Boyle et al., 2018, van de Rest et al., 2017). Whereas CHO effects on cognition are strong and well-documented (Messier, 2004, Riby, 2004, Smith et al., 2011), the effects of CHO administration on mood are not as dependable, a finding that could be attributed to a number of factors including the diverse methodologies employed by researchers to assess CHO–mood interactions.

It is evident from the literature that vast methodological differences exist across studies. One of the main factors influencing the reliability of the CHO–mood relationship might be related to the time-course of CHO effects. The serotoninergic mechanism that is supposed to underlie CHO–mood interactions can provide us with a plausible timeframe based on which we can infer the magnitude of the effects of CHOs at different time-points. Considering that a reliable increase in tryptophan availability and serotonin synthesis occurs beyond the first hour post-CHO consumption (Fernstrom and Wurtman, 1971, Markus, 2008, Wurtman et al., 2003), it can be expected that CHO effects would be particularly pronounced around the 1- to 2-h mark. In line with this theory, some studies have reported beneficial effects of CHO on mood 60 minutes post-ingestion (e.g., Ali et al., 2017, Lieberman et al., 2002, Markus, 2007, Reay et al., 2006, Smit et al., 2004). However, mood-boosting effects of CHOs have been observed as early as 15, 30 and 45 min after consumption (Benton and Owens, 1993, Owen et al., 2012, Smit et al., 2004), suggesting that there might be additional, faster-acting mechanisms mediating the CHO–mood relationship other than the influence on the serotoninergic system. In fact, CHO ingestion has been associated with a cascade of physiological effects, including alterations in neural and peripheral metabolism, and increased synthesis of neurotransmitters other than serotonin (Korol and Gold, 1998, Riby, 2004), all of which could be plausibly related to mood enhancement.

Additionally, studies assessing the effects of CHO on cognition and mood have administered a wide variety of CHO types and doses, and have implemented different fasting intervals prior to CHO consumption to investigate the optimal conditions under which CHO effects are most prominent. Although the majority of studies in the area routinely administer glucose (Mantantzis et al., 2017, Mantantzis et al., 2018, Scholey and Fowles, 2002, Sünram-Lea et al., 2001), a number of other reports have opted for sucrose (van der Zwaluw et al., 2014, Zacchia et al., 1991), fructose (Miller et al., 2013), galactose (Duckworth et al., 2013), and isomaltulose (Dye et al., 2010, Young and Benton, 2014). This methodological choice could influence the magnitude of CHO–mood interactions as considerable differences exist in the way that each CHO is metabolized and converted into energy (see Bantle et al., 1983, Rippe and Angelopoulos, 2013). As different CHO types are metabolized in distinct ways and within different timeframes, this should be taken into consideration when examining the potentially time-sensitive relationship between CHO and mood outcomes.

In a similar way, CHO dose is an important factor whose influence has been systematically examined in previous studies (e.g., Sünram-Lea et al., 2011). Although recent work has suggested that CHO dose should be determined based on individual differences in glucoregulatory capacity and the cognitive/behavioral domain being examined (e.g., Owen et al., 2010), results from a meta-analysis suggest that 25 g of CHO is sufficient to observe facilitation effects on cognitive outcomes in both young and older adults (Riby, 2004). Studies on glucose, in particular, have shown that its effects on cognitive indices follow an inverted U-shape dose–response curve, suggesting that below and above a certain threshold glucose either has no effect on behavior or can even lead to cognitive decrements (for a review, see Sünram-Lea and Owen, 2017). Although our knowledge of the moderating effects of CHO dose is limited to cognitive performance indices, it is possible that CHO effects on mood follow similar patterns. However, the selection of CHO doses in published reports is not always justified or adequately explained by researchers.

In addition, studies have used varied fasting intervals prior to CHO administration, ranging from no fasting (Reid and Hammersley, 1998) to 2-h (Giles et al., 2012) and overnight fasting restrictions imposed (e.g., 12 h; Owen et al., 2013, Scholey et al., 2014). However, the moderating effect of fasting duration on CHO effects is not yet clear. In fact, one of the few studies investigating how fasting intervals affect CHO effects on mood has found calmness and alertness to be differentially affected by CHOs under different fasting restrictions (Owen et al., 2012). Specifically, whereas the CHO group's alertness ratings increased following a 2-h fast, higher levels of calmness were found only for the CHO groups that were required to fast overnight. Although a 2-h fast is usually the minimum requirement to observe CHO facilitation effects (for a meta-analysis, see Riby, 2004), a wide variety of fasting regimes is employed across studies measuring CHO effects on behavior and the moderating influence of such methodological decisions is not as yet clear.

The relationship between CHO administration and mood is further complicated by the use of different testing conditions and tasks preceding the evaluation of mood. A range of experimental paradigms have been employed to assess the effects of CHO on behavioral outcomes, with effects on mood assessed after cognitively (Scholey et al., 2009, Scholey et al., 2014) and physically demanding tasks (Ali et al., 2017, Backhouse et al., 2007, O’Neal et al., 2013), stress-inducing procedures (Markus, 2007), and periods of inactivity during which participants are not asked to perform any tasks (Reid and Hammersley, 1995, Reid and Hammersley, 1998). This poses a problem for the investigation of mood effects as activity prior to mood assessment is likely to affect mood ratings. Furthermore, as the facilitation effects of CHOs are suggested to be more reliable in the cognitive domain (for a review, see Boyle et al., 2018), some studies assess mood as a variable of secondary importance, without appropriate justification as to why such measures are included and no a priori hypotheses with regards to expected mood outcomes. More importantly, the focus on cognitive outcomes means that sample sizes are selected based on the number of participants needed to observe CHO-related cognitive facilitation. It has been proposed that the effects of CHOs on mood are relatively small and observable only with large sample sizes (Benton and Owens, 1993; for a review, see Benton, 2002). As a result, studies assessing CHO effects on mood as a secondary outcome may not be adequately powered to identify such effects, potentially increasing the number of false negatives in published reports. A more systematic review of the literature and meta-analytic attempts are urgently needed.

