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Intrauterine growth restriction and sugar consumption at two years of age in the BRISA cohort

BMC Pediatrics volume 25, Article number: 305 (2025) Cite this article

Abstract

Background

Alterations in insulin sensitivity in the fetus during pregnancy have been associated with IUGR and future increases in sweet food cravings.

Objective

To analyze the association between intrauterine growth restriction (IUGR) and sugar consumption at two years of age in the BRISA cohort.

Methods

Data from the pre-natal study and the follow-up of the BRISA cohort in the second year of life were used. The outcome assessed was sugar consumption, using three indicators: total energy from sugars, total grams of sugars and % of energy from sugars, analyzed continuously using a 24-hour recall (24 h). The exposure was IUGR, assessed as p50 and defined by the birth weight ratio (KRAMER et al., 1988), calculated by dividing the weight of the newborn by the weight corresponding to the 50th percentile of the birth weight for gestational age curve. To analyze the relationship between sugar consumption and IUGR, a propensity score based on the Inverse Probability of Treatment Weighting (IPTW) for continuous treatment was used. To minimize the bias due to loss to follow up, the sample was weighted by the inverse of the probability of selection.

Results

A total of 553 mother-infant pairs were analyzed. The mean birth weight was 3,291 g, with an IUGR rate of 15.19%. There was no association between IUGR and the percentage of energy intake that was derived from sugars. It was observed that infants without IUGR had a lower total energy intake of sugars (β: -11.29; 95%CI: -21.19; − 1.19) and a lower total gram intake of sugars (β: -1.89; 95%CI: -3.48; − 0.30).

Conclusion

IUGR infants had higher sugar intake at two years of age than non-IUGR infants, which means fetal growth restriction can affect eating behavior in later life, leading to the choice of highly palatable, energy-rich foods.

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Introduction

Intrauterine growth restriction (IUGR) is characterized as a pathological condition in which the fetus has a growth rate lower than its normal potential for its gestational age [1]. This condition is considered a public health problem that predominates in low- and middle-income countries, where it affects up to 25% of pregnancies, while in developed countries it occurs in 3 to 9% of pregnancies [2].

The reduction in fetal growth occurs mainly due to placental dysfunction and restriction of nutritional supply to the fetus [3]. From a metabolic point of view, nutritional deficiency induces the development of adaptive mechanisms by the fetus to ensure the maintenance of its basal metabolic functions and survival [4]. These mechanisms include the increased production of glucose and altered sensitivity to insulin, prioritizing the supply of glucose to vital organs such as the heart and brain [4, 5]. These changes can lead to long-term consequences such as obesity, type 2 diabetes mellitus, metabolic syndrome and insulin resistance [6].

Studies carried out on animal models and children have highlighted the mechanisms that may explain the relationship between IUGR and increased consumption of sweet foods [7,8,9,10,11,12]. Children and adults with IUGR have shown more impulsive behavior, poor inhibitory control and a modified hedonic response (taste reactivity) to palatable foods, i.e. those high in sugars and/or fats [9, 13,14,15].

A study carried out with 150 four-year-old children in Canada examined whether the 7R (seven-repeat hypofunctional allele) is associated with total caloric intake and/or food choices in preschoolers, suggesting that previous associations between the 7R allele and overeating/obesity in adults may stem from food choices observable in preschool years [16].

Another study, carried out by Silveira et al., investigated whether a multilocus genetic score reflecting dopamine (DA) signaling capacity is differentially associated with the spontaneous intake of palatable foods in children, according to fetal growth status, and found that variations in a genetic score reflecting DA signaling are associated with differences in sugar intake only in children with IUGR, which suggests that DA function is involved in this behavioral trait in these children [15].

There is evidence that IUGR leads to increased preference and impulsivity for sugary foods through altered reward sensitivity and decreased sensitivity of brain systems to hedonic control [9, 11, 17].

However, few studies have investigated spontaneous sugar consumption in children born with IUGR. The aim of this study is to analyze the relationship between IUGR and sugar consumption at two years of age in a birth cohort.

Methods

Study design and sampling

This is a longitudinal, population-based epidemiological study carried out with pre-natal data from the second year of follow-up of the study Brazilian Ribeirão Preto and São Luís Birth Cohort Studies (BRISA), which investigates risk factors for pre-term birth and its consequences throughout life in two Brazilian cities (Ribeirão Preto and São Luís) [18]. The details of the population, sample selection and site characterization were published previously [18, 19]. For this study, data from the São Luís pre-natal care cohort, which began in 2010, were used, with a convenience sample of 1,447 pregnant women who were assessed at 22 to 25 weeks of gestational age. Of these, 1,381 were monitored at birth (2010/2011) and 1,151 children were assessed in 2012/2013 [18].

For the analyses of this study, observations that did not have answers in the outcome, exposure and complementary variables were excluded from the sample, so the final analytical sample included 553 mother-infant binomials.

Data collection

Data were collected at three different times: prenatally, at birth and at two years of age. In the prenatal stage, pregnant women were contacted at ultrasound services and prenatal clinics and invited to take part in the research, then interviewed using a structured questionnaire, and the newborns were assessed. The follow-up was carried out when the children were two years old, in 2012/2013.

Intrauterine growth restriction (IUGR)

For this study, the birth weight of the newborn was divided by the weight corresponding to the 50th percentile of the birth weight for gestational age curve on the Kramer index [20]. IUGR was defined as the birth weight ratio lower than 0.85, which means that the fetus had a growth rate lower than its normal potential for gestational age.

Consumption of sugar at the age of two

Sugar consumption at the age of two was assessed using the 24-hour Dietary Recall Survey (24 h), which helped obtain verbal information about the children’s food intake in the 24 h preceding the interview. The 24 h was applied by trained interviewers, who surveyed mothers about their children’s food consumption in detail, also gathering information related to preparation and quantification in household measures [21]. The interviews were conducted in person or via telephone. Usually, the first dietary assessment was conducted in person and the second or third ones could be via telephone or in person.

Children who had atypical food intake on the day before the 24 h was applied were excluded from the study, as were mothers who refused to take part in the study. Food intake was considered atypical based on a negative answer to the question “Was the child fed normally yesterday?”

The frequency of sugar consumption was calculated as the sum of daily intake of the following foods: soft drinks, industrialized juice, chocolate drinks, chocolate candy, cakes, candies, sweets and cookies, dichotomized into as 0–2 times/day, 3–4 times/day, and ≥ 5 times/day. We collected information on some industrialized products from the packaging when these were not available in the table or in the nutri-plus virtual software. For the conversion of household measurements, we used the household measures by Pinheiro et al. [22]. Three indicators were evaluated for sugar consumption: total energy from sugar, total grams of sugar and % of energy from sugar, all analyzed continuously.

Complementary variables

The variables were obtained using validated and standardized questionnaires administered to mothers in the first 24 h after childbirth. The following complementary variables were considered: sex of the child (male or female); mother’s age (< 20 years, 20–34 years or ≥ 35 years); mother’s skin color (white/yellow/oriental, brown/mixed-race or black); mother’s schooling (0 to 8 years, 9 to 11 years or 12 years or more); mother’s occupation (manual worker, non-manual worker or does not work) and socio-economic classification, assessed according to the Brazilian Economic Classification Criteria of the Brazilian Association of Research Companies (classes A/B, C or D/E, with A/B being the most favored and D/E the least favored) [23]. In addition, the factors type of birth (cesarean or vaginal); hypertension during pregnancy (yes or no); diabetes during pregnancy (yes or no); alcohol consumption during pregnancy (yes or no); smoking during pregnancy (yes — if the mother consumed at least one cigarette a day — or no); number of children (continuous); pre-pregnancy body mass index (BMI) (malnutrition, eutrophy, obesity or overweight) and birth weight (grams) were assessed.

Data analysis

A directed acyclic graph (DAG) was created using the DAGitty program (Fig. 1), which identified the minimum set of adjustment variables, selecting the following ones: socioeconomic classification; alcohol consumption and smoking during pregnancy; gestational diabetes and hypertension; maternal skin color; schooling; age and occupation; pre-pregnancy BMI; sex of the child; number of children and type of birth. The DAG serves as a visual depiction of causal assumptions, presenting an overview of the causal research question and its context. When a DAG contains all relevant variables and their causal relationships, it enables the identification of the presence of ‘confounding.’ Confounders are factors associated with both the exposure and the outcome, but are not in the causal path between them. Thus, considering these covariates in the analysis phase eliminates confounding and some forms of selection bias.

