Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-19T11:41:29.171Z Has data issue: false hasContentIssue false

Complementary feeding practices and their association with adiposity indicators at 12 months of age

Published online by Cambridge University Press:  23 November 2020

Ameyalli M. Rodríguez-Cano
Affiliation:
Departamento de Nutrición y Bioprogramación, Instituto Nacional de Perinatología “Isidro Espinosa de los Reyes”, Ciudad de México, Mexico
Jennifer Mier-Cabrera
Affiliation:
Departamento de Nutrición y Bioprogramación, Instituto Nacional de Perinatología “Isidro Espinosa de los Reyes”, Ciudad de México, Mexico
Carolina Rodríguez-Hernández
Affiliation:
Departamento de Nutrición y Bioprogramación, Instituto Nacional de Perinatología “Isidro Espinosa de los Reyes”, Ciudad de México, Mexico
Ana L Allegre-Dávalos
Affiliation:
Departamento de Nutrición y Bioprogramación, Instituto Nacional de Perinatología “Isidro Espinosa de los Reyes”, Ciudad de México, Mexico
Cinthya Muñoz-Manrique
Affiliation:
Departamento de Nutrición y Bioprogramación, Instituto Nacional de Perinatología “Isidro Espinosa de los Reyes”, Ciudad de México, Mexico
Otilia Perichart-Perera*
Affiliation:
Departamento de Nutrición y Bioprogramación, Instituto Nacional de Perinatología “Isidro Espinosa de los Reyes”, Ciudad de México, Mexico
*
Address for Correspondence: Dra. Otilia Perichart-Perera, Departamento de Nutrición y Bioprogramación, Subdirección de Investigación en Intervenciones Comunitarias, Torre de Investigación, Instituto Nacional de Perinatología “Isidro Espinosa de los Reyes”, Montes Urales 800, Col. Lomas Virreyes, Alcaldía Miguel Hidalgo, Ciudad de México, Mexico. Email: otiliaperichart@inper.gob.mx
Rights & Permissions [Opens in a new window]

Abstract

Nutrition during the first 1000 days of life represents a window of opportunity to reduce the risk of metabolic dysfunctions later in life. Exclusive breastfeeding (EBF) and adequate introduction of solid foods are essential to promote metabolic and nutritional benefits. We evaluated the association of infant feeding practices from birth to 6 months (M) with adiposity indicators at 12 M. We performed a secondary analysis of 106 healthy term infants born from a cohort of healthy pregnant women. Type of breastfeeding (exclusive or nonexclusive), the start of complementary feeding (CF) (before (<4 M) or after (≥4 M)), and adiposity (body mass index – BMI, body mass index-for-age – BMI/A, waist circumference – WC, and waist circumference–length ratio – WLR) were evaluated at 12 M using descriptive statistics, mean differences, X2, and linear regression models. During the first 6 M, 28.3% (n = 30) of the infants received EBF. Early CF (<4 M) was present in 26.4% (n = 28) of the infants. Children who started CF < 4 M were less breastfed, received added sugars as the most frequently introduced food category, and showed higher BMI, BMI/A, WC, and WLR; those who consumed added sugars early (<4 M) had a higher WC. Starting CF < 4 M was the main factor associated with a higher WC at 12 M. Unhealthy infant feeding practices, such as lack of EBF, early CF, and early introduction of sugars, may be associated with higher adiposity at 12 M.

Type
Original Article
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.
Copyright
© The Author(s), 2020. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

Introduction

Nutrition during the first 1000 days of life represents a window of opportunity to reduce the risk of metabolic dysfunctions leading to obesity, diabetes, and cardiovascular diseases in later stages of life.Reference Mameli, Mazzantini and Zuccotti1,Reference Adair2 Exclusive breastfeeding (EBF) and adequate introduction of solid foods are essential to promote metabolic and nutritional benefits.Reference Andersen, Girma and Wells3,Reference Moss and Yeaton4

International recommendations clearly state that all infants should be exclusively breastfed for the first 6 months (M) of life and it is advisable to continue breastfeeding for up to 2 years.5 The benefits of EBF have been widely described in the literature, positively influencing immunological, nutritional, and clinical outcomes, and showing a reduction in the risk of developing overweight and obesity later in life.Reference Ip, Chung and Raman6Reference Yan, Liu, Zhu, Huang and Wang9

Experts recommend a timely introduction of complementary feeding (CF) between 4 M and 6 M, and the inclusion of different food groups, prioritizing iron intake and delaying the consumption of added sugars and sugary drinks until 24 M.Reference Fewtrell, Bronsky and Campoy10,11 Some studies have shown that starting CF before 4 M (<4 M) is associated with an increased risk of overweight or obesity, although others have not observed this association.Reference Adair2,Reference Burdette, Whitaker, Hall and Daniels12Reference Pearce, Taylor and Langley-Evans14 The association between the type of food initially introduced and the risk of obesity is even less clear.

