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Article

Sugar-Sweetened Beverages and Allergy Traits at Second Year of Life: BRISA Cohort Study

by
Alessandra Karla Oliveira Amorim Muniz
1,
Elcio Oliveira Vianna
2,
Luana Lopes Padilha
1,
Joelma Ximenes Prado Teixeira Nascimento
1,
Rosangela Fernandes Lucena Batista
1,
Marco Antonio Barbieri
2,
Heloisa Bettiol
2 and
Cecilia Claudia Costa Ribeiro
1,*
1
Postgraduate Program in Public Health, Department of Public Health, Federal University of Maranhão—UFMA, Sao Luis 65020-060, Maranhao, Brazil
2
Ribeirão Preto Medical School, University of São Paulo—USP, Ribeirao Preto 14049-900, Sao Paulo, Brazil
*
Author to whom correspondence should be addressed.
Nutrients 2023, 15(14), 3218; https://doi.org/10.3390/nu15143218
Submission received: 2 June 2023 / Revised: 16 July 2023 / Accepted: 16 July 2023 / Published: 20 July 2023
(This article belongs to the Section Carbohydrates)

Abstract

:
Sugar-Sweetened Beverage (SSBs) consumption has risen in early life and it is plausible that it might increase children’s risk of allergies. In this paper, we analyzed the association of SSB consumption with allergies in children’s second year of life. This study analyzed data from a São Luís BRISA prenatal cohort in the follow-up of children (n = 1144) in their second year of life. Allergy Traits were a latent variable deduced from medical diagnoses of allergic rhinitis, atopic dermatitis, and food allergies. SSBs were investigated as a percentage of daily calories based on 24 h recalls, including industrialized fruit juices, soft drinks, and ready-made chocolate milk. Other variables analyzed were socioeconomic status, age, body mass index z-score, episodes of diarrhea, and breastfeeding. Our finds were that higher consumption of daily calories from SSBs was associated with higher Allergy Trait values (SC = 0.174; p = 0.025); older age (SC = −0.181; p = 0.030) was associated with lower Allergy Trait values; and episodes of diarrhea were correlated with Allergy Traits (SC = 0.287; p = 0.015). SSB exposure was associated with Allergy Traits in children’s second year of life; thus, abstaining from these beverages may also confer additional advantages in curtailing allergic diseases during early childhood.

1. Introduction

Sugar-sweetened beverages (SSBs) are the primary source of free sugars in individuals’ diets, significantly contributing to the energy density of the Western diet [1]. These beverages are those processed with added sugars, especially sucrose or high fructose corn syrup, and are represented by soft drinks, fruit flavored drinks, sweetened teas and coffees, energy drinks, and sweetened milks [2].
SSBs have been associated with epidemics of non-communicable diseases such as obesity, diabetes, and cardiovascular diseases [3]. Renowned international institutions have suggested limiting sugar intake to 5% of daily calories [4], 25 g/day for children and adolescents, and avoiding consumption until two years of age [5].
We have shown in BRISA Cohort analyses that consuming soft drinks during pregnancy is associated with childhood asthma traits in children’s second year of life [6]. Pregnant women’s soft drink consumption also increases early exposure to sugary items in their offspring [7]. Finally, higher sugar consumption by children is associated with Asthma Traits at two years of age, a latent variable composed of the following indicators: number of wheezing episodes, emergency care for wheezing, asthma diagnosis, and rhinitis diagnosis [8].
Higher sugar consumption during pregnancy can modulate children’s immunological responses, increasing their risk of allergic diseases. Allergic diseases comprise chronic immune-mediated diseases, which are more prevalent among children and are mainly represented by atopic dermatitis, allergic rhinitis, bronchial asthma, and food allergies [9].
Allergic diseases are a global public health problem, as they are highly prevalent and inappropriate care leads to complications and future NCDs, increasing morbidity, mortality, and health costs [10].
A systematic review with four cohort studies showed that sugar consumption during pregnancy was associated with greater chances of children developing allergic outcomes such as allergic rhinitis, atopy and eczema, wheezing, and food allergies up to seven years of age [11].
Sugar consumption causes advanced glycation end products (AGE), which can signal allergic pathways, triggering food allergies [12]. An animal model study showed the association between an AGE-causing diet and food allergy incidences [13]. AGE can also alter gut microbiota [14], and early-age gut dysbiosis seems to relate to the development of allergic diseases such as atopic dermatitis and food allergies [15].
Thus, it would be plausible that SSB exposure in a child’s early life may increase their risk of allergies. This subject is interesting since the consumption of these beverages has increased in early life. This study analyzed the association of SSB consumption with allergies in children’s second year of life. To represent allergies in young children, we tested the latent variable Allergy Traits, with evidence of validation in our previous study in the BRISA cohort [16], consisting of shared variance among atopic dermatitis, allergic rhinitis, and food allergy medical diagnoses.

2. Materials and Methods

Data from the Brazilian Ribeirão Preto and São Luís Birth cohort (BRISA) were analyzed for São Luís city in this study. São Luís is the capital of the state of Maranhão, located in one of the poorest regions of Brazil (Northeast), with a 0.768 Municipal Human Development Index [17]. The prenatal BRISA cohort followed its participants in three moments: baseline in the gestation period, first follow-up at birth, and second follow-up around the second year of life [18].

2.1. Study Population and Sample

At baseline, pregnant women who received prenatal care from the 22nd and 25th gestational weeks and agreed to participate were included (n = 1447). On the occasion of birth (1st follow-up), from May 2010 to November 2011, puerperal women (n = 1381) were interviewed again during the first 24 h after delivery. In the 2nd follow-up, mothers and children (n = 1151) were evaluated between September 2011 and March 2013. The study sample comprised 1144 mother–child pairs, considering follow-up losses [8,18] and the exclusion of non-respondents to the allergy outcome (Supplementary Figure S1).

