Artigos

INTRODUCTION
Food allergy (FA) affects approximately 10% of the population1, occurring primarily in children2, and its prevalence is increasing2–4, becoming a public health issue2,3. FA occurs after ingestion and/or contact with one or more foods that trigger an abnormal immune response2,5.
FAs are classified according to the immune mechanism involved and can be IgE-mediated, non-IgE-mediated (cell-mediated), or mixed2. Cutaneous, gastrointestinal, respiratory, cardiovascular, and systemic manifestations may occur2. Treatment involves excluding the food allergen from the diet6,7 plus symptomatic treatment when necessary7. Once food allergens are excluded, appropriate nutritional substitution must be ensured8,9.
Exclusion diets prevent allergic reactions but may pose nutritional risks9. Children on allergen-free diets are at greater risk of inadequate micronutrient intake, nutritional deficiencies, impaired growth, and feeding difficulties10. On the other hand, they may develop obesity, possibly because of poor food choices and unbalanced diets11. Childhood and adolescence are critical periods from a nutritional perspective due to growth and development12, and exclusion diets often restrict essential nutrients for these stages11. In addition, children with FA may be in a state of persistent subclinical inflammation of the gastrointestinal mucosa11. Therefore, the growth of children and adolescents with FA is a matter of concern.
Most studies indicate that growth parameters in children with FA are lower than in children without FA10. However, most research is cross-sectional, few studies have assessed the impact on growth for more than one year13, and most findings are heterogeneous due to differences in the studied populations and growth assessment methods10. Some studies have investigated the impact of FA on growth and nutritional status, particularly in schoolers and/or adolescents14–21, across different countries. However, to our knowledge, no studies have been conducted in Brazil. As a developing country with a culturally diverse population, especially regarding dietary habits and different social conditions, it is important to understand the long-term impact of FA on the growth of Brazilian children and adolescents.
Thus, the main objective of this study is to compare the height of adolescents with presumed FA to those without FA in a birth cohort from a city in the state of São Paulo, Brazil. Secondary objectives include comparing body-mass index (BMI) and waist circumference (WC) within the same population and exploring differences among subgroups regarding the number and types of foods involved in presumed FA and the duration of allergen exclusion from the diet.?
METHOD
This is a cross-sectional analysis performed with data from a longitudinal study of the BRISA birth cohort (an acronym for Brazilian Ribeirão Preto and São Luís Birth Cohort Studies). The BRISA cohort is a population-based prospective birth cohort study conducted in two Brazilian cities, Ribeirão Preto/São Paulo (RP/SP) and São Luís/Maranhão22. For the present study, only the RP/SP cohort was included.
In RP/SP, data collection occurred in eight public and private maternities, including 7,752 newborns, corresponding to 95.7% of all live births in 2010. Among these, 3,796 children were reassessed between one and three years of age (from January 2011 to October 2013), and 2,963 adolescents (38% of the original cohort) were reassessed between 11 and 13 years of age (from March 2022 to July 2023), with the latter being eligible for the present study. The following participants were excluded from the study: twins; those non-orally fed; those with a self-reported diagnosis of conditions that influence growth (Cerebral Palsy, Down Syndrome, Turner Syndrome, Marfan Syndrome, West Syndrome, Saethre-Chotzen Syndrome, myelomeningocele, achondroplasia, growth deficiency, abnormalities in growth hormone production, and precocious puberty); and those whose parents/guardians and/or the participants themselves did not consent to participate.
The article followed the STROBE (Strengthening the Reporting of Observational Studies in Epidemiology) statement recommendations23. ChatGPT was consulted for assistance in translating the article into English and revising it. This study was approved by the Research Ethics Committee of the Ribeirao Preto Medical School, University of Sao Paulo (CAAE 64519822.0.0000.5440), and informed consent and assent forms were obtained.
The participants were then categorized into two groups: the interest group, consisting of those with presumed FA (current or past), and the non-exposed (NE) group, composed of adolescents without this condition.
Diagnosis of Food Allergy (FA)
FA was initially identified based on the response provided at 11–13 years of age to the following question: “Has [participant’s name] ever had or currently have a medical diagnosis of food allergy?” Adolescents who answered “no” were assigned to the NE group, while those who answered “yes” were selected to answer a specific questionnaire to characterize the FA diagnosis further.