Fig. 1
figure 1

Directed Acyclic Diagram (DAG) of the relationship between IUGR and sugar consumption. IUGR: Intrauterine growth restriction

Full size image

Descriptive analyses were carried out with estimates of absolute and relative frequencies, mean and standard deviation.

Due to the losses to follow-up, the sample was weighted by the inverse of the probability of selection. All the variables were compared by applying the chi-square test to the children who were seen in the second follow-up and those who were not. The probability of the child attending the second follow-up appointment was calculated using a logistic regression model. The inverse of the probability of selection was then calculated in order to minimize spurious associations resulting from sample losses and used to weight the estimates of the model.

To analyze the relationship between IUGR and sugar consumption (total energy from sugar, total grams of sugar and % of energy from sugar), a propensity score was used based on the Inverse Probability of Treatment Weighting (IPTW) for continuous treatment. Lastly, a sensitivity analysis was carried out to determine how fragile the estimated effect could be in relation to unobserved confounding. For the sensitivity analysis, the Omitted Variable Bias (OVB) criterion was used, in which the Robustness Value (RV) and the proportion of variation in the result explained exclusively by the treatment—R2—are taken into account [24, 25].

Statistical analysis was carried out using the R program version 4.0.3 (The R Foundation for Statistical Computing).

Ethical aspects

The project was approved by the Research Ethics Committee of the UFMA University Hospital under substantiated opinion no. 223/2009, protocol 4771/2008-30, and met the criteria of Resolution 196/1996 of the National Health Council and its complementary regulations. The interviewees were invited to take part in the survey. Upon agreeing, they signed the Informed Consent Form (ICF).

Results

A total of 553 mother-infant binomials were analyzed. The mean birth weight was 3,291 g and 15.19% of births presented IUGR. In relation to sugar consumption, the mean from Total energy from sugar was 69.67 (± 84.74), total grams of sugars 11.78 (± 14.33) and percentage of energy from sugars 6.11 (± 7.78). The births were by cesarean section in 50.45% of cases, and 50.81% of the infants were female (Table 1).

The mean age of the women was 26.52 (± 5.43) years, 49.37% did not work and 77.03% had nine to eleven years of schooling. A total of 67.63% of the study population identified as brown/mixed-race and 69.08% belonged to economic class C (Table 1).

The number of women who experienced hypertension during pregnancy was 8.32%, 3.44% of the women suffered from gestational diabetes and 68.72% were classified as eutrophic for their pre-pregnancy BMI. During pregnancy, 22.78% of the women consumed alcohol and 3.44% smoked (Table 1).

Table 1 Characterization of the study sample. BRISA Birth Cohort - São Luís, Maranhão, Brazil, 2011–2012
Full size table

Table 2 shows the crude and adjusted analyses of the association between IUGR and the different indicators of sugar consumption. No association was found between IUGR and the percentage of energy intake that was derived from sugar. However, there was an association between IUGR and the total energy from sugar and the total grams of sugar in both the crude and adjusted analyses. The adjusted analysis showed that children with a higher p50 (birth weight ratio) had a lower sugar intake expressed as total energy from sugar (β: -11.29; 95%CI: -21.19; − 1.19) and a lower sugar intake expressed as total grams of sugar (β: -1.89; 95%CI: -3.48; − 0.30).

Table 2 Crude and adjusted analysis of the relationship between IUGR and sugar consumption
Full size table

According to the sensitivity analysis, the R2 value is lower than the Robustness Value (RV), so it can be said that these confounding factors do not explain the observed effect (Table 3).

Table 3 Sensitivity analysis of the relationship between IUGR and sugar consumption at two years of age
Full size table

Discussion

There was an association between IUGR and total energy from sugar and total grams of sugar. No association was found between IUGR and the percentage of energy intake that was derived from sugar.

IUGR leads to a decrease in the action of receptors located in the nucleus accumbens and ventral pallidum, reducing the sensitivity of hedonic systems [9, 26]. Thus, IUGR is inversely related to the hedonic response to sweet taste, which leads to a decrease in sensitivity to the pleasure caused by sweet foods and induces greater consumption of these foods [9].

The results of this study are in line with those of other papers [9, 27] that have shown that individuals with IUGR, when compared to individuals without IUGR, do in fact make specific dietary choices at different times of their lives, most of which are foods rich in carbohydrates or sugar.