2.2. Data Collection

The following information was used from the baseline questionnaire: household income (multiples of the Brazilian minimum wage; about BRL 510.00 in 2010), maternal schooling (in years), occupation of the head of the family, and economic class according to the Brazil Economic Classification Criteria—CEB [19] (D/E—poorer, C, and A/B—richer).
The following information from the second follow-up was used: children’s age (months), allergy diagnoses (atopic dermatitis, allergic rhinitis, and food allergies), total duration of breastfeeding, children’s length (cm) and weight (kg), and episodes of diarrhea in the previous two weeks.
The body mass index (BMI) z-score was evaluated based on the growth curves of the World Health Organization (WHO) [20], according to the age and sex of the children. The BMI z-score was used as a categorical variable, based on the WHO cut-off points for nutritional status: thinness, eutrophy, risk of overweight, overweight, and obesity [20].
Duration of breastfeeding was obtained from the following questions in the second follow-up: “Did the baby receive breast milk yesterday?” and “If not, until what age was the baby breastfed?” The variable was treated as categorical (did not breastfeed; ≤6 months; 6 to 12 months; 12 to 18 months; and >18 months of breastfeeding).
The investigation of Allergy Traits was based on the following questions in the follow-up questionnaire: “Since birth, has a physician diagnosed atopic dermatitis (eczema; intermittent skin allergy characterized by an intensely itching skin rash in any area of the body except around the baby’s eyes and nose or near their diaper)?”, “Has any doctor ever told you that your baby has allergic rhinitis?”, and “Has any physician ever told you that your baby has an allergy to any food?”.
Venous blood specimens collected were transferred to tubes containing anticoagulant ethylenediaminetetraacetic acid (EDTA) and utilized for determining eosinophil counts in children, expressed in cells per microliter (cells/μL).

Food Intake and Consumption of SSBs

The dietary intake of 733 children in the present study was assessed through interviews with their mothers and guardians, using 24-h dietary recall (24HDR), a valid assessment tool for analyzing habitual nutrient intake of the day before, as demonstrated in a previous study using the same population sample [21]. On the date of application of the recall, the youngest age presented by the children was 12 months (0.5%), and the oldest was 32 months (0.1%), with a mean age of 16.1 + 2.3 months.
The mother or guardian responded in detail about the foods and drinks consumed by the child, including the brand, method of preparation, portion size, or volume consumed, with the aid of a photo album.
The interviewers were trained in using the 24HDR, receiving a manual explanation of how to complete it. Training personnel performed a quality control step before inserting food consumption data into the program. Information on food and drink was collected and quantified in a standardized way. Subsequently, the Virtual Nutri Plus® program (2010 version) converted consumption data into energy and nutrients. Then, the data were imported into Stata® (version 15.0), where each child’s daily sugar intake was calculated. More details can be seen in a previous study [21].
Based on the reported foods and amounts, the total consumed energy per child and the percentage of calories from sugars added to beverages to this total daily intake was estimated. The consumption of SSBs was expressed as a percentage consumption of daily calories (%SSBs) and grams of added sugar ingested per day (grams/day), which were reported as a continuous variable.
Notably, the sugary drinks included sugar-sweetened beverages, not considering drinks sweetened with table sugar or alternative low- or no-energy sweeteners, such as aspartame and sucralose. Thus, the following SSBs were included in our analysis: industrialized fruit juices (excluding fresh fruit juice), soft drinks, and ready-made chocolate milk [8].

2.3. Statistical Analysis

Descriptive analyses were performed using Stata, version 15.0, in which continuous variables were represented as central tendency measures (mean and median) and categorical variables as relative and absolute frequencies.
Considering that the consumption data do not follow a normal distribution and that we had missing data, Plus software imputed values for the missing data based on the variables that preceded them in the path analysis, using frequency analysis and Bayesian analysis [22]. The Least Weighted Squares Mean and Variance adjusted -WLSMV was used as the model estimation method, because it is robust to non-normal and allows the imputation of missing data [23].
Two latent variables were included in our analysis: (a) socioeconomic status, composed of maternal schooling, occupation of the head of the family, household income, and economic class, to which we added [24] (b) Allergy Traits: a latent variable consisting of atopic dermatitis, allergic rhinitis, and food allergy medical diagnoses [16].
Allergy Traits were evaluated by confirmatory factor analysis (CFA). We analyzed the theoretical model through structural equation modeling (SEM) in the statistical software Mplus®, version 8 (Los Angeles, CA, USA). The following adjustment indices evaluated model fit: (a) p > 0.05 and confidence intervals above 90.0%, a root mean square error of approximation < 0.08 (RMSEA), and (b) the comparative adjustment (CFI) and Tucker–Lewis indices (TLI) (>0.95) [23]. We weighted the sample to follow-up losses, using it to estimate our structural equation models.

2.4. Structural Equation Modeling (SEM)

SEM is an epidemiological tool for testing a hypothetical causal structure of multiple observable and latent variables, minimizing measurement error in the estimation process. Latent variables are not observed but are derived from the combination of effect indicator variables, representing the common variance shared among them, resulting in an estimation of effects free from the bias originated by measurement errors. In the structural equation model, effect indicators are chosen to correspond to the theoretical definition of the concept: the latent variable [23].
Latent variables help capture complex phenomena that are challenging to measure directly, such as allergies in the first two years, reducing their measurement error. Advantageously, we have proposed Allergy Traits, with validation evidence in our previous study in the BRISA cohort [16].
Figure 1 presents the conceptual model for the analysis of SSBs and Allergy Traits based on SEM.
Based on the literature, we constructed a hypothesis of our conceptual model: Socioeconomic Status (SES) will be the most distal variable, which is directly associated with the other variables of the model; SSBs will directly affect Allergy Traits around the second year of life [6,8,9,10,11,12] and these will also affected by the child’s age [25]; diarrhea will be correlated with Allergy Traits [26,27,28], and breastfeeding will be a protective factor for allergic diseases [29].