Overall, the research area of CHO–mood interactions is surprisingly complicated, owing to methodological differences identified across empirical reports. Our goal was to investigate the relationship between CHO consumption and mood by using synthesis methods to group and analyze results from all available studies assessing CHO–mood interactions. We set out to examine whether the assertion that CHOs improve mood is robust, or whether this perception is guided by a small number of influential studies reporting a positive relationship. There have been several reviews on the CHO–mood relationship (Benton, 2002, Benton and Donohoe, 1999b, Benton and Nabb, 2003, Boyle et al., 2018, Gibson and Green, 2002, van de Rest et al., 2017) but this is the first attempt at using synthesis methods to deconstruct exactly how CHOs affect mood. The purpose of the present meta-analysis is to analyze all available data to see how different mood constructs are affected by CHOs and how methodological decisions can help us understand the discrepant nature of published findings. It should be noted that the diverse methodological choices of published studies complicate the use of synthesis methods and the grouping of effect sizes from different studies. This does not only relate to the type of CHOs used, the doses, or the timeframe of mood assessment following CHO ingestion, but also to the use of different mood assessment tools to investigate similar mood constructs (for a review of mood tests routinely used in nutritional research, see Polak et al., 2015).

Therefore, we will provide an overview of the methodologies used in studies assessing CHO–mood interactions and aim to systematically disentangle the effect of moderating variables on the CHO–mood relationship. First, if the effects of CHOs are related to fluctuations in serotonin synthesis and availability, we expected that strong CHO–mood interactions would appear beyond the first hour post-CHO ingestion. As the serotoninergic system has been shown to affect depression, anxiety and aggression, we expected the effects to be more reliable for mood constructs related to these specific aspects of emotionality. However, if CHO effects on mood are related to other mechanisms, it is possible that stronger CHO–mood interactions would be obtained at earlier time-points and for different mood constructs (e.g., fatigue and alertness). Investigating the time-sensitivity of CHO–mood interactions will provide us with a better understanding of the time-course of CHO effects: do people experience a temporary ‘sugar high’ following CHO ingestion that fades within the first hour post-CHO consumption (e.g., Benton and Owens, 1993), or are the beneficial effects of CHOs more likely to appear hours after ingestion because of the influence of the serotoninergic system?

Second, if the suggestion that most individual studies are potentially underpowered to detect statistically significant CHO-related mood fluctuations is valid, we would not expect to see strong effects of CHO on mood in the reports included in this meta-analysis. However, the synthesis methods should allow us to examine how even small trends identified in individual studies can potentially be combined to provide a clear picture of how CHOs affect different aspects of mood. Finally, it was expected that the methodological differences between studies would lead to highly variable results as evidenced by high levels of heterogeneity in the meta-analyses.

Section snippets

Search strategy

A comprehensive literature search was conducted to identify empirical articles and original research addressing the CHO–mood relationship in the following databases: MedLine/PubMed, Scopus and Web of Science. Titles, abstracts and keywords were scanned in each database using the following search terms: (carbohydrate* OR glucose OR dextrose OR galactose OR lactose OR sucrose OR fructose OR macronutrient* OR sugar* OR sweet*) AND (supplement* OR consume* OR admin* OR ingest* OR drink* OR eat*)

Results

Of the 5757 studies identified in the literature search stage, 51 met the inclusion criteria and were considered relevant to the present meta-analysis. However, 20 studies had to be excluded at the final stage because of data/information not being available or authors not replying to data requests, leaving 31 studies (N = 1259) available for the meta-analysis (see Fig. 1). Separate meta-analyses are presented for each of the three time windows, as specified in the method section.

Separate forest

Discussion

Although several reviews have been published to investigate the complex relationship between CHO and mood, no research has attempted to systematically deconstruct CHO–mood interactions and assess the influence of moderator variables. In light of studies presenting conflicting findings regarding the effects of CHOs on different aspects of mood at different time-points, the aim of this study was to assess the immediate (0–30 min), short-term (31–60 min), and long-term (61+ min) effects of acute

Conclusions

As the public consumes sugar-sweetened energy drinks to cope with fatigue and negative mood, our goal was to understand whether this pervasive perception holds under scrutiny. Overall, our meta-analysis does not provide support for the supposed CHO–mood relationship and casts doubt on how the neurobiological mechanisms implicated translate into observable mood outcomes. Interestingly, the only evidence uncovered in the present work points to a detrimental effect of CHO on mood constructs such

Role of the funding source

This work was funded by a University of Warwick Postgraduate Scholarship awarded to KM. The sponsor had no involvement in the study design, analysis and interpretation of the data or the decision to submit the article for publication.

Conflicts of interest

None.

Acknowledgements

We thank Vivien Hung, Calum Hartley, Calvin Deans-Browne and Aleksa Cvoro for help in information extraction, and the researchers who have provided us with data.

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    References with an asterisk indicate studies included in the meta-analysis.

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