A study by Shultis and colleagues (2005) evaluating the association between birth weight and childhood diet, carried out in the south west of England, based on a subgroup of children from the Avon longitudinal study of parents and children (ALSPAC), aged 8, 18, 43 months and 7 years, showed that there was an association between birth weight and the diet of children aged 8 to 43 months, but not those aged 7 years. Fat intake was inversely associated with birth weight, and carbohydrate intake was positively associated with birth weight at 43 months of age [28]. It is important to note that although IUGR determines low birth weight [29], the two terms refer to different conditions, since not every fetus that has suffered from IUGR is born small for gestational age (SGA) [2]. Small for gestational age (SGA) infants are those whose birth weight is below the 10th percentile of birth weight for gestational age, while IUGR is a pathological condition of fetal deprivation that causes the fetus not to reach its growth potential [2, 30].

A study carried out with newborns with a gestational age of 25 to 29 weeks on the first day of life evaluated their hedonic response after administering a sucrose solution orally, showing a negative correlation between the degree of IUGR and the positive reaction to the sweet taste [9].

Another study carried out with 24-year-old individuals from a Brazilian birth cohort showed a higher carbohydrate intake in women born with severe IUGR. In addition, a continuous association was found between IUGR and a predilection for carbohydrates in adulthood [13]. However, it is worth noting that this study analyzed the consumption of simple and complex carbohydrates in a generalized way, unlike the present study, which specifically investigated the consumption of added sugar, a type of simple carbohydrate.

Despite the difference in the ages assessed in the various studies described above, they all tend towards the same conclusion: there is an increase in the consumption of palatable foods in individuals with IUGR and a small-for-gestational-age (SGA) birth weight.

This relationship between IUGR and the consumption of palatable foods can be explained by the “thrifty phenotype hypothesis,” which states that fetuses become accustomed to a deficient supply of nutrients, which can lead to changes in physiology, body systems or the metabolism, in addition to altering the sensitivity of tissues, resulting in abnormal structure and function in adulthood [31].

The results of this study showed that intrauterine growth is related to the hedonic response to sweets in children aged two years. Hedonic programming, when related to the intake of palatable foods, is considered to be one of the mechanisms that explain people’s different food choices at older ages [9, 12].

In addition, there is evidence that IUGR affects the mesolimbic dopamine reward pathway in adult rats, which leads to reduced levels of dopamine receptor in the nucleus accumbens and, consequently, favors the preference for highly palatable foods, high in sugars and fats [12]. In a prospective cohort study composed of Brazilian adolescents, participants who were born small-for-gestational age had a higher snack caloric density and this eating behavior was associated with insulin sensitivity and changes in the hippocampus. Insulin modulates the central dopaminergic response, which is related to reward sensitivity [32]. Therefore, the change in insulin sensitivity in these neural pathways due to restriction can modify behavioral responses [11, 17].

Impulsivity and poor inhibitory control also seem to play an important role in altered eating behavior in children with IUGR [14, 33]. This increased impulsivity in IUGR children is not limited to eating behavior and affects other aspects of decision-making and inhibitory control processes [34]. A study conducted by Silveira et al. (2012), which evaluated impulsivity in the thrifty phenotype among three-year-old Canadian children, found, in girls with a history of IUGR, a lower capacity to delay the response to food impulses, which could indicate a relationship between IUGR and food preferences in girls. Given the young age of the children, the study suggests that the change in eating patterns due to IUGR is probably not secondary to metabolic effects, but instead that the altered eating behavior would subsequently lead to metabolic changes such as obesity and resistance to insulin and leptin [9, 14]. Thus, corroborating previous studies [14, 17], the young age of the children in the present study also suggests that IUGR programs eating behavior in children independent of their metabolism.

One of the strengths of this study is that it was longitudinal and sought to assess the effect of IUGR and sugar consumption at two years of age. To date, this is one of the few studies to assess this association in this age group. Data were collected and analyzed rigorously, and the use of the DAG made it possible to identify potential confounding factors, colliders and mediating variables, reducing the likelihood of confounding or selection bias. The use of propensity score as a method of analysis can be considered another positive aspect of the study, as it made it possible to balance the covariates observed between the exposed and unexposed groups, in an attempt to bring an observational study closer to an experimental one. Balancing the distribution of covariates is possible by randomizing the individuals in the groups.