Recent estimates suggest that 38.2 million infants <5 years old and more than 158 million children aged 5–19 years old are overweight or obese and it is predicted to reach 254 million by 2030.15,Reference Lobstein and Brinsden16 In Mexico, from 1998 to 2012, the prevalence of overweight and obesity in children <5 years old increasedReference Shamah-Levy, Cuevas-Nasu, Rivera-Dommarco and Hernández-Ávila17 from 7.8% to 9.7% and by 2018, 22.2% of infants 0–4 years old were at risk of overweight.18

Although not well documented, the start of CF in Mexican infants has been reported to happen around 4.3–5 M of life, where fruit is probably the most commonly offered first food.Reference González de Cosío, Escobar-Zaragoza, González-Castell and Rivera-Dommarco19,Reference Pantoja-Mendoza, Meléndez, Guevara-Cruz and Serralde-Zúñiga20 However, in Mexico, as in Latin America, it is a common cultural practice to start CF with foods that do not provide the nutrients that infants require for optimal growth and development, such as atole (sweetened rice/corn-based beverage), herbal teas, broths, fermented dairy products, and Swiss-type flavored/sweetened cheese. Likewise, mothers avoid offering foods such as citrus fruits, strawberry/kiwi, pork, chocolate, egg, beans, and “hot/cold” foods.Reference Romero-Velarde, Villalpando-Carrión and Pérez-Lizaur21 In addition, inadequate dietary practices have been documented in Mexican children.Reference Rodríguez-Ramírez, Muñoz-Espinosa, Rivera, González-Castell and González de Cosío22 It has been recently reported that 83.3% of the infants (1–4 years old) consume sugary drinks, 63.6% consume sweets, snacks, and desserts, and 48.6% consume sweetened breakfast cereals.18 The intake of added sugars in children of this age is estimated to be 40.5 g daily,Reference Sánchez-Pimienta, Batis, Lutter and Rivera23 which is excessive. On the other hand, only 48.8% of them consume fruits, 37.5% legumes, and 20.2% vegetables.18

The objective of this longitudinal study was to evaluate the association of infant feeding practices (breastfeeding, timing of introduction of CF, and starting CF with sugars) from 0 to 6 M with adiposity indicators at 12 M.

Method

Settings

This is a secondary analysis from a cohort of healthy pregnant women and their infants, which was conducted at Instituto Nacional de Perinatología “Isidro Espinosa de los Reyes” (No. 212250-49511).Reference Perichart-Perera, Muñoz-Manrique and Reyes-López24 Women’s participation was voluntary and all of them signed an informed consent. In adolescents (<19 years old), both parents and participants gave consent. Women were followed up until the end of their pregnancy and accepted that their children were nutritionally assessed during the 12 M of life.

Study population

For the purpose of this analysis, we only included data collected from healthy term infants (≥37 weeks). We eliminated data from babies whose mothers had gestational diabetes and/or preeclampsia or when nutritional/anthropometric information was missing/incomplete at 6 M and 12 M.

All clinical and sociodemographic information from the mothers such as age, parity, education level, and pregestational body mass index (BMI) were obtained from the cohort’s records. Pregestational BMI was classified as normal (18.5–24.9 kg/m2), overweight (25–29.9 kg/m2), or obesity (≥30 kg/m2) according to WHO criteria.25

Adiposity indicators

At birth, we obtained all clinical (gestational age – weeks) and anthropometric infant data (weight, length, and head circumference) from the institute’s medical record. BMI was computed and BMI-for-age (BMI/A), and length-for-age (L/A) z-scores were evaluated.

At 12 M, an experienced, well-trained nutritionist took all anthropometric measurements following the techniques described by Lohman.Reference Lohman, Roche and Martorell26 She did one-time measures of weight (1582 Baby/Mommy digital scale, Tanita Corporation of America, Inc., IL, USA), length (SECA 207 portable infantometer, SECA Corp., MD, USA), and waist circumference (WC) (anthropometric tape; Gulick II, Country Technology, WI, USA) while infants were dressed in the minimum of clothing. Waist circumference–length ratio (WLR) was computed. Sex-specific z-scores were calculated using the Anthro software v. 3.0.1 (WHO, Geneva, Switzerland). We evaluated the infants’ nutritional status as wasted (< −2 SD), normal (> −2 SD), risk of overweight (> +1 SD), overweight (> +2 SD), or obesity (> +3 SD) by means of BMI/A, according to WHO’s references.27

Feeding practices

During the follow-up visits (1 M, 3 M, and 6 M), mothers were asked about their babies feeding practices, including information regarding breastfeeding patterns and CF. Questions included whether infants were breastfed, formula-fed, or both, as well as if they had ever been fed any other food/liquid (e.g. water, juices, herbal teas, other types of milk, semi-solid, or solid food) during their first 6 M of life.

We classified breastfeeding practices during the first 6 M as (1) exclusive (EBF) or (2) nonexclusive (non-EBF). For the purpose of the study, EBF included breast milk, tap water, non-sweetened herbal teas, oral rehydration solution, drops, and syrups. Non-EBF category included infants that received any amount of formula or received both breast milk and formula or were only formula-fed. We also recorded the month when CF was started, as well as the type of food offered. We evaluated the intake of cereals, vegetables, fruits/natural juices, legumes, animal products, dairy, and added sugars. The latter category included food sweetened with table sugar, brown sugar, honey, or syrup, industrialized juices, soda, gelatin, jam, condensed milk, flavored milk, and soft/hard candy. When CF started <4 M, we classified it as early CF.

At 12 M, a 24-Hour Food Recall (24 HR) was administered to mothers in order to assess their children’s diet. We used the Food Processor SQL program (version 10.4, ESHA Research, OR, USA) to analyze the collected information, obtain the energy intake (kcal/d, kcal/kg), as well as the percentage of energy (%E) of macronutrients.

Statistical analysis

We used descriptive statistics (mean ± SD) to describe continuous variables and frequencies (n (%)) to describe categorical variables. Using Student’s t-/Mann–Whitney U tests, we evaluated differences in weight, length, BMI, BMI z-score, WC, and WLC at 0 M and 12 M between boys and girls; as well as, adiposity (BMI, BMI z-score, WC, and WLC) indicators at 12 M according to parity, start of CF and EBF. One-way ANOVA/Kruskal–Wallis was used to evaluate differences in adiposity indicators at 12 M according to mothers’ age (<18, 18–35, and >35 y), education level (basic, medium, and high), and pregestational BMI (normal, overweight, and obesity). To assess differences between categories of BMI/A (wasted, normal, risk of overweight, overweight, and obesity) at 0 M and at 12 M, we used the chi-square test. These analyses were performed using SPSS (v. 22, SPSS Statistics/IBM Corp, NY, USA).

To test the association of feeding practices with adiposity indicators (BMI, BMI/A, WC, and WLR) at 12 M, we used adjusted linear regression models. Infant predictor variables included BMI at birth, actual age (days), energy intake (kcal/kg), protein intake (as %E), sex, EBF during 6 M (yes or no), and the start of CF <4 M (yes or no). Maternal predictor variables included in the models were pregestational BMI (kg/m2), age (y), category of educational level (basic, medium, and high), and nulliparity (yes or no). A value of P < 0.05 was considered statistically significant. All models were performed using STATA software (v. 12, StataCorp, Texas, USA).

Results

Of the 263 newborns from the cohort, 233 were born at term and were eligible to follow-up. One-hundred and sixty-six mothers accepted to continue and returned with their infants for nutritional and anthropometric assessment up to 12 M (dropout rate: 28.7%). For the purpose of this analysis, we eliminated data from 60 children due to lack of nutritional information at 6 M or anthropometric assessment at 12 M (n = 54) or because they were born from mothers who developed preeclampsia/gestational diabetes (n = 6). We analyzed data collected from 106 infants.

At birth, the mean gestational age was 39.0 ± 1.1 weeks. Low birth weight was present in 12.2% (n = 12) of the newborns and only three (2.8%) weighed >3500 g. Most of them had a normal BMI/A; only one had low BMI/A. Stunting (L/A <–2 SD) was present in 38.9% (n = 37) of the infants. Boys had greater weight and length at birth and 12 M (P < 0.05). We found no differences in BMI/A, WC, nor WLR according to sex at any follow-up visit. At 12 M, most of the infants continued with a normal BMI/A, although there was an increase in infants classified at risk of being overweight and as overweight. There were no cases of obesity or differences by sex at any follow-up visit. Descriptive anthropometric data is shown in Table 1.

Table 1. Baseline anthropometric data at birth and at 12 M

Data are shown as mean ± SD; n (%). Student’s t-test, *P < 0.05, + P < 0.01; Mann–Whitney U test, # P < 0.05, $ P < 0.01.

BMI, Body Mass Index; BMI/A, Body Mass Index-for-Age; M, Months; WC, Waist Circumference; WLR, Waist circumference–length ratio.

Regarding feeding practices, 28.3% (n = 30) of the children received EBF during the first 6 M. At 12 M, only 33.3% (n = 35) continued receiving breast milk. The mean age when CF started was 4.2 ± 1.2 M; nevertheless, the earliest onset registered was 1 M. Those infants who did not receive EBF started CF earlier (3.9 ± 1.2 M vs. 4.6 ± 1.1 M; P = 0.031). We found no difference in the start of CF with food group categories according to breastfeeding classification.

In addition, 26.4% (n = 28) of the children started CF <4 M. The food category which mothers used most frequently to start CF was fruits/natural juices (72.2%, n = 70), followed by added sugars (52.6%, n = 51), and vegetables (49.5%, n = 48) (Fig. 1). Added sugars (71.4% vs. 44.9%, P = 0.025) was the most frequently introduced food category in children who started CF <4 M; meanwhile, in those who started CF >4 M, vegetables (32.1% vs. 52.5%, P = 0.043) and fruits/natural juices (57.1% vs. 78.3%, P = 0.047) categories were the most frequent (Fig. 1).

Fig. 1. Food categories used by mothers to start complementary feeding (CF) in infants.

The mean energy intake at 12 M was 1002 ± 416 kcal/d and the distribution of macronutrients was 17 ± 5% from protein, 27 ± 7% from fat, and 57 ± 9 % from carbohydrates.

At 12 M, those who received EBF showed a tendency to have a lower BMI/A (P = 0.081). No other differences were observed in anthropometric indicators at 12 M according to breastfeeding classification (Table 2). Children who started CF <4 M had a higher BMI, BMI/A, WC, and WLR (Table 2). Those who started CF early and with sugars had a higher weight (8807.0 ± 999.7 kg vs. 9486.6 ± 1226.4 kg; P = 0.007) and WC (41.1 ± 3.2 cm vs. 42.7 ± 2.5 cm; P = 0.012) at 12 M.

Table 2. Adiposity indicators at 12 M according to maternal and infant variables

Data are shown as mean ± SD. Student’s t-test, *P < 0.05; Mann–Whitney U test, & P < 0.05.

BMI, Body Mass Index; BMI/A, Body Mass Index-for-Age; M, Months; WC, Waist Circumference; WLR, Waist circumference–length ratio.

Adjusted regression linear models showed that early CF (<4 M) and energy intake (kcal/kg) influenced WC at 12 M. On the other hand, a mother’s high education level had a statistically significant effect on BMI (kg/m2). No other independent maternal–infant variables showed an effect on BMIA, BMI/A, WC nor WLR (Table 3).

Table 3. Association of maternal/infant variables and feeding practices with adiposity indicators at 12 M

BMI, Body Mass Index; BMI/A, Body Mass Index-for-Age; M, Months; WC, Waist Circumference; WLR, Waist circumference-length ratio.

Bold numbers indicate statistical significance.

Discussion

This longitudinal analysis shows important associations between feeding practices during the first 6 M of life and adiposity indicators at 12 M in Mexican infants. We observed that an early start of CF is associated with a higher WC, even after adjusting for relevant maternal and infant characteristics, including EBF exposure during the first 6 M of life. We found that added sugars are common as one of the first foods introduced in CF, especially in those who start <4 M.

The National Nutrition and Health Survey in Mexico18 showed that 28.6% of the infants receive EBF during the first 6 M and only 46.9% of the infants still received breast milk at 12 M. This data is comparable to those findings in our sample. The effect of breastfeeding on the prevention of obesity has been challenging to confirm for various reasons, including methodological issuesReference Burdette, Whitaker, Hall and Daniels12,Reference Durmusx, Heppe and Gishti28 and confounding factors.Reference Horta and Victora29,Reference Robinson, Marriott and Crozier30 Our results show a tendency of BMI to be lower in those children who received EBF during the first 6 M, but the association is lost when adjusting for confounding variables. Studies have found a lower BMI and body fat in children between 2 and 10 years old exposed longer to EBF/BF.Reference Durmusx, Heppe and Gishti28,Reference Robinson, Marriott and Crozier30Reference Hunsberger, Lanfer and Reeske32 When adjusting for maternal variables (age, pregestational BMI, education level, and parity), these associations are maintained, although their attenuation is important.

The absence of EBF has been associated with an early onset of CF.Reference Moss and Yeaton4,Reference Roess, Jacquier and Catellier33Reference Grummer-Strawn, Scanlon and Fