The negative impact of sugar-sweetened beverages on children’s health: an update of the literature

While sugar sweetened beverage (SSB) consumption has declined in the last 15 years, consumption of SSBs is still high among children and adolescents. This research synthesis updates a prior review on this topic and examines the evidence regarding the various health impacts of SSBs on children’s health (overweight/obesity, insulin resistance, dental caries, and caffeine-related effects). We searched PubMed, CAB Abstracts and PAIS International to identify cross-sectional, longitudinal and intervention studies examining the health impacts of SSBs in children published after January 1, 2007. We also searched reference lists of relevant articles. Overall, most studies found consistent evidence for the negative impact of SSBs on children’s health, with the strongest support for overweight/obesity risk and dental caries, and emerging evidence for insulin resistance and caffeine-related effects. The majority of evidence was cross-sectional highlighting the need for more longitudinal and intervention studies to address this research question. There is substantial evidence that SSBs increase the risk of overweight/obesity and dental caries and developing evidence for the negative impact of SSBs on insulin resistance and caffeine-related effects. The vast majority of literature supports the idea that a reduction in SSB consumption would improve children’s health. Electronic supplementary material The online version of this article (10.1186/s40608-017-0178-9) contains supplementary material, which is available to authorized users.


Background
Sugar sweetened beverages (SSB)which include drinks with added sugar such as soda, fruit drinks and energy drinksare frequently consumed by children and adolescents in the United States (U.S.) [1]. There is evidence that consumption of SSBs has recently begun to decline in the U.S., with this decrease largely driven by fewer children consuming these beverages [2,3]. From 2003 to 2014, the percentage of children in the U.S. consuming at least one sugar-sweetened beverage on a typical day declined significantly from 80% to 61% [3]. Much of this decline was driven by a decrease in the percentage of young children ages 2 to 5 consuming SSBs, although the decline was significant for all age groups. Over the same period, consumption from caloric beverages (SSBs, milk and 100% juice) declined from 463 to 296 daily calories, and the fraction of all beverage calories from SSBs decreased from 49% to 45% [3]. Within SSBs, the number of calories from soda and fruit drinks consumed per day declined from 116 kcal to 49 kcal and 70 kcal to 31 kcal, respectively [3]. Despite these important declines, consumption of SSBs by children and adolescents in the U.S. still remains high. In 2013-2014, 46.5% of children aged [2][3][4][5]63.5% of children aged 6-11 and 65.4% of adolescents aged [12][13][14][15][16][17][18][19] reported consuming at least one SSB on a given day [3]. Additionally, high levels of SSB consumption persist among low-income and racial and ethnic minorities.
In light of the frequent consumption of SSBs among children and adolescents in the U.S., there has been an interest in critically examining associated health consequences. As a result, there has been a substantial rise in the number of studies investigating the health effects of SSBs over the past decade. Evidence has emerged linking SSB consumption to a number of health consequences among adults including weight gain [4,5], cardiovascular risk factors (e.g., dyslipidemia) [6], insulin resistance and type 2 diabetes [7,8] and non-alcoholic fatty liver disease [9]. Studies among children are more limited and have generally focused on weight gain [4] and dental caries [10], as well as insulin resistance to a lesser extent [11,12]. An emerging body of research has also examined the association between caffeinated SSBs (e.g., energy drinks or colas) and caffeine-related health consequences including reduced sleep quality and headaches [13]. Given the growing number of studies assessing SSBrelated health consequences, concise summaries of the evidence base are needed in order to inform policy and advocacy efforts focused on reducing SSB consumption.
This review aims to synthesize the existing evidence regarding the impact of SSB consumption on children's health. Unlike previous reviews which have been limited in scope (e.g., focusing on a single outcome such as weight gain) [14,15], this review summarizes evidence from cross-sectional, longitudinal and intervention studies on a broad range of health outcomes relevant to children including: obesity, insulin resistance, dental caries, and caffeine-related effects. A previous review published in 2009 summarized many early studies on SSBs and children's health [16]. Using a narrative review approach, we update the literature by reviewing more recent studies published up until 2017.

Search selection
For each of the health impacts (obesity, insulin resistance, dental caries and caffeine-related effects), separate searches were conducted of PubMed, Web of Science and PAIS International. For all searches, a search hedge was created in three parts: 1) terms relevant to SSBs including "beverage" and "sodas", 2) terms restricting to children and adolescents including "pediatric" and "teens" and 3) terms specific to the outcome being examined such as "body mass index" and "body weight" for the search on overweight and obesity risk (see Additional file 1: Appendix for full list of search terms). These search terms were chosen to retrieve the most relevant results using an iterative process in consultation with a medical librarian. For searches of PubMed, MeSH subject headings were used. In addition to database searches, reference lists of SSB reviews and articles were searched. Following the removal of duplicate studies, one author (K.V.) screened titles, abstracts and full-texts and another author (S.B.) confirmed the inclusion of these studies. Included studies had to be peer-reviewed articles examining the effects of SSBs on a specific health outcome, be limited to children and adolescents, and be published after January 1, 2007. We selected 2007 as the start date because the most recent relevant review [16] included studies published prior to this. Studies were excluded if they were not published in English, were not conducted in high-income countries (defined as membership in Organisation for Economic Co-operation and Development) or were grey literature. We limited our scope to high-income countries to promote generalizability of results.

Cross sectional studies
Most cross-sectional studies found significant positive associations between SSB intake and obesity risk among children and adolescents [17-19, 21-25, 27, 29-32, 34, 35, 55]. For example, among 12 to 19 year olds in the 1999-2004 National Health and Nutritional Examination Survey (NHANES), each additional SSB serving (250 g) consumed per day was associated with a 0.93percentile increase in Body Mass Index (BMI) z-score [34]. These positive findings were well-replicated across a range of OECD countries, including Canada, Spain, Greece and in Australia where those who consumed more than one SSB servings (≥250 g) per day were 26% more likely to be overweight or obese compared to those who consumed less than one serving per day [27]. They are also consistent with results focused on specific subgroups such as among Mexican-American children aged 8-10 years where each additional SSB serving (240 mL) per week was associated with a 1.29 greater odds of obesity [17] and among toddlers living in low-income families where no SSB intake was associated with a 31% lower obesity prevalence compared to households where toddlers consumed two or more SSB servings (serving = 12 fluid ounces) per day [23]. Some of the cross-sectional studies found positive associations only within subsets of the sample [18,19,21,29,32,35,55], including: boys [32,35], boys aged 6 to 11 [21], children aged 9 to 11 [29], and among Mexican-American and non-Hispanic White adolescents only [18].
A small number of cross-sectional studies reported null findings [20,26,33], and one study conducted in Korea among 9 to 14 year olds reported an inverse association among males [28].

Longitudinal studies
Like the cross-sectional data, longitudinal studies generally demonstrated that increased SSB consumption was associated with weight-related outcomes among children and adolescents [38, 39, 47-49, 51, 53, 56]. For example, among a nationally representative survey of 2 to 5 year olds in the U.S., children who consumed more than one Note: *indicates statistical significance (p<0.05) as reported by each study SSB serving (serving = 8 fluid ounces) per day at 2 years old had a significantly greater increase in BMI z-score over the next 2 years compared to infrequent/non SSB drinkers [38]. Two of the positive studies examined longitudinal associations between SSB consumption and obesity risk among minority populations, with one finding that high SSB intake (defined as greater than median intake in study population) among Latino toddlers was associated with a 0.46 unit increase in weight for height z-score at 6-month follow-up [37] and the other finding that SSBs were positively associated with 2-year overweight risk among African-American preschool children [47]. Some studies found mixed results [36-38, 40, 44, 45, 52], with two reporting the positive association between SSB intake and increased weight was only significant among girls [36,45]. The first study found high SSB intake (≥15 servings/week) at 13 months old was significantly associated with an increased BMI among girls at ages 2, 3, 4, and 6 years old [45]. Another study found that girls who moved to the top tertile of SSB consumption (>335 g/day) between 14 and 17 years of age had increased BMI and nearly a five-fold greater odds of overweight or obesity risk compared to girls who remained in the lowest tertile of SSB consumption [36]. One study found a positive association when using SSB consumption at 15 years to predict change in BMI from ages 15-21 and found null results when using SSB consumption at 9 years as a predictor [52].
Intervention studies A small number of intervention studies have examined SSB consumption and overweight and obesity risk among children [58][59][60]. Three recent randomized controlled trials found a reduction in BMI or obesity risk in the intervention group compared to the control. De Ruyter and colleagues conducted a double-blinded placebo-controlled trial wherein 641 normal weight Dutch children were randomized to receive either a 250 mL of an SSB or a sugar-free beverage each day for 18 months [58]. At the end of the trial, the difference in BMI z-score was significantly different between the two groups, with the SSB group increasing on average by 0.15 units (compared to 0.02 units in the sugar-free group). The second study randomized 224 overweight and obese American adolescents who regularly consumed SSBs to either participate in a program to reduce SSB consumption or receive no intervention [59]. At the end of the 1-year intervention, those in the intervention group had beneficial changes in BMI and weight compared to those who did not receive the intervention, but these differences were no longer significant when participants were followed-up for an additional year after the end of the intervention. However, in a pre-planned subgroup analysis of Hispanic participants, there were significant differences in BMI between groups at both follow-up periods. The third study was a cluster randomized trial in which schools in the United Kingdom were randomized to either an intervention discouraging consumption of SSBs or no intervention for one year [61]. A significant difference in BMI z-score and overweight/obesity risk between groups was observed at the end of the first year, supporting a positive association between SSBs and obesity risk [61]. Two years after the intervention had been discontinued, the researchers completed a follow-up assessment and reported the differences between the groups were no longer significant [60].

Insulin resistance
A modest number of studies reported a positive association between SSB consumption and insulin resistance risk among children and adolescents, with the majority conducted cross-sectionally [62][63][64][65], one conducted longitudinally [66] and no intervention studies conducted ( Table 2).

Cross sectional studies
A number of cross-sectional studies found a positive association in the whole or a subset of their study population [62][63][64][65]. For example, among 12-19 year olds in NHANES, each additional SSB serving (250 g) consumed per day was associated with a 5% increase in HOMA-IR (a marker of insulin resistance which is calculated using fasting glucose and insulin levels) [55]. One study reported associations by race, with positive associations found among White and African Americans, but null associations among Mexican Americans [18]. Another study reported a stronger association between SSB consumption and higher HOMA-IR among overweight/obese participants compared to normal weight participants [64].

Longitudinal studies
Only one longitudinal study was conducted to examine this association, reporting that an additional 10 g/day of added sugar from liquid sources was associated with a 0.04 mmol/L higher fasting glucose, 2.3 pmol/L higher fasting insulin and a 0.01 unit increase in HOMA-IR over two year follow-up [66].

Cross sectional studies
The vast majority of cross-sectional studies found evidence for a positive association between SSB consumption and dental caries [67,[69][70][71][72][73][74][75][76][77][78][79][80][81][82]. For example, one study reported that the prevalence of caries was 22% higher for each additional SSB serving consumed by children per day [81]. Several studies replicated this positive association among low-income children [70,73,75], with one study reporting that high SSB consumption (≥5 oz/day) was associated with a 4.6 greater odds of dental caries compared to those with lower SSB consumption [70]. Some studies examined how specific timing of SSB consumption affects dental caries, with one study [72] finding an association with dental caries and SSBs consumed at bedtime and another [69] finding an association with dental caries and SSBs consumed at nighttime among 3 year-olds and for SSBs consumed between meals among 5-year olds. One cross-sectional study reported null results, finding no association between self-reported SSB consumption and dental caries among Alaska Natives a result which may have been related to the small sample size (N = 51) [68].

Longitudinal studies
All longitudinal studies included in this review found a positive or mixed association between SSB consumption and dental caries in at least part of the study population [83][84][85][86][87][88]. One study reported that a high consumption of SSBs (≥3 servings per week) among infants 10 to 12 months old was associated with a 1.83 greater odds of dental caries at age 6, compared with infants who did not consume SSBs during infancy [84]. Some studies reported these positive findings among specific subgroups including: low-income [86], African American [83] and American Indian children [85]. For example, Lim et al. conducted a cluster analysis and reported that African American children who changed from being low consumers of SSBs at baseline (mean consumption = 567.4 mL/day) to high consumers of SSBs at 2-year follow-up (mean consumption = 1032.4 mL/day) had a 1.75 times higher mean number of new dental caries compared with high consumers of milk-juice at both baseline and 2-year follow-up [83].

Intervention studies
Only one intervention study has been conducted to assess SSB consumption and dental caries [89]. Maupomé et al. conducted community-wide interventions to reduce SSB consumption, improve breastfeeding practices, and promote consumption of water for thirst among American Indian toddlers. While the intervention communities demonstrated improvements in the number of dental caries, it is not possible to attribute this specifically to reduction in SSB consumption as the intervention was a multi-pronged approach.

Caffeine-related effects
A growing number of studies reported on the caffeine-related effects associated with SSB consumption with studies almost exclusively cross-sectional (Table 4).

Cross sectional studies
A number of cross-sectional studies examined the effects of energy drink consumption among children and adolescents [90][91][92][93][94][95][96][97], with each study often reporting on multiple outcomes. Some studies found evidence for an association between energy drink consumption and sleep-related issues such as sleep dissatisfaction, tiredness/fatigue and late bedtime [92,93,95], and others reported an association between energy drink intake and increased headaches [91][92][93]. One study reported an association between energy drink consumption and risktaking behaviors such as cigarette, marijuana and drug use [90], and two studies found an association between energy drink consumption and stress, depressive symptoms, and suicidal ideation, plan or attempt [90,95]. Other outcomes examined in these cross-sectional studies reported include irritation [92], stomach ache and low appetite [93]. Some of the cross-sectional studies examined caffeinerelated effects of cola drinks [93,96,97]. One found that both low and high consumption of cola were associated with lower stress and found null associations with anxiety and depression [96]. Another examined both cola and energy drinks and found that higher consumption of both beverages was associated with headaches, stomach-aches, sleeping problems and low appetite [93]. More specifically, among males, drinking more than one cola per day was associated with a 1.34 greater odds of sleeping problems and among females drinking more than one cola per day was associated with a 1.55 greater odds of sleeping problems.

Longitudinal studies
One longitudinal study was conducted and it found evidence that increased energy drink consumption was associated with attention deficit/hyperactivity disorder inattention and hyperactivity at 16-month follow-up, but did not find evidence for associations with depression, panic and anxiety [94].      1 Many more studies are now conducted exclusively on children and adolescents, while previous evidence was based on results found among adults. While the majority of this research is still cross-sectional (limiting the ability to make inferences about causality), the past decade has seen a growing number of longitudinal studies being implemented, as well as an increasing amount of intervention trials. The majority of this research on SSBs over the past decade has centered on the relationship with weight gain. The findings of this review confirm that there is clear and consistent evidence that the consumption of SSBs heightens obesity risk among children and adolescents. Although a formal quality assessment or strength of evidence evaluation was not conducted, the vast majority of cross-sectional, longitudinal and intervention studies find strong evidence for a positive relationship in all or part of their study population. The exact mechanism through which SSBs impact childhood obesity is not entirely understood. Generally, the research points to the low satiety of SSBs and incomplete compensation [98,99]. In other words, drinking calories in liquid form does not decrease hunger in the same way as solid food. Additionally, people do not sufficiently reduce their total energy intake to make up for the excess calories obtained from SSBs. There is also a lively debate about whether the effect of calories from SSBs on body weight is worse than some other foods or nutrients [100,101].
The association between SSB consumption and weight gain is paramount, given that childhood obesity affects roughly one in six (13 million) children in the U.S., disproportionately impacting children who are low-income and racial and ethnic minorities [102]. From 1976 to 2016, the prevalence of childhood obesity in the U.S. more than doubled in children ages 2 to 5 (from 5% to 13.9%), nearly tripled in children aged 6 to 11 (from 6.5% to 18.4%) and quadrupled in adolescents' ages 12 to 19 (from 5% to 20.6%) [103][104][105]. While there is some indication that childhood obesity rates may leveling in the U.S. [104], the overall prevalence of obesity among children in 2016-2016 was estimated at 18.5% [105], meaning it is still considerably higher than the Healthy People 2020 goal of 14.5% [4]. Given that children who are overweight and obese youth are likely to remain so as adults [106], obesity and its adverse health consequences create a serious threat to children's current and future health [107]. Hence, reducing SSB consumption is an important intervention point to reduce the burden of childhood obesity in the U.S. This review also finds strong and consistent evidence that consumption of SSBs is associated with dental caries among children and adolescents. The mechanism for the association between SSB consumption and dental caries is well understood: dental caries are caused by acids produced by bacteria metabolizing sugar in the mouth. Increased sugar from SSBs intensifies the acid production and causes further decay of teeth [108]. The majority of studies examining this relationship are cross-sectional, but a modest number of longitudinal studies as well as one intervention study also support the association.
While evidence has shown a positive relationship between SSB consumption and type 2 diabetes among adults [5,12,109], the available literature among child and adolescents is limited. The majority of studies among children and adolescents do not directly examine the link between SSB consumption and type 2 diabetes and instead measure insulin resistance, a biomarker of increased cardio-metabolic risk and type 2 diabetes. It is hypothesized that the high content of sucrose and highfructose corn syrup present in SSBs may increase dietary glycemic load leading to insulin resistance and inflammation [7]. While not as strong and consistent as the relationships between SSB consumption and weight gain or dental caries, most studies in this review generally support an association between SSB consumption and insulin resistance among children and adolescents. However, this is limited by a small number of studies and the predominance of a cross-sectional study design.
The findings of this review also point to an association between caffeinated SSBs and a wide range of health issues including poor quality or reduced sleep, headaches, risk-seeking behavior and depressive symptoms. The presence of caffeine in energy drinks and other caffeinated SSBs (e.g., cola), in conjunction with the large volumes consumed, can lead to neurological and psychological effects associated with high caffeine consumption. The majority of studies examining the caffeine-related effects of SSBs focus on energy drinks, with very few analyzing the effects of other caffeinated SSBs such as colas. One reason for this may be the considerably higher level of caffeine content in energy drinks: a 250 mL energy drink has an average of 80 mg of caffeine (range: 27-87 mg), compared to 40 g of caffeine (range: 30-60 mg) in a 330 mL cola drink [110]. Additionally, studies examining caffeinerelated effects have almost exclusively been crosssectional, limiting the strength of inferences that can be made and bringing forth issues of reverse causation.
While there is a large and growing body of research examining the impact of SSBs on children's health, important gaps remain. First, researchers should utilize more rigorous study designs (intervention trials and longitudinal studies) and move away from a reliance on cross-sectional studies. This will strengthen the evidence base and allow firmer conclusions to be made regarding the causal relationships between SSB consumption and negative health consequences. Second, more consistency is needed in the definition of SSBs (e.g., specifying which beverages are included and what is a typical serving size) and measurement strategy (e.g., FFQ vs. 24-h recall). Similarly, more uniformity is needed in assessing outcomes, particularly in the risk of overweight/obesity where studies vary considerably in the outcomes measured (e.g., BMI, BMI z-score, BMI percentile, overweight/obese status). Third, researchers should more rigorously examine differences in health risks by subpopulations (e.g., race/ethnicity, socioeconomic status, age and gender) to determine if the intake of SSBs in particularly harmful in certain population subsets. While it is established that lowincome and racial and ethnic minorities consume more SSBs, it is unclear the extent to which health consequences are magnified among these groups. This is important particularly for targeting interventions and policy approaches to reduce children's SSB consumption. Better insights in these areas have the potential to inform realworld policies and recommendations that may greatly benefit children's health. Finally, additional research is needed about caffeinated SSBs and their impact on children's health. Energy and sport drink consumption is rising rapidly in the U.S. [13] and so studies examining the negative health effects of caffeinated SSBs are needed to inform future efforts to reduce consumption. This review has several limitations. First, it only focuses on four main health effects associated with SSB consumption and does not address other potential consequences which have been documented among consumers of SSBs (e.g., hyperlipidemia, non-alcoholic fatty liver disease). Second, our conclusions for a particular health consequence did not include a quality assessment and was limited to an informal evaluation of consistency and lack of conflicting studies. Third, article screening was not done in duplicate, although all included articles were confirmed by a second reviewer.

Conclusion
This review provides clear and consistent evidence that consumption of SSBs increases obesity risk and dental caries among children and adolescents, with emerging evidence supporting an association with insulin resistance and caffeine-related effects. In general, the strength of evidence for all four health consequences could be improved through the implementation of more longitudinal and intervention studies. Additionally, more consistency is needed from studies in the measurement of exposures (e.g., standardized measurement and definition of SSBs) and outcomes (e.g., assessment of weight-related outcomes) to create a stronger evidence base. Future research should compare low-income and racial/ethnic minority subgroups in order to determine if differences in health risks associated with SSBs exist. Although SSB consumption has declined in the last 15 years, consumption still remains high (61% of children consume at least one SSB per day). The vast majority of the available literature suggests that reducing SSB consumption would improve children's health.