Limitations include loss to follow-up leading to a small sample size. However, the sample was weighted by the inverse of the probability of selection, minimizing the existence of possible spurious associations resulting from these losses. Another limitation may be related to the use of a single 24 h, which can under- or overestimate individual food consumption, since this questionnaire is based on habitual eating patterns and may reflect availability and convenience rather than real preferences, thus not accurately portraying children’s real eating habits. Additionally, the age at which food consumption was assessed in this study may become a limitation, since at this age food intake is greatly influenced by parental behavior, based on the assumption that parents of children with IUGR could feed their babies differently to encourage them to grow up [35, 36]. Lastly, as mentioned before, although there is a similarity between the definitions of SGA and IUGR, they refer to different conditions. Thus, another limitation of this study is that IUGR was defined by birth weight, which may lead to an overestimation of IUGR among SGA fetuses and an underestimation of IUGR among appropriate for gestational age (AGA) fetuses [2]. However, in the absence of other available indicators (such as ultrasound measurements), birth weight has been consistently used to define IUGR in studies, including ours [37].

In conclusion, fetal growth restriction can affect feeding behavior in children at two years of age, leading to higher sugar intake in IUGR infants than in non-IUGR infants. Thus, it is important to develop further studies to better understand the mechanisms of early events that lead to specific behavioral preferences, as well as to establish the validity of preventive measures to improve the intrauterine environment and thus reduce the risk of obesity in childhood.

Data availability

The data that support the findings of this study are available from e-mail rosangela.flb@ufma.br , but restrictions apply to the availability of these data, which were used under license for the current study, and so are not publicly available. Data are however available from the authors upon reasonable request and with permission of Rosangela Fernandes Lucena Batista.

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Acknowledgements

We thank the mothers participating in the project, who, by answering all questionnaires, allowed us to obtain all the information for accomplishing this research; the funding institutions that provided the resources for developing this research; and the graduate program in Collective Health of the Federal University of Maranhão for making the data of this research available.

Funding

This research was funded by the Support Program for Centers of Excellence (Pronex); National Council for Scientific and Technological Development (CNPq); Maranhão Research Foundation (FAPEMA); São Paulo Research Foundation (FAPESP).

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Authors and Affiliations

  1. Collective Health Post-graduate Program, Universidade Federal do Maranhão, São Luís, Maranhão, Brazil

    Liliana Yanet Gómez Aristizábal, Juliana Ramos Carneiro, Cecilia Claudia Costa Ribeiro, Rosângela Fernandes Lucena Batista, Maria Teresa Seabra Soares de Britto e Alves, Vanda Maria Ferreira Simões & Antônio Augusto Moura da Silva

  2. Collective Health Post-graduate Program, Universidade do Extremo Sul Catarinense, Criciúma, Santa Catarina, Brazil

    Susana Cararo Confortin

  3. Universidad CES, Escuela de Graduados. Medellín, Cl 10A #22 – 04, Medellín, Antioquia, Colombia

    Liliana Yanet Gómez Aristizábal

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Contributions

LYGA: conception, design, and analysis of the data, interpretation of the results, writing and revision of the manuscript, and relevant critical review of the intellectual content. SCC: interpretation of the results, writing and revision of the manuscript, and relevant critical review of the intellectual content. JRC: interpretation of the results, writing and revision of the manuscript, and relevant critical review of the intellectual content. CCR: conception and writing and revision of the manuscript, relevant critical review of the intellectual content. RFLB: relevant critical review of the intellectual content and revision of the manuscript. MTSSBA: relevant critical review of the intellectual content and revision of the manuscript. VMFS: relevant critical review of the intellectual content and revision of the manuscript. AAMS: conception and design, interpretation of the results, writing and revision of the manuscript, and relevant critical review of the intellectual content.

Corresponding author

Correspondence to Liliana Yanet Gómez Aristizábal.

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Ethics approval and consent to participate

The project was approved by the Research Ethics Committee of the UFMA University Hospital under substantiated opinion no. 223/2009, protocol 4771/2008-30, and met the criteria of Resolution 196/1996 of the National Health Council and its complementary regulations. The interviewees were invited to take part in the survey. Upon agreeing, they signed the Informed Consent Form (ICF).

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This section is not applicable for this paper.

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The authors declare no competing interests.

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Gómez Aristizábal, L., Confortin, S.C., Carneiro, J.R. et al. Intrauterine growth restriction and sugar consumption at two years of age in the BRISA cohort. BMC Pediatr 25, 305 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12887-025-05448-4

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Keywords

BMC Pediatrics

ISSN: 1471-2431

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