2.5. Consistency Analysis

In this study, we included an additional analysis to test the consistency of the association of SSBs with Allergy Traits. In this analysis, the eosinophil count replaced the diagnosis of allergic rhinitis (subjective measure). Previously, we had tested an allergic rhinitis compound in a latent asthma trait associated with SSBs in children in the second year of life [8].
Eosinophils were included as an outcome indicator because they actively participate in inflammatory responses, rising in allergic diseases [30]. Eosinophilia in the fourth week of life predicts the onset of atopic dermatitis in childhood, especially in individuals at high risk of atopy [31].
By introducing an objective measure predictive of allergic diseases replacing allergic rhinitis, we constructed an accurate indicator to identify if the association of SSBs would be a consistent result for Allergy Traits.
Furthermore, the association of other sugary products [8] and products referred to in the literature as allergens, such as milk and dairy products, were analyzed with Allergy Traits to assess our analysis’ consistency. Staple foods (fruits, vegetables, rice, leguminous plants, meats, fish, and shrimp) were also regressed in the models in their association with Allergy Traits.

2.6. Ethical Aspects

This study was approved by the Research Ethics Committee of the Federal University of Maranhão Hospital (protocol 4771/2008-30). All volunteers’ parents consented to participate in our research after being informed of its objectives.

3. Results

Table 1 shows the sociodemographic characteristics of the children’s families. Atopic dermatitis was very prevalent (10.3%) in the children’s second year of life. Eosinophilia was the most prevalent abnormality (one third had more than 580 cells/μL) (Table 2).
Our proposed model showed good fit for all analyzed parameters (Table 3). Atopic dermatitis (Factor Loading (FL) = 0.868; p = 0.002), food allergy (FL = 0.339; p = 0.012), and allergic rhinitis (FL = 0.255; p = 0.030) showed convergent factor loadings (Table 4).
Among the children, 14.5% already consumed SSBs, and 8.2% consumed more than the limit established by the WHO. On average, the children consumed 8.3% of their daily calories from SSBs (Table 5).
The higher percentage consumption of daily calories from SSBs was associated with higher values of Allergy Traits (Standardized Coefficient (SC) = 0.174; p = 0.025). Age increases reduced Allergy Trait values (SC = −0.181; p = 0.030). Episodes of diarrhea showed a correlation with Allergy Traits in children (SC = 0.287; p = 0.015) (Table 6).
Our consistency analysis showed no association between the percentage of daily calories from solid and pasty sugary products with Allergy Traits. Among the other products tested, only dairy consumption showed significant association, appearing as a protective factor for the Allergy Traits (Supplementary Table S2).
In the additional model of consistency analysis, which included eosinophil count as an indicator of latent outcome, the higher percentage consumption of daily calories from SSBs remained associated with higher values of Allergy Traits (SC = 0.223; p = 0.013).

4. Discussion

Early SSB exposure was associated with higher Allergy Trait values in children’s second year of life. Other sugary products failed to explain the allergy outcome.
Allergy Traits provided a good construct to assess for allergies in children’s second year of life due to three clinical indicators based on medical diagnoses (atopic dermatitis, allergic rhinitis, and food allergies) that had convergent factor loading. This approach proved advantageous as it can reduce measurement errors from any isolated allergic indicator, especially in children’s first years.
This is the first study to show early SSB exposure and allergy indicators in children’s second year of life. An analysis of children as young as six years and adolescents showed that consuming drinks with excessive free fructose ≥ 5 times/week increased their chances of allergic sensitization by 2.5 times as compared to consuming less than 3 times a month [26]. In a previous study, we showed the association between early SSB exposure and Asthma Traits in children’s second year of life [8]. The clinical indicators we proposed for the latent variables Asthma Traits (rhinitis and wheezing episodes) and Allergy Traits may be expected in individuals’ allergic march.
The explanation for the association between SSB exposure and allergies especially involves three main mechanisms: Modulate Children’s Mechanism, AGE’s Mechanism, and Dysbiosis’ Mechanism (Figure 2).
A higher consumption of SSBs during pregnancy resulted in a higher percentage of calories from sugary products in children at two years of age [7]. These findings involve genetic and environmental alterations, which can lead to a preference for sweets due to changes in taste, as well as the ingestion of greater amounts of sugars in offspring [27].
Increased consumption of SSBs by children can lead to increased oxidative stress, AGE, inflammatory response, gut dysbiosis, exacerbation of immune response, and increased Allergy Traits. The AGE’s Mechanism can involve (1) high concentrations of AGE-forming sugars that could falsely signal food allergens, activating innate immunological responses and developing early food allergies [12]; (2) high AGE levels that can trigger immunological responses by the Th2 pathway [13]; and (3) an excess of unabsorbed free fructose and the alkaline intestinal medium that could form fructose-associated AGE (enFruAGE) and pro-inflammatory signaling by fructositis, leading to large mucus production and respiratory problems [14,28].
Early exposure to sugar leads to structural and functional changes in the microbiome (dysbiosis) and in the production of inflammatory cytokines [25]. Another pathway of the dysbiotic mechanism is associated with increased intestinal permeability in the presence of fructose, favoring the colonization of pathogenic microorganisms, the dysregulation of the immune system, and the development of food allergies [15,32]. In general, opportunistic pathogen growth, altered metabolic profiles, and increased inflammation may explain how gut microbiome alterations affect hosts’ health [33].
The gut microbiota regulates immune responses, affecting sites far from the gastrointestinal tract, such as the gut–skin axis. Thus, the intestine–skin axis represents the interaction of the intestine in epithelial barrier modulation, in which the cytokines and cells it produces begin to act on the skin [34,35]. An in vitro study showed that changes in intestinal permeability could increase cytokines and dermal inflammatory disease signals, accumulating fatty acids in the skin and reducing its functionality [36].
In this study, diarrhea was correlated with Allergy Traits. Diarrhea can be a symptom of food allergies [37] and characterizes gut dysbiosis [38], which can precede allergic disease and increase the risk of its development [15,39].
Children with allergies (especially to food) show diarrhea episodes [40] and elimination diets up to their second year of life, reducing nutrient absorption and the weight gain [41]. The relationship between obesity and allergies has been shown in older children and adolescents [42]; moreover, the effect of SSBs on excess weight is not observed in the second year of life, but at more advanced ages [7,43]. The BMI z-score by age was not associated with Allergy Traits in our study, but it is possible that this effect is observed in older children.
Age increase (in months) reduced Allergy Trait values. Immune tolerance to antigens begins during pregnancy and continues throughout a child’s first years. During this period environmental factors, including nutrition, can permanently alter and irreversibly the damage the immune system [44]. The window of immunity has been defined as a window of opportunity and also of susceptibility and comprises the period of the first thousand days of life [45]. Thus, ingesting the first allergenic proteins in the diet configures exposures that help modulate immune responses and reduce the risk of allergies [46].
Unexpectedly, our consistency analysis showed dairy consumption as a protective factor for the Allergy Traits. Children diagnosed with food allergies and atopy may already have diets that exclude milk and its derivatives. Dairy products can also elevate butyrate levels, which can act on the immune system by regulatory T-cell expansion and are related to beneficial bacterial colonization [47]. Dietary fiber may also raise butyrate levels; however, our results showed no association with Allergy Traits.
As an additional analysis, the dairy consumption with Allergy Traits lost significance when we removed the food allergy indicator from the latter. These results support that apparent protection had been biased because children diagnosed with food allergies typically excluded milk and its derivatives.
By replacing allergic rhinitis with eosinophil count in the consistence analysis, we included a more objective measure of our studied outcome, provided greater consistency to association of SSBs with Allergy Traits, and avoided attributing the weight of the association to allergic rhinitis, which we tested in a previous study to Asthma Traits [8]. This study estimated the association between beverages rich in added sugars and the latent variable “child asthma traits” in the second year of life, and similarly to what was verified in the present study, the authors showed that a high percentage of daily calories from added sugars to SSBs was directly associated with higher values of childhood asthma traits, without mediation pathways [8].
We can list the lack of allergenic tests in the BRISA Cohort, and the allergy indicators based on a questionnaire, in which the parents reported diagnosis of allergic diseases as limitations of this study. Circumventing them, we analyzed this outcome as a latent variable based on the variance between three indicators, reducing measurement errors. As a strength, equation modeling enabled us to explore multiple exposures, including other dietary items associated with Allergy Traits.
Although the lack of other studies evaluating the association of SSBs with allergic diseases in the same age group configures innovation, it hindered the comparability of our data in different populations. An age group that should not be exposed [5] to sugar consumption showed a worrying incidence rate, and the percentage of children with early exposure to SSBs can be compared to data from American children.
In US children aged 0–5 years, SSBs were consumed by 5% of children aged 6 to 11 months and 31% of children aged 12 to 23 months, and the caloric contribution of these beverages concerning the intake total was 3.4% [48]. The introduction of SSBs has been frequent and begins early in childhood, even before six months. Introducing these drinks during pregnancy and in the first six years of life determines the preference for sweet flavors and their intake in increasing quantities later [27]. Thus, the consumption of SSBs ceases to be an option included by parents that belong to children’s choices and preferences.
Allergies and asthma feature among the immune-mediated non-communicable diseases associated with increased future risk of other such diseases [49,50]. The origins of immune-mediated diseases have been explained by the early exposure of immature immunological systems [51].

5. Conclusions

We showed that SSB exposure is associated with Allergy Traits in children’s second year of life, similar to what we already pictured for Asthma Traits. This latent variable does not aim at clinical implementations in allergy diagnosis; instead, it is possible for epidemiological studies, which, like ours, may identify factors associated with greater consistency to Allergy Traits, to encourage prevention strategies in the health care of newborns and children.

6. Clinical Implications

International guidelines have cautioned against consuming SSBs in children under two years to mitigate the risk of obesity and non-communicable diseases in later life. Our findings suggest that early non-exposure to SSBs may also reduce immune-mediated diseases. Abstaining from these beverages may also confer additional advantages in curtailing allergic diseases during early childhood. Our findings suggest that coping with these immune-mediated diseases should focus on the economic and commercial determinants that increase such early exposure to SSBs.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/nu15143218/s1, Figure S1: Flow diagram of the BRISA prenatal cohort study, São Luís, Brazil title; Table S1: Food consumption data (daily) in children’s second year of life. BRISA Prenatal Cohort, São Luís, Brazil, 2010–2013; Table S2: Adjusted model indicators and standardized estimates of direct effects considering the association between food consumption variables and Allergy Traits in children’s second year of life. BRISA Prenatal Cohort, São Luís, Brazil, 2010–2013.

Author Contributions

A.K.O.A.M. and C.C.C.R. drafted survey questions; A.K.O.A.M., L.L.P., J.X.P.T.N. and C.C.C.R. contributed to the data analyses; A.K.O.A.M. wrote the original draft; all authors contributed to the writing, reviewing, and editing of this manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Coordination for the Improvement of Higher Education Personnel (CAPES): Finance Code 001; Department of Science and Technology (DECIT/Brazilian Ministry of Health): Processo 17617/2017-29; and the São Paulo Research Foundation (FAPESP): 2008/53593-0.

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki, and approved by the Ethics Committee of the Federal University of Maranhão Hospital (protocol 4771/2008-30).

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Data Availability Statement

The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.