The questionnaire was applied via telephone call with parents/guardians and participants between January and December 2023 by a single researcher (LDN). It was developed by a pediatric allergist based on the questionnaire by Solé et al24. Until now, no validated and translated questionnaire in Portuguese has been available in the literature to confirm an FA diagnosis.
The questionnaire addressed topics such as age at diagnosis, family history of allergic diseases, coexisting conditions, involved foods, timing of the adverse reaction after ingestion, and associated symptoms. Additionally, participants were asked about how the medical diagnosis was established, the duration of the allergen exclusion diet, and follow-ups with medical specialists (gastroenterologist and/or allergist) and a nutritionist.
The responses were thoroughly reviewed by two researchers (LDN and FC). Following this review, based on clinical manifestations and the treatment received, individuals with unlikely FA were identified and excluded: diagnoses not made by a physician, food intolerances, drug allergies, diagnoses based only on laboratory tests (absent signs/symptoms), diagnoses inconsistent with FA (e.g., food poisoning), and significant data collection issues that prevented accurate analysis. Thus, the participants were categorized into two groups: 1) presumed FA group – participants with a positive response for a medical diagnosis of FA and a specific questionnaire consistent with the diagnosis; 2) NE group (without FA) – participants with a negative response for a medical diagnosis of FA (Figure 1).
In secondary analyses aiming to investigate the impact of FA on growth further, participants were classified into subgroups based on the number of foods involved in presumed FA (non-exposed, one food, or two or more foods), the duration of allergen exclusion from the diet (non-exposed, ? 36 months, or > 36 months), or the type of food involved in presumed FA (non-exposed, cow’s milk, other foods, or exclusively food dye). Participants with cow’s milk allergy may also have presumed FA to other foods. However, those with presumed FA to other foods did not have milk allergy, and individuals with allergy exclusive to food dye were classified separately. Regarding exclusion diet duration, for participants with allergy to two or more foods, the total exclusion periods were recorded and intersected according to the age range during which the allergen was eliminated from the diet.
Anthropometric assessment
Anthropometric measurements were obtained from the participants in the three stages of the cohort, conducted by trained staff and following standardized measurement techniques. At birth, weight and length were converted into Z-scores according to the INTERGROWTH-21st25,26, curves for weight-for-age (W/A), length-for-age (H/A), and weight/length-for-age (WL/A) indices using the INTERGROWTH-21st30 software27. At ages 1–3 years, weight and height were converted into Z-scores for W/A, height-for-age (H/A), and body-mass index-for-age (BMI/A) based on the 2006 World Health Organization (WHO) growth standard curves28, using the Anthro software29. Preterm children (< 37 weeks of gestational age) were classified according to their corrected age. Regarding WC classification, since there is no available reference for this age range, only the mean value was reported. At ages 11–13, height and BMI were converted into Z-scores for H/A and BMI/A according to the 2007 WHO growth reference curves30, using the AnthroPlus software31. Excess weight was defined as BMI/A>+1. WC was classified as normal/high according to McCarthy et al32, considering the 90th percentile as the threshold for classification33.
Sociodemographic, economic, and health data of the child
The following variables were considered: 1) At birth: maternal self-reported skin color/race, maternal marital status and education level, socioeconomic conditions as defined by the Brazilian Economic Classification Criteria (CCEB/ABEP)34, child’s sex, type of delivery, gestational age (GA) at birth, Apgar score at the 5th minute of life, maternal lifestyle habits during pregnancy (tobacco and alcohol consumption), and hypertension and diabetes mellitus during pregnancy; 2) At ages 1–3 years: presence of disease and/or physical impairment or developmental delay, duration of exclusive breastfeeding (EBF), and age at introduction of semi-solid or solid foods; 3) At ages 11–13 years: reported parental height (used to calculate the target parental height35), reported skin color or race/ethnicity, history of hospitalizations, use of dietary supplements, continuous use of medication (corticosteroids), pubertal staging classification (assessed using the Pubertal Development Scale adapted for the Brazilian population by Pompeia et al36), and diagnosis of conditions and/or diseases in the child (genetic and chromosomal syndromes, mental and neurodevelopmental disorders, major physical impairments, major congenital malformations, and chronic conditions—determined based on reports of disease and/or physical impairment or intellectual disability at ages 1–3 years, diagnosis of conditions or diseases, and the presence of coexisting diseases in the FA questionnaire at ages 11–13 years).
Statistical analysis
Statistical analysis was performed using STATA 14.0 (StataCorp LLC, College Station, USA), SAS 9.4 (SAS, Cary, USA) and GraphPad Prism 10.3.1 (Boston, Massachusetts, USA), with a significance level set at 5%. Results are presented as means [standard deviations] or absolute and relative frequencies (%). The primary outcome was the H/A Z-score (continuous) at ages 11–13 years, while the secondary outcomes included the BMI/A Z-score (continuous), elevated WC (>p90, categorical), and excess weight status (BMI/A>+1, categorical) at ages 11–13 years. The study model and the definition of adjustment variables for the analyses were developed based on the causal directed acyclic graph (DAG)37,38, available in the supplementary material (Figure S1).
Simple and multiple linear regression models were adjusted to investigate associations between exposure variables and continuous outcomes, considering the following covariates: type of delivery, socioeconomic status (CCEB-ABEP) at birth, and W/A classification at birth. Mean differences (MD) and their respective 95% confidence intervals (95% CI) were estimated. Simple and multiple log-binomial regression models were fitted for categorical outcomes using the same set of covariates for adjustment. Prevalence ratio (PR) and their respective 95% CI were estimated.?
RESULTS
A total of 2,753 adolescents were included, of whom 144 (5.2%) were classified in the presumed FA group and 2,609 in the NE group. The study population selection flowchart is presented in Figure 1. Table 1 describes the sociodemographic, economic, and health characteristics of the participants and their mothers/families.
The specific FA questionnaire was primarily answered by the participants’ mothers (96.5%, n=139), followed by other family members (2.8%, n=4) and the father (0.7%, n=1). A summary of the characteristics of participants in the presumed FA group is presented in Table 2. The majority reported a family history of allergic rhinitis (73.6%). Regarding the implicated foods, food dyes were the most frequently reported (32.6%), followed by cow’s milk (31.3%) and shrimp and other seafood (11.8%). All participants received a medical diagnosis based on signs and symptoms, with cutaneous reactions (82.6%) being the most reported. A total of 68.1% underwent an exclusion diet as a diagnostic test, while only 4.2% underwent an oral food challenge (OFC). Most participants are no longer on an exclusion diet (73.6%), with a mean duration of 48.2 [41.9] months. Regarding specialized care, 10.4% reported receiving or having received care from a nutritionist and 47.2% from a specialist physician (allergist and/or gastroenterologist).
Regarding the exploratory subgroup analyses of adolescents with presumed FA, 28 (19.4%) had or currently have presumed FA involving two or more foods; 45 (31.3%) had or currently have presumed FA to cow’s milk, 65 (45.1%) to other foods, and 34 (23.6%) exclusively to food dyes. Seventy-one (49.3%) participants excluded or have excluded the food allergen from their diet for more than 36 months.
The anthropometric measurements and nutritional status classification of the study participants across the three stages of the birth cohort (birth, 1–3 years, and 11–13 years) are detailed in Table S1, available in the supplementary material. Briefly, regarding height (absolute and H/A), the mean values across the three cohort stages were similar between groups. No participant in the presumed FA group was classified as having very short stature (H/A<–3), either at ages 1–3 years or 11–13 years. Only three (2.1%) participants in the presumed FA group were short (H/A<–2) at birth, one (0.9%) at ages 1–3 years, and two (1.4%) at ages 11–13 years with a frequency similar to that of the NE group.
Regarding BMI, the mean values (absolute and BMI/A) were also similar between groups at ages 1–3 years and 11–13 years, with most participants being eutrophic. Only four (3.6%) participants were classified as thin/wasted (BMI/A<–2) at ages 1–3 years and one (0.7%) at ages 11–13 years in the presumed FA group, with a similar frequency observed in the NE group. The prevalence of excess weight (BMI/A>+1) was 21.4% and 28.4% in the presumed FA and NE groups, respectively, at ages 1–3 years. By ages 11–13 years, the prevalence of excess weight increased approximately 2.2-fold in the presumed FA group (46.5%) and 1.5-fold in the NE group (42.4%). Additionally, most participants had WC>p90 at ages 11–13 years in both groups, with 55.6% in the presumed FA group and 51.2% in the NE group.
The results of the association analyses for H/A and BMI/A are presented in Figure 2. No differences were found in mean H/A or BMI/A between groups, either in the simple or adjusted regression analyses. In the exploratory subgroup analysis, adolescents with presumed FA to other foods had a significantly higher H/A than those in the NE group (simple model: MD 0.28, 95% CI 0.01; 0.54, p=0.04; adjusted model: MD 0.27, 95% CI 0.003; 0.53, p=0.04) and those with presumed FA to cow’s milk (simple model: MD 0.40, 95% CI –0.01; 0.80, p=0.06; adjusted model: MD 0.41, 95% CI 0.002; 0.81, p=0.04). Additionally, adolescents with presumed FA to other foods had a significantly higher BMI/A than those in the NE group (simple model: MD 0.38, 95% CI 0.04; 0.72, p=0.03; adjusted model: MD 0.35, 95% CI 0.008; 0.69, p=0.04), but not those with presumed FA to cow’s milk. No differences were found in the remaining comparisons. Detailed results of the analyses comparing the NE and presumed FA groups, as well as subgroup analyses by type of implicated food, duration of allergen exclusion from the diet, and number of implicated foods in presumed FA, can be found in Table S2, available in the supplementary material.
Regarding the proportion of adolescents with increased WC, no differences were found between the presumed FA and NE groups in either the simple or adjusted regression analyses. In the subgroup analysis by type of implicated food, adolescents with presumed FA to other foods had a higher prevalence of increased WC compared to the NE group (PR 1.23, 95% CI 1.02; 1.49, p=0.03); however, this difference was not maintained in the adjusted analysis (PR 1.21, 95% CI 0.88; 1.65, p=0.23). No differences were found in the remaining comparisons (Table 3).
No differences were found in the proportion of adolescents with excess weight between the presumed FA and NE groups. However, in the subgroup analysis, adolescents with presumed FA to other foods had a significantly higher prevalence of excess weight compared to the NE group (54% vs. 42%, PR 1.27, 95% CI 1.01; 1.60, p=0.04); however, this difference was not maintained in the adjusted analysis (PR 1.23, 95% CI 0.88; 1.73, p=0.22). No differences were found in the remaining comparisons (Table 3).
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DISCUSSION
To our knowledge, this is the first population-based Brazilian study to investigate the long-term growth of adolescents with FA. In this study, no differences were observed in the mean H/A Z-score between the presumed FA group and the NE group (primary outcome). Additionally, no differences were found in the mean BMI/A Z-score or in the proportions of increased WC and excess weight between groups (secondary outcomes). However, in exploratory analyses, the subgroup with presumed FA to foods other than cow’s milk had higher H/A z-scores, higher BMI/A Z-scores, and a greater prevalence of increased WC and excess weight than the NE group.
Most of the available studies have been conducted on younger children, primarily during the first years of life, and have shown a negative impact of FA on growth. For example, Costa et al39 observed lower W/A, H/A, and BMI/A Z-scores in Brazilian children with FA (median age of 10 months) compared to children without FA. Similarly, Meyer et al40 found lower weight-for-length (W/L), BMI/A, and H/A Z-scores in children with FA (median age of 23 months) in Spain, Brazil, and the Netherlands, respectively. However, long-term growth and nutritional status in school-aged children and adolescents with FA remain poorly studied.
Studies conducted in different countries that have assessed the growth of school-aged children or adolescents with FA are methodologically heterogeneous, use different references for growth and nutritional status assessment, and report conflicting results. Studies conducted in the United States, South Korea, and Italy found an association between FA and impaired growth in this age group. In a cohort of American children with persistent IgE-mediated FA, followed from early childhood to adolescence, Robbins et al15 found lower W/A and H/A Z-scores (but not BMI/A) in children with cow’s milk allergy compared to those allergic to peanuts and/or tree nuts. In school-aged Korean children, Baek et al17 demonstrated that FA and restrictive diets were associated with lower H/A Z-scores. Similarly, D’Auria et al19 found lower H/A Z-scores in Italian children with FA. In contrast, studies conducted in Canada, Slovenia, and the United Kingdom reported different findings, aligning more closely with our study. Smith et al16 observed lower H/A Z-scores in Canadian children with FA at ages 7–10 but not at ages 11–14. In Slovenia, Poredos et al18 found no differences in H/A, W/A, or BMI/A Z-scores between children with cow’s milk, egg, or peanut allergy and those without FA. In a study conducted in the United Kingdom on adolescents (11–18 years) and adults (19–65 years) with FA, Maslin et al41 found no differences in BMI compared to controls. We speculate that differences in dietary patterns and socioeconomic conditions among these countries may partially explain these discrepancies.
Regarding the effects of restrictive diets during the first year of life, Maslin et al20 found no differences in anthropometric measurements (weight, height, BMI, and WC) between children and adolescents (7 to 13 years old) in the United Kingdom who followed a cow’s milk exclusion diet and those who did not. In Japan, Mukaida et al21 observed lower weight but no differences in height among children aged 7 to 15 years who avoided egg, milk, or wheat due to FA compared to those who did not. Conversely, in Norway, Karlsen et al14 found lower weight and height at ages 1, 2, and 4 years and the current age (6 to 10 years) in children with a previous cow’s milk allergy, compared to controls. In our study, most participants were no longer on food-exclusion diets (73.6%), and most had excluded the allergenic food for less than 36 months (50.7%). This may explain why no differences in anthropometric measurements were found between groups, as developing tolerance to the allergenic food may contribute to improved growth10. Furthermore, it is important to emphasize that adequate food substitution can contribute to adequate growth10.
The impact of FA involving two or more foods on nutritional status and growth has been increasingly discussed. However, in our study, no differences in H/A Z-score, BMI/A Z-score, the prevalence of WC>p90, and excess weight were found between the NE group and individuals who excluded either one or two or more foods from their diet. In the previously mentioned study by Mukaida et al21, the authors did not find differences in weight and height based on the number, similar to our findings, or the type of foods avoided. However, when stratified children by age at allergen exclusion, children who avoided two or more foods and those who excluded cow’s milk before age three had lower height than those who excluded only one food or did not exclude cow’s milk. In our study, the H/A and/or BMI/A Z-scores in the presumed FA subgroup with other allergens were higher than in the NE and cow’s milk presumed FA subgroups. Current evidence regarding the type and number of foods avoided remains inconclusive10.
Another interesting secondary finding in our study was the high prevalence of excess weight and WC>p90 in both groups. When analyzed by type of food allergen, the prevalence of WC>p90 and excess weight was higher in the presumed FA subgroup with other allergens compared to the NE group. This may be related to unbalanced diets, poor food choices, and inadequate dietary substitutions, particularly in consuming ultra-processed foods9. Meyer et al42 emphasize that nutritional management should address “undernutrition” and “overnutrition”. Therefore, attention to diet quality and nutritional follow-up is essential, highlighting the role of the nutritionist. In our study, presumed FA to foods other than cow’s milk and food dyes exclusively may increase the prevalence of excess weight. However, more specific future investigations are needed, as the impact on growth may be more pronounced for certain food allergens, yet findings in the literature remain inconsistent10.
It is important to emphasize that children with FA should be monitored under the Brazilian National Policy for Comprehensive Child Health Care of the Ministry of Health, which aims for comprehensive, longitudinal, and multidisciplinary care. Therefore, monitoring growth, food safety, and nutritional adequacy, and referral to specialists when indicated, is essential43.
The high prevalence of allergy to food dyes observed in our study (32.6%) was unexpected, as it is rarely described in the literature5. We speculate that this high prevalence may be linked to greater exposure to ultra-processed foods (which typically contain dyes) in childhood today. In a recent cross-sectional study conducted in Brazil by Kotchetkoff et al44, which included 110 infants, preschoolers, school-aged children, and adolescents diagnosed with IgE-mediated and non-IgE-mediated FA at a multidisciplinary center, high consumption of ultra-processed foods was observed. Furthermore, an association was found between the prevalence of allergy to multiple foods and the more frequent intake of ultra-processed foods. We speculate that families may opt for ultra-processed foods due to their perceived safety in selecting allergen-free products, considering that Brazilian regulations mandate the labeling of major food allergens45. The high prevalence of presumed FA to food dyes in our study may also be explained by the self-reported nature of the diagnosis, which could overestimate the results. For example, in a Brazilian study including 9,265 children enrolled in early childhood education schools, 23.5% of infants and 17.6% of preschoolers had parent-reported FA, yet only 4% were confirmed after a medical consultation46. Additionally, only 47.2% of participants in our study received follow-up care with a specialist physician, which may have influenced the reported prevalence. Notably, only 10.4% of participants had access to a nutritionist, reflecting the challenging reality of accessing this professional in the study region. This underscores the urgent need to raise awareness among families, healthcare professionals, and public health authorities about the importance of nutritional follow-up for this population.
As limitations, we acknowledge that the diagnosis of FA was self-reported, which is why we identified it as “presumed FA.” However, to ensure the greatest possible accuracy of these reports, a specific FA questionnaire was developed by a specialist physician, discussed in collaboration with him, and all questionnaires were carefully reviewed to verify the information provided. The diagnosis of FA remains challenging47. Clinical history is considered the cornerstone of FA diagnosis1,2, while the gold standard is the double-blind, placebo-controlled food challenge (DBPCFC)2. However, its use in population-based prospective studies is difficult48. In this study, only 4.2% of adolescents reported having undergone an OFC for FA diagnosis, raising important considerations about the gap between recommended procedures and clinical practice. The OFC requires substantial resources and time availability and carries a risk of allergic reactions6, making its widespread implementation challenging. Additionally, as this study is a population-based birth cohort, the results likely represent the reality in São Paulo state, Brazil; however, they may not be generalizable to the entire Brazilian population or other countries.
Another important limitation concerns the potential selection bias due to losses to follow-up in the birth cohort. Birth cohort studies are complex and difficult to conduct, primarily due to the challenge of maintaining participant follow-up over time. To minimize follow-up losses, the fieldwork team included specific interviewers dedicated to contacting, locating, and scheduling participants. There were also communication challenges in administering the specific FA questionnaire. Notably, at least six contact attempts were made using different approaches to reduce participant losses. Additionally, the FA questionnaire was administered simultaneously or close to the cohort data collection to optimize participation. Furthermore, this study only assessed anthropometric measurements, and we acknowledge that additional analyses—such as dietary intake, diet quality, blood tests, and inflammatory markers—would have been valuable for a more comprehensive understanding of our findings.
As strengths of this study, we highlight the longitudinal follow-up of these individuals, which allows for a better understanding of the findings. Additionally, we emphasize the large number of individuals constituting the NE group, making the comparison as close to reality as possible and with the power to detect more subtle differences.
In conclusion, adolescents with presumed FA do not differ in mean Z-scores for H/A (primary outcome) and BMI/A, as well as in the proportions of increased WC and excess weight (secondary outcomes), when compared to adolescents without presumed FA in a birth cohort from a city in the state of São Paulo, Brazil. However, exploratory analyses suggested higher H/A, higher BMI/A, and a greater prevalence of increased WC and excess weight in the subgroup with presumed FA to foods other than cow’s milk compared to the NE group. Thus, our findings reinforce the importance of nutritional follow-up in this population, as nutritional monitoring and dietary guidance to support adequate growth and development. From a public health perspective, the integration of nutritionists in the care of adolescents with FA becomes a promising strategy in preventing both malnutrition and overweight/obesity in this population.
Acknowledgments
We especially thank all participants and their parents/guardians for agreeing to participate in this study, as well as the funding sources for enabling the study to be conducted and sustained over time. We would like to thank pediatric allergist Fábio André Dias for his assistance in developing the food allergy questionnaire.
Funding sources
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES – Finance Code 001), Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), and Departamento de Ciência e Tecnologia/Ministério da Saúde - Conselho Nacional de Desenvolvimento Científico e Tecnológico (DECIT/MS - CNPq).
Declaração de Disponibilidade de Dados
Os dados de pesquisa estão disponíveis mediante solicitação ao autor de correspondência.?
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