Abstract
Consensus has yet to be reached on the impact of early sugar introduction on early childhood dental caries (ECC). This study aimed to evaluate the association between the time of introduction of sugar in the infant’s diet and ECC at 48 months, using data from the 2015 Pelotas Birth Cohort Study. This cohort comprises 4,275 children. At 48 months, 3,654 (91.1%) children had their oral health clinically evaluated by a team of 12 trained and calibrated dentists and their dental caries experience and cavitated lesions were assessed. The period of life in which sugar was first introduced into the child’s diet was considered the primary exposure of the study, collected through questionnaires at 3, 12, 24, and 48 months of age. Analyses were conducted using Stata, version 15.0. Descriptive analyses were initially performed. Poisson regression with robust variance adjustment for the crude and adjusted analysis was used to estimate the effect of the sugar introduction on ECC. The highest prevalence of caries experience (43.3%) was in children in which sugar was introduced into the infant’s diet before 12 months of age. A higher prevalence of caries experience was found for less educated (49.8%) and younger (51.7%) mothers, and in poorer families (48.3%). In the adjusted analysis, the experience of caries was 48% greater in the group with sugar introduction before 12 months of age, compared to those where sugar was introduced after 24 months of age In conclusion, our results support the adoption of preventive measures to delay the supply of sugar in early life in order to reduce the caries experience in children.
Introduction
Nutrition plays a fundamental role in all stages of life, especially in the early years, which are decisive for growth and development, the formation of habits, and the maintenance of health [Beluska-Turkan et al., 2019]. The World Health Organization recommends exclusive breastfeeding during the first 6 months of life, and nonexclusive breastfeeding is promoted from 6 months to the first 2 years of the children’s life. After 6 months of age, healthy foods should be introduced into the children’s diet [Brazil Ministry of Health, 2019; WHO, 2015]. The American Heart Association and International Association of Paediatric Dentistry (IAPD) recommend reducing sugar consumption in early childhood and not offering any free sugars to children under 2 years of age [Vos et al., 2017; Pitts et al., 2019]. Besides, the WHO advises intake of free sugars to be less than 10% of total energy intake for children and adults [WHO, 2015]. Even with these recommendations, the prevalence of early sugar consumption is high worldwide, with sugar consumption in the first year of life ranging from 44% to 98% [Wang et al., 2018; Feldens et al., 2020].
Dental caries is one of the most prevalent chronic diseases in early childhood worldwide [WHO, 2019], and it has been demonstrated that a high sugar consumption trajectory leads to the occurrence of caries in early childhood [Echeverria et al., 2022]. Eating patterns characterized by a high frequency of intake of sweetened foods and beverages are associated with a higher incidence of early childhood caries (ECC) [Tinanoff et al., 2019]. Sugar consumption involves psychological aspects by modulating the innate taste for sweets [Chaffee et al., 2015] and the pleasure associated with consuming sugary foods [Panduro et al., 2017]. Early exposure to sweet foods could predict similar dietary patterns in the following stages of life [Fidler Mis et al., 2017; Murray, 2017], which increases the risk for several chronic diseases through the life cycle, including caries [Pitts et al., 2019].
The longitudinal observational design is an excellent option to explore whether sugar introduction at an early age influences the occurrence of caries in ECC. Few longitudinal studies investigated the early introduction of sugar into the diet and the occurrence of dental caries [Thitasomakul et al., 2009; Chaffee et al., 2015; Bernabé et al., 2020]. Brazil is the largest sugar producer in the world, with a very high consumption of sugar per capita [Pinto, 2019], and also presents a high prevalence of dental caries at age 5 [Brazil Ministry of Health, 2012]. Establishing the role of early sugar introduction in early childhood dental caries could help to establish public health policies to prevent or reduce the disease.
There has yet to be a consensus on the impact of early sugar introduction on the caries experience of infants. This study aimed to evaluate the association between the time of introduction of sugar in the infant’s diet and ECC at 48 months, using data from the 2015 Pelotas Birth Cohort Study. The hypothesis of our study is that sugar introduced earlier into the diet will significantly increase the occurrence of caries at 48 months.
Materials and Methods
This study is reported according to the STROBE (STrengthening the Reporting of OBservational studies in Epidemiology) Statement [Von Elm et al., 2007]. This study uses data from the 2015 Pelotas Birth Cohort Study. Pelotas is a medium-sized city in southern Brazil [IBGE, 2021].
Eligible participants comprised all children born alive in hospitals in Pelotas, whose mothers lived in the city’s urban area, in the city’s fishing colony, or the Jardim América suburb of the neighboring city of Capão do Leão/RS during the whole year of 2015. This approach was adopted to allow comparability with previous cohort studies in the city. A research team visited all hospitals in Pelotas daily in 2015, to identify births and invite families to take part in the study. In that year, 5,598 children were born in the city. Four thousand three hundred eighty seven were born to mothers living in the urban area; 54 were stillborn; and the remaining 4,333 constituted the study’s target population. There were 51 refusals and seven births not captured by the study teams. Therefore, the 2015 Birth Cohort comprises 4,275 children (98.7% of the target population). In addition to the baseline, four follow-ups have been performed, at 3 (n = 4,110; 97.2% response rate), 12 (n = 4,018, 95.4%), 24 (n = 4,014; 97.4%), and 48 (n = 4,010; 95.4%) months. Additional information on the 2015 Birth Cohort methodology can be obtained from a previous study [Hallal et al., 2017]. The present study uses data from the 3-, 12-, 24-, and 48-month follow-ups of the 2015 Birth Cohort Study, as described in Figure 1. Data collection was performed at the research center and comprised questionnaires, physical and cognitive development assessments. The variables used in the present study were collected through standardized questionnaires and clinical oral examination.
Questionnaires were applied to mothers or guardians by interviewers trained in the RedCap software [Harris et al., 2009] in each follow-up in the epidemiology center. In all follow-ups, practical training was carried out for the interviewers. The questionnaire was previously tested in a pilot study applied to pregnant women in 2014 who were not eligible for the 2015 Cohort. In addition, key questions were reassessed in a subsample of the study (10%) for quality control through a telephone interview by the study coordinators.
At 48 months, 3,654 (91.1%) children had their oral health clinically evaluated at the Epidemiological Research Center by a team of 12 trained and calibrated dentists. Theoretical-practical training and calibration of the team that performed the exams were carried out. For the practical training and calibration of the examiners, 15 children from a municipal school were repeatedly evaluated by dentists and a gold standard dentist for the following conditions: dental caries in the white spot phase, cavitated lesions, pulp involvement, and occlusion. All children examined were authorized to be part of the study by their parents by signing the informed consent form. The inter-examiner agreement on dental caries measured by the weighted Kappa statistic was 0.91. Regarding ECC, two outcomes were considered: (1) caries experience, including white spot lesions and cavitated lesions and (2) cavitated lesions, assessed by the simplified ICDAS index [Topping and Pitts 2009].
The period of life in which sugar was first introduced into the child’s diet was considered the primary exposure of the study, obtained at each follow-up through the following questions: At the 3-month follow-up, it was measured by asking: “Did the child receive sugar or honey in the last 24 h?” Also, it was asked: “Has the child received chocolate milk in the past 24 h?” The answers were categorized as no and yes. The child was considered as having consumed sugar if the mother/caregiver answered positively to any of the questions. The consumption of sugar during the 12-month follow-up was considered through the mother’s or guardian’s report on the consumption of chocolate milk and soft drinks. It was also asked if the child received any drink from the bottle: “Is this drink sweetened with sugar?” The answers were categorized as no and yes. Sugar consumption was considered if the answer was yes to any of these questions. The consumption of sugar in the 24-month follow-up was considered through the affirmative answer for the consumption of any of the following foods: juice in a box or bottled juice or powdered juice or bottled coconut water or coconut water in a box, soft drink, sweet cookie, candies, lollipops, chewing gums, chocolates, or jelly. The answers were categorized as no and yes. Still, to compose the consumption of sugar at 24 and 48 months, the following questions were considered: “Sugar or honey in drinks such as milk, tea, or juice offered to the child?”; “Chocolate milk?”; “Sugar or honey in fruits?”, also categorized as no and yes.
Based on these questions, the period of introducing sugary foods and beverages to the child’s diet was considered (before 12 months, from 12 to 24 months, or after 24 months). These ranges were chosen based on the recommendation that sugar should not be offered to children until 24 months of age, according to the International Pediatric Dentistry Association [Pitts et al., 2019]. The following sociodemographic variables were considered as possible confounding factors of the association between sugar consumption and dental caries: family income at birth (discrete variable, collected as the sum of all earnings in the last month in Brazilian reais and categorized into income quintiles); maternal education (ordinal variable, collected in the number of years of formal education completed by the child’s birth and categorized as none, from 1 to 3; from 4 to 7; from 8 to 11; 12 and more); maternal age at delivery (discrete variable, collected in years and categorized as less than 20 years; 20–35 years; and over 35 years).
Analyses were conducted using Stata, version 15.0. Descriptive analyses were initially performed using relative and absolute frequencies. Poisson regression with robust variance adjustment for the crude and adjusted analysis was used to estimate the effect of the introduction of sugars on a diet on dental caries. Measures were expressed as prevalence ratio and 95% confidence interval (95% CI).
This study was performed following the Declaration of Helsinki. The research project was submitted and approved by the Ethics and Research Committee of the Faculty of Medicine of the Federal University of Pelotas under protocol No. 717.271/201. All mothers or primary guardians were previously informed about and approved the child’s participation in the study, signing an informed consent form.
Results
Most mothers in the 2015 Birth Cohort had 9–11 years of education (34.1%) and were aged 20–34 years (70.6%). Most children participating in the cohort had the introduction of sugar into the diet before 12 months of age (49.3%) (Table 1). The prevalence of ECC was 37.5% (95% CI: 35.8–39.0), while cavitated lesions were present in 26.0% (95% CI: 24.6–27.5) of the evaluated children.
An association was found between the experience of dental caries at the age of four and maternal education, maternal age, family income, and the age of sugar introduction. The highest prevalence of caries experience (43.3%) and cavitated lesions (30.7%) was observed in children where sugar was introduced before the first year of life. Also, a higher prevalence of caries experience was found in children from less educated mothers (49.8%), from younger mothers (51.7%), and from poorer families (48.3%). The highest prevalence of cavitated lesions was observed in children from poorest families (35.7%), from less educated (39.7%), and younger mothers (38.6%) (as shown in Table 1).
The experience of dental caries was 1.92 times greater in children that had an earlier introduction of sugar (<12 months) compared to those to which sugar was introduced later (>24 months). In the adjusted analysis, the experience of caries was 48% greater in the group with sugar introduction before 12 months of age, compared to that group where sugar was introduced after 24 months of age (Table 2). When sugar introduction occurred between 12 and 24 months, the prevalence of ECC was 1.45 times higher compared to the group in which the introduction was after 24 months. Adjusting for confounders, the prevalence of dental caries experience was 34% higher than the group that received sugar after 24 months of age (shown in Table 2). When considering cavitated lesions, after adjustments, there was no significant difference between the groups with the different times of sugar introduction after adjusting for confounding factors, but there was consistency in relation to the direction of the results. Those children who received sugar between 12 and 24 months had a 29% higher prevalence of cavitated lesions compared to those who consumed only after 24 months. Children who received sugar before 12 months had 38% more cavities compared to the group of children who received sugar after 24 months.
Discussion
The overall finding of our study shows that an early introduction of sugar in the child’s diet resulted in a higher prevalence of caries in early childhood – the earlier the introduction of sugar, the greater the risk of caries development. A few longitudinal studies have evaluated this relationship in different populations, showing similar results. A prospective study in Scotland showed that introducing sugar-sweetened beverages during the first year of life would result in children having a trajectory of high levels of dental caries [Bernabé et al., 2020]. The introduction of a more significant number of cariogenic items before 6 months of age was positively associated with severe caries in early childhood in Brazil (S-ECC) [Chaffee et al., 2015]. Furthermore, sugar consumption at 5 months in Thailand was associated with an increased incidence of ECC [Thitasomakul et al., 2009]. Therefore, in addition to the high sugar consumption trajectory being associated with a higher incidence of ECC [Echeverria et al., 2022], the early introduction of sugar in the diet is also associated with the occurrence of caries in this age-group. It is important to point out that we evaluated the occurrence of dental caries at age 4. The World Health Organization (WHO) recommends age 5 as the age index to evaluate the occurrence of dental caries in primary teeth. However, since we were working in a cohort study, there are several aspects determining when follow-ups are carried out, such as the different health outcomes considered and funding availability. Possibly, a caries examination at age 5, with the longer time for lesions to progress to cavitation, would have resulted in a stronger relationship between early sugar introduction and cavitated lesions. This is an assumption that remains to be tested and we cannot forget that not all the early caries lesions will progress into cavitated lesions.
Given the many harms of sugar consumption in early childhood, interventions are needed to delay the introduction of sugar into infant feeding. Taxation of sugar-containing products has been advocated as one of the ways to reduce chronic diseases, including tooth decay [Jevdjevic et al., 2019]. There is evidence that sugary beverage taxes (sugar-sweetened beverage) can efficiently mitigate sugar consumption [Hagenaars et al., 2021]. A systematic review provides evidence on the effect of taxing foods exceeding a specific sugar threshold value on consuming sugar-added foods. After implementing the Hungarian public health product tax, the mean consumption of taxed sugar-added foods decreased by 4.0% [Pfinder, 2020]. In this sense, delaying sugar introduction and decreasing its intake may decrease dental caries and prevent other diseases. Oral health professionals should help identify and address sugar-related behaviors in pediatric patients and advocate for broader approaches, including taxes, warning labels, and policies to reduce added sugar intake, prevent cavities, and improve health outcomes in children [Chi and Scott 2019]. In addition, recommendations to parents and caregivers about avoiding early introduction to sugar are of paramount importance for controlling dental caries.
Some study limitations must be acknowledged. The magnitude of the association between early sugar introduction and ECC may have been underestimated due to the need for a standardized instrument to measure diet. However, this is a limitation of studies on this particular subject. Another limitation is that the outcome may have been overestimated due to using initial caries lesions through epidemiological examination. This study also had several strengths, such as the use of a population-based birth data with low losses and refusals, robust methodology, oral health examinations performed by trained and calibrated dentists, and adequate adjustment for possible confounding. We explore this association through a large sample of children with various measurement points of the infant diet, including sugary drinks and sweet foods.
An association between the age of introduction to sugar and the experience of dental caries at 48 months was identified. The highest prevalence of ECC (43.3%) was in children in which sugar was introduced into the infant’s diet before 12 months of age. Our results reinforce the need to adopt preventive measures to delay the supply of sugar in early life, such as taxing products containing sugar, government incentives for the purchase of fruits and vegetables, and promoting preventive guidelines during prenatal, immediate postnatal, and in the first 2 years of life by health professionals. More studies on the effect of these interventions should be carried out.
Statement of Ethics
This study was performed following the Declaration of Helsinki. The research project was submitted and approved by the Ethics and Research Committee of the Faculty of Medicine of the Federal University of Pelotas under protocol No. 717.271/201. All mothers or primary guardians were previously informed about and approved the child’s participation in the study, signing an informed consent form.
Conflict of Interest Statement
The authors have no conflicts of interest to declare.
Funding Sources
The 2015 Birth Cohort Study was conducted by the Graduate Program in Epidemiology (PPGEpi) at UFPel with the support of the Brazilian Association of Collective Health (ABRASCO). The 2015 Pelotas Cohort was funded by the Wellcome Trust (095582). Funding was also received for specific segments of the National Council for Scientific and Technological Development (CNPq) and the Foundation for Research Support of the State of Rio Grande do Sul (FAPERGS). The follow-up at 24 months of self-financing by Pastoral da Criança; the 48-month follow-up after receiving funding from FAPERGS – PPSUS, Wellcome Trust (10735_Z_18_Z), and Bernard van Leer Foundation (BRA-2018-178). The monitoring of oral health at 48 months in the 2015 Cohort was financed by the Notice FAPERGS/CNPQ PRONEX 12/2014 (16.0471-4), and the CNPQ Universal Notice (454796/2014-5 and 426230/2018-3) granted to the Researcher Main (FFD). This study was partly funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível SuperiordBrasil (CAPES), Finance Code 001.
Author Contributions
M.S. Echeverria contributed to conception, design, data acquisition, and interpretation, performed all statistical analyses, and drafted and critically revised the manuscript; H.S. Schuch contributed to conception and design, performed all statistical analyses, and drafted and critically revised the manuscript; M.S. Cenci contributed to conception and design and critically revised the manuscript; J.V.S. Motta contributed to conception and design and critically revised the manuscript; A.D. Bertoldi, M.B. Correa, and M.-C.D.N.J.M. Huysmans critically revised the manuscript; and F.-F. Demarco contributed to conception, design, data acquisition, and funding obtaining and critically revised the manuscript.
Data Availability Statement
The original data are not publicly available due to legal grounds, but they can be assessed from the corresponding author at a reasonable request. Further inquiries can be directed to the corresponding author.