Acknowledgments

We would like to thank the funding and/or supporting by: the National Council for Scientific and Technological Development (CNPq), the Department of Science and Technology (DECIT/Brazilian Ministry of Health), the São Paulo Research Foundation (FAPESP), the Maranhão State Research Foundation for Scientific and Technological Development (FAPEMA), Foundation of Support to Teaching, Research and Assistance of Clinics Hospital of Ribeirão Preto Medical School, University of São Paulo (FAEPA), Coordination for the Improvement of Higher Education Personnel (CAPES): Finance Code 001 and Amazônia Legal 0810/2020/88881.510244/2020-01.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Malik, V.S.; Popkin, B.M.; Bray, G.A.; Després, J.P.; Hu, F.B. Sugar-Sweetened Beverages, Obesity, Type 2 Diabetes Mellitus, and Cardiovascular Disease Risk. Circulation 2015, 121, 1356–1364. [Google Scholar] [CrossRef] [PubMed]
  2. CDC—Center for Disease Control Prevention. The CDC Guide to Strategies for Reducing the Consumption of Sugar-Sweetened Beverages. 2010. Available online: https://stacks.cdc.gov/view/cdc/51532/cdc_51532_DS1.pdf (accessed on 1 June 2023).
  3. Santos, L.P.; Gigante, D.P.; Delpino, F.M.; Maciel, A.P.; Bielemann, R.M. Sugar Sweetened Beverages Intake and Risk of Obesity and Cardiometabolic Diseases in Longitudinal Studies: A Systematic Review and Meta-Analysis with 1.5 Million Individuals. Clin. Nutr. ESPEN 2022, 51, 128–142. [Google Scholar] [CrossRef] [PubMed]
  4. World Health Organization. Diretriz: Ingestão de Açúcares Por Adultos e Crianças. 2015. Available online: https://www.paho.org/hq/dmdocuments/2015/NOTA-DIRECTRIZ-AZUCAR-POR-EDITADO.pdf (accessed on 1 June 2023).
  5. American Heart Association—AHA. Added Sugars. Available online: http://www.heart.org/HEARTORG/HealthyLiving/HealthyEating/Nutrition/Added-Sugars_UCM_305858_Article.jsp#.XL-mGehKjIV (accessed on 23 April 2019).
  6. Nascimento, J.X.P.T.; Ribeiro, C.C.C.; Batista, R.F.L.; De Britto Alves, M.T.S.S.; Simões, V.M.F.; Padilha, L.L.; Cardoso, V.C.; Vianna, E.O.; Bettiol, H.; Barbieri, M.A.; et al. The First 1000 Days of Life Factors Associated with “Childhood Asthma Symptoms”: Brisa Cohort, Brazil. Sci. Rep. 2017, 7, 16028. [Google Scholar] [CrossRef] [Green Version]
  7. Pinto, D.A.S.; Nascimento, J.X.P.T.; Padilha, L.L.; Da Conceição, S.I.O.; França, A.K.T.D.C.; Simaes, V.M.F.; Batista, R.F.L.; Barbieri, M.A.; Ribeiro, C.C.C. High Sugar Content and Body Mass Index: Modelling Pathways around the First 1000 d of Life, BRISA Cohort. Public Health Nutr. 2021, 24, 4997–5005. [Google Scholar] [CrossRef] [PubMed]
  8. Padilha, L.L.; Vianna, E.O.; Vale, A.T.M.; Nascimento, J.X.P.T.; da Silva, A.A.M.; Ribeiro, C.C.C. Pathways in the Association between Sugar Sweetened Beverages and Child Asthma Traits in the 2nd Year of Life: Findings from the BRISA Cohort. Pediatr. Allergy Immunol. 2020, 31, 480–488. [Google Scholar] [CrossRef] [PubMed]
  9. Hendaus, M.A.; Jomha, F.A.; Ehlayel, M. Allergic Diseases among Children: Nutritional Prevention and Intervention. Ther. Clin. Risk Manag. 2016, 12, 361–372. [Google Scholar] [CrossRef] [Green Version]
  10. Sánchez-Borges, M.; Martin, B.L.; Muraro, A.M.; Wood, R.A.; Agache, I.O.; Ansotegui, I.J.; Casale, T.B.; Fleisher, T.A.; Hellings, P.W.; Papadopoulos, N.G.; et al. The Importance of Allergic Disease in Public Health: An ICAALL Statement. World Allergy Organ. J. 2018, 11, 8. [Google Scholar] [CrossRef] [PubMed]
  11. Gupta, A.; Singh, A.; Fernando, R.L.; Dharmage, S.C.; Lodge, C.J.; Waidyatillake, N.T. The Association between Sugar Intake during Pregnancy and Allergies in Offspring: A Systematic Review and a Meta-Analysis of Cohort Studies. Nutr. Rev. 2022, 80, 904–918. [Google Scholar] [CrossRef] [PubMed]
  12. Smith, P.K.; Masilamani, M.; Li, X.M.; Sampson, H.A. The False Alarm Hypothesis: Food Allergy Is Associated with High Dietary Advanced Glycation End-Products and Proglycating Dietary Sugars That Mimic Alarmins. J. Allergy Clin. Immunol. 2017, 139, 429–437. [Google Scholar] [CrossRef] [Green Version]
  13. Yu, G.; Zhang, Q.; Li, H.; Wang, Y.; Sheng, H.; Zhang, S.; Fu, L. Effects of Allergen-Specific and Non-Specific AGEs on the Allergenicity of Ovalbumin in a Mouse Model of Food Allergy. Mol. Nutr. Food Res. 2023, 67, 2200221. [Google Scholar] [CrossRef]
  14. Dechristopher, L.R.; Tucker, K.L. Excess Free Fructose, Apple Juice, High Fructose Corn Syrup and Childhood Asthma Risk—The National Children’s Study. Nutr. J. 2020, 19, 60. [Google Scholar] [CrossRef] [PubMed]
  15. Bunyavanich, S.; Berin, M.C. Food Allergy and the Microbiome: Current Understandings and Future Directions. J. Allergy Clin. Immunol. 2019, 144, 1468–1477. [Google Scholar] [CrossRef] [PubMed]
  16. Muniz, A.K.O.A.; Ribeiro, C.C.C.; Vianna, E.O.; Serra, H.C.O.A.; Nascimento, J.X.P.T.; Cardoso, V.C.; Barbieri, M.A.; da Silva, A.A.M.; Bettiol, H. Factors Associated with Allergy Traits around the 2nd Year of Life: A Brazilian Cohort Study. BMC Pediatr. 2022, 22, 703. [Google Scholar] [CrossRef] [PubMed]
  17. IBGE. Available online: https://cidades.ibge.gov.br/brasil/ma/sao-luis/panorama (accessed on 6 October 2019).
  18. Confortin, S.C.; Ribeiro, M.R.C.; Barros, A.J.D.; Menezes, A.M.B.; Horta, B.L.; Victora, C.G.; Barros, F.C.; Gonçalves, H.; Bettiol, H.; Dos Santos, I.S.; et al. RPS Brazilian Birth Cohorts Consortium (Ribeirão Preto, Pelotas and São Luís): History, Objectives and Methods. Cad. Saude Publica 2021, 37, 1–14. [Google Scholar] [CrossRef]
  19. Associação Brasileira de Empresas de Pesquisa ABEP Critério de Classificação Do Brasil 2010. Available online: http://www.abep.org/Servicos/Download.aspx?id=01 (accessed on 1 June 2023).
  20. WHO. WHO Child Growth Standards Based on Length/Height, Weight and Age. Acta Paediatr. 2006, 450, 76–85. [Google Scholar] [CrossRef]
  21. Padilha, L.L.; França, A.K.T.D.C.; Da Conceição, S.I.O.; Carvalho, W.R.C.; Batalha, M.A.; Da Silva, A.A.M. Nutrient Intake Variability and the Number of Days Needed to Estimate Usual Intake in Children Aged 13–32 Months. Br. J. Nutr. 2017, 117, 287–294. [Google Scholar] [CrossRef] [Green Version]
  22. Muthén, L.K.; Muthén, B.O. Statistical Analysis with Latent Variables User’s Guide, 8th ed.; Muthén & Muthén: Los Angeles, CA, USA, 1998. [Google Scholar]
  23. Kline, R. Principles and Practice of Structural Equation Modeling, 4th ed.; The Guilford Press: New York, NY, USA, 2016. [Google Scholar]
  24. Ribeiro, M.R.C.; da Silva, A.A.M.; de Britto e Alves, M.T.S.S.; Batista, R.F.L.; Ribeiro, C.C.C.; Schraiber, L.B.; Bettiol, H.; Barbieri, M.A. Effects of Socioeconomic Status and Social Support on Violence against Pregnant Women: A Structural Equation Modeling Analysis. PLoS ONE 2017, 12, e0170469. [Google Scholar] [CrossRef] [Green Version]
  25. Wang, Y.; Qi, W.; Song, G.; Pang, S.; Peng, Z.; Li, Y.; Wang, P. High-Fructose Diet Increases Inflammatory Cytokines and Alters Gut Microbiota Composition in Rats. Mediators Inflamm. 2020, 2020, 6672636. [Google Scholar] [CrossRef]
  26. Yu, R.; Yang, B.; Cai, L.; Lu, X.; Wang, X. Excess Free Fructose Beverages and Allergy in Children and Adolescents: Results From NHANES 2005–2006. Ann. Fam. Med. 2018, 16, 408. [Google Scholar] [CrossRef]
  27. Laitala, M.L.; Vehkalahti, M.M.; Virtanen, J.I. Frequent Consumption of Sugar-Sweetened Beverages and Sweets Starts at Early Age. Acta Odontol. Scand. 2017, 76, 105–110. [Google Scholar] [CrossRef]
  28. DeChristopher, L.R. Perspective: The Paradox in Dietary Advanced Glycation End Products Research—The Source of the Serum and Urinary Advanced Glycation End Products Is the Intestines, Not the Food. Adv. Nutr. 2017, 8, 679. [Google Scholar] [CrossRef] [Green Version]
  29. Oddy, W.H. Breastfeeding, Childhood Asthma, and Allergic Disease. Ann. Nutr. Metab. 2017, 70, 26–36. [Google Scholar] [CrossRef] [PubMed]
  30. Fulkerson, P.C.; Rothenberg, M.E. Targeting Eosinophils in Allergy, Inflammation and Beyond. Nat. Rev. Drug Discov. 2013, 12, 117–129. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  31. Rossberg, S.; Gerhold, K.; Geske, T.; Zimmermann, K.; Menke, G.; Zaino, M.; Wahn, U.; Hamelmann, E.; Lau, S. Elevated Blood Eosinophils in Early Infancy Are Predictive of Atopic Dermatitis in Children with Risk for Atopy. Pediatr. Allergy Immunol. 2016, 27, 702–708. [Google Scholar] [CrossRef]
  32. Blázquez, A.B.; Berin, M.C. Microbiome and Food Allergy. Transl. Res. 2017, 179, 199. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Belkaid, Y.; Hand, T.W. Role of the Microbiota in Immunity and Inflammation. Cell 2014, 157, 121. [Google Scholar] [CrossRef] [Green Version]
  34. Ahluwalia, B.; Magnusson, M.K.; Öhman, L. Mucosal Immune System of the Gastrointestinal Tract: Maintaining Balance between the Good and the Bad. Scand. J. Gastroenterol. 2017, 52, 1185–1193. [Google Scholar] [CrossRef]
  35. Akdis, C.A. The Epithelial Barrier Hypothesis Proposes a Comprehensive Understanding of the Origins of Allergic and Other Chronic Noncommunicable Diseases. J. Allergy Clin. Immunol. 2022, 149, 41–44. [Google Scholar] [CrossRef]
  36. Lee, H.R.; Sung, J.H. Multiorgan-on-a-Chip for Realization of Gut-Skin Axis. Biotechnol. Bioeng. 2022, 119, 2590–2601. [Google Scholar] [CrossRef]
  37. Zubeldia-Varela, E.; Barker-Tejeda, T.C.; Obeso, D.; Villaseñor, A.; Barber, D.; Pérez-Gordo, M. Microbiome and Allergy: New Insights and Perspectives. J. Investig. Allergol. Clin. Immunol. 2022, 32, 327–344. [Google Scholar] [CrossRef]
  38. Li, Y.; Xia, S.; Jiang, X.; Feng, C.; Gong, S.; Ma, J.; Fang, Z.; Yin, J.; Yin, Y. Gut Microbiota and Diarrhea: An Updated Review. Front. Cell. Infect. Microbiol. 2021, 11, 625210. [Google Scholar] [CrossRef] [PubMed]
  39. Zhang, Q.; Cheng, L.; Wang, J.; Hao, M.; Che, H. Antibiotic-Induced Gut Microbiota Dysbiosis Damages the Intestinal Barrier, Increasing Food Allergy in Adult Mice. Nutrients 2021, 13, 3315. [Google Scholar] [CrossRef] [PubMed]
  40. El-Asheer, O.M.; El-Gazzar, A.F.; Zakaria, C.M.; Hassanein, F.A.; Mohamed, K.A. Frequency of Gastrointestinal Manifestations among Infants with Cow’s Milk Protein Allergy, Egypt. Egypt. Pediatr. Assoc. Gaz. 2022, 70, 34. [Google Scholar] [CrossRef]
  41. Meyer, R.; De Koker, C.; Dziubak, R.; Venter, C.; Dominguez-Ortega, G.; Cutts, R.; Yerlett, N.; Skrapak, A.K.; Fox, A.T.; Shah, N. Malnutrition in Children with Food Allergies in the UK. J. Hum. Nutr. Diet. 2014, 27, 227–235. [Google Scholar] [CrossRef] [PubMed]
  42. Visness, C.M.; London, S.J.; Daniels, J.L.; Kaufman, J.S.; Yeatts, K.B.; Siega-Riz, A.M.; Liu, A.H.; Calatroni, A.; Zeldin, D.C. Association of Obesity with IgE Levels and Allergy Symptoms in Children and Adolescents: Results from the National Health and Nutrition Examination Survey 2005–2006. J. Allergy Clin. Immunol. 2009, 123, 1163–1169.e4. [Google Scholar] [CrossRef] [Green Version]
  43. Pan, L.; Li, R.; Park, S.; Galuska, D.A.; Sherry, B.; Freedman, D.S. A Longitudinal Analysis of Sugar-Sweetened Beverage Intake in Infancy and Obesity at 6 Years. Pediatrics 2014, 134, S29–S35. [Google Scholar] [CrossRef] [Green Version]
  44. García-Serna, A.M.; Martín-Orozco, E.; Hernández-Caselles, T.; Morales, E. Prenatal and Perinatal Environmental Influences Shaping the Neonatal Immune System: A Focus on Asthma and Allergy Origins. Int. J. Environ. Res. Public Health 2021, 18, 3962. [Google Scholar] [CrossRef]
  45. Di Costanzo, M.; De Paulis, N.; Capra, M.E.; Biasucci, G. Nutrition during Pregnancy and Lactation: Epigenetic Effects on Infants&rsquo; Immune System in Food Allergy. Nutrients 2022, 14, 1766. [Google Scholar] [CrossRef]
  46. van Splunter, M.; Liu, L.; Joost van Neerven, R.J.; Wichers, H.J.; Hettinga, K.A.; de Jong, N.W. Mechanisms Underlying the Skin-Gut Cross Talk in the Development of IgE-Mediated Food Allergy. Nutrients 2020, 12, 3830. [Google Scholar] [CrossRef]
  47. Roduit, C.; Frei, R.; Ferstl, R.; Loeliger, S.; Westermann, P.; Rhyner, C.; Schiavi, E.; Barcik, W.; Rodriguez-Perez, N.; Wawrzyniak, M.; et al. High Levels of Butyrate and Propionate in Early Life Are Associated with Protection against Atopy. Allergy 2019, 74, 799–809. [Google Scholar] [CrossRef]
  48. Demmer, E.; Cifelli, C.J.; Houchins, J.A.; Fulgoni, V.L. Ethnic Disparities of Beverage Consumption in Infants and Children 0–5 Years of Age; National Health and Nutrition Examination Survey 2011 to 2014. Nutr. J. 2018, 17, 78. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  49. Ascott, A.; Mulick, A.; Yu, A.M.; Prieto-Merino, D.; Schmidt, M.; Abuabara, K.; Smeeth, L.; Roberts, A.; Langan, S.M. Atopic Eczema and Major Cardiovascular Outcomes: A Systematic Review and Meta-Analysis of Population-Based Studies. J. Allergy Clin. Immunol. 2019, 143, 1821–1829. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  50. Juber, N.F.; Lee, C.C.; Pan, W.C.; Liu, J.J. Associations between Pediatric Asthma and Adult Non-Communicable Diseases. Pediatr. Allergy Immunol. 2021, 32, 314–321. [Google Scholar] [CrossRef] [PubMed]
  51. Bisgaard, H.; Bønnelykke, K.; Stokholm, J. Immune-Mediated Diseases and Microbial Exposure in Early Life. Clin. Exp. Allergy 2014, 44, 475–481. [Google Scholar] [CrossRef] [PubMed]
Figure 1. A conceptual model for analysis of the association between SSB consumption and Allergy Traits in children aged around two years. BRISA Prenatal Cohort, São Luís, Brazil, 2010–2013.
Figure 1. A conceptual model for analysis of the association between SSB consumption and Allergy Traits in children aged around two years. BRISA Prenatal Cohort, São Luís, Brazil, 2010–2013.
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Figure 2. Plausible Mechanisms to association of early exposure to SSBs and allergies.
Figure 2. Plausible Mechanisms to association of early exposure to SSBs and allergies.
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Table 1. Family’s sociodemographic characteristics in the baseline. BRISA Prenatal Cohort. São Luís, Brazil, 2010–2013.
Table 1. Family’s sociodemographic characteristics in the baseline. BRISA Prenatal Cohort. São Luís, Brazil, 2010–2013.
VariableBaseline
Maternal years of schoolingn%
0–4171.5
5–811410.0
9–1187276.2
≥1212611.0
No information available151.3
Occupation of the head of the family
Unskilled manual workers30826.9
Semi-skilled manual workers45739.9
Skilled manual workers514.5
Office positions16114.1
Higher education professionals 575.0
Administrators/owners363.1
No information available746.5
Household income 1
<1121.1
1 and <352145.5
3 and <536031.5
≥520718.1
No information available443.8
Economic class
D-E16914.8
C74364.9
A-B 216614.5
No information available665.8
Total1144100
1 Number of minimum wage. 2 A and B are the highest family incomes.
Table 2. Demographic and health characteristics in children’s second year of life. BRISA Prenatal Cohort, São Luís, Brazil, 2010–2013.
Table 2. Demographic and health characteristics in children’s second year of life. BRISA Prenatal Cohort, São Luís, Brazil, 2010–2013.
Variable2nd Year of Life
Age (months)MeanSD 1
16.02.3
Median Percentiles 25–75
15.014.0–17.0
Gendern%
Male57149.9
Female56849.6
No information available50.4
Duration of breastfeeding
Did not breastfeed80.7
≤6 months15713.7
6 to 12 months12611.0
12 to 18 months72063.0
>18 months706.1
No information available635.5
BMI z-score 2
Thinness211.8
Eutrophy69160.4
Risk of overweight28925.3
Overweight988.6
Obesity322.8
No information available131.1
Physician made diagnosis of allergic rhinitis
No107193.6
Yes736.4
Physician made diagnosis of atopic dermatitis
No102689.7
Yes11810.3
Physician made diagnosis of food allergies
No111297.2
Yes322.8
Eosinophil count (tertile)
1st tertile (13–311 cells/μL)25522.3
2nd tertile (312–580 cells/μL)25522.3
3rd tertile (>580 cells/μL)25522.3
No information available37933.1
Total1144100
1 SD: standard deviation. 2 z-score of Body mass index for age and sex.
Table 3. Indexes of model fit by structural equation model to analyze association between Allergy Traits and SSB consumption in children’s second year of life. BRISA Prenatal Cohort, São Luís, Brazil, 2010–2013.
Table 3. Indexes of model fit by structural equation model to analyze association between Allergy Traits and SSB consumption in children’s second year of life. BRISA Prenatal Cohort, São Luís, Brazil, 2010–2013.
IndicatorsModel
Root Mean Square Error of Approximation (RMSEA)0.017
RMSEA (90% CI 1)0.000–0.028
p-value1.0
Comparative Fit Index (CFI)0.973
Tucker-Lewis Fit Index (TLI)0.956
1 Confidence Interval.
Table 4. Standardized coefficients, standard errors, and p-values of latent variable Socioeconomic Status and Allergy Traits. BRISA Prenatal Cohort, São Luís, Brazil, 2010–2013.
Table 4. Standardized coefficients, standard errors, and p-values of latent variable Socioeconomic Status and Allergy Traits. BRISA Prenatal Cohort, São Luís, Brazil, 2010–2013.
Latent VariableIndicator VariablesFactor LoadingSE 1p-Value
Socioeconomic status (SES)Occupation of the head of the family0.5330.031<0.001
Household income0.6230.034
Maternal schooling 0.4320.030
Economic class 0.6780.031
Allergy TraitsAtopic dermatitis0.8680.2790.002
Allergic rhinitis0.2550.1170.030
Food allergy0.3390.1350.012
1 SE = Standard Error.
Table 5. Consumption of SSBs and other products with added sugar data (daily) in children’s second year of life. BRISA Prenatal Cohort, São Luís, Brazil, 2010–2013.
Table 5. Consumption of SSBs and other products with added sugar data (daily) in children’s second year of life. BRISA Prenatal Cohort, São Luís, Brazil, 2010–2013.
VariableMeanSD 1MedianPercentiles 25–75
Consumption of sugar-sweetened
beverages
%8.36.85.93.4–11.6
g20.013.616.510.5–23.0
Chocolate milk (Kcal)120.391.888.244.1–180.7
Soft drinks (Kcal)56.427.650.338.7–68.4
Industrialized juices (Kcal)75.851.763.045.0–87.0
Consumption of sugared
pasty products
%11.56.810.06.6–13.8
g20.512.119.89.9–22.0
Dairy drinks (Kcal)124.868.7131.765.8–131.7
Popsicles and ice cream (Kcal)172.762.2193.7110.5–221.0
Industrialized baby food (Kcal)75.813.776.073.0–76.0
Consumption of sugared
solids
%7.55.65.83.9–9.7
g15.412.310.97.2–18.1
Cakes (Kcal)121.694.995.347.7–214.5
Cookies (Kcal)90.381.363.742.5–90.0
Percentage of sugar intake in products with high sugar in relation to total calorie
SSBs n%
None62785.5
≤5%466.3
>5%608.2
Sugared pasty productsNone40455.1
≤5%354.8
>5%29440.1
Sugared
solids
None67892.5
≤5%233.1
>5%324.4
All products with high sugarNone31042.3
≤5%638.6
>5%36049.1
Total733100
1 SD = Standard Deviation.
Table 6. Adjusted model indicators and standardized estimates of direct effects considering the association between variables and Allergy Traits in children’s second year of life. BRISA Prenatal Cohort, São Luís, Brazil, 2010–2013.
Table 6. Adjusted model indicators and standardized estimates of direct effects considering the association between variables and Allergy Traits in children’s second year of life. BRISA Prenatal Cohort, São Luís, Brazil, 2010–2013.
ExposuresStandardized Estimates of the Direct Effect on Allergy Traits
SC 1SD 2p-Value
Child’s Age (association)−0.1810.0830.030
Higher percentage consumption of daily calories from SSBs (association)0.1740.0780.025
Episodes of diarrhea (correlation)0.2870.1180.015
1 SC = Standardized Coefficient; 2 SD: standard deviation.
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Muniz, A.K.O.A.; Vianna, E.O.; Padilha, L.L.; Nascimento, J.X.P.T.; Batista, R.F.L.; Barbieri, M.A.; Bettiol, H.; Ribeiro, C.C.C. Sugar-Sweetened Beverages and Allergy Traits at Second Year of Life: BRISA Cohort Study. Nutrients 2023, 15, 3218. https://doi.org/10.3390/nu15143218

AMA Style

Muniz AKOA, Vianna EO, Padilha LL, Nascimento JXPT, Batista RFL, Barbieri MA, Bettiol H, Ribeiro CCC. Sugar-Sweetened Beverages and Allergy Traits at Second Year of Life: BRISA Cohort Study. Nutrients. 2023; 15(14):3218. https://doi.org/10.3390/nu15143218

Chicago/Turabian Style

Muniz, Alessandra Karla Oliveira Amorim, Elcio Oliveira Vianna, Luana Lopes Padilha, Joelma Ximenes Prado Teixeira Nascimento, Rosangela Fernandes Lucena Batista, Marco Antonio Barbieri, Heloisa Bettiol, and Cecilia Claudia Costa Ribeiro. 2023. "Sugar-Sweetened Beverages and Allergy Traits at Second Year of Life: BRISA Cohort Study" Nutrients 15, no. 14: 3218. https://doi.org/10.3390/nu15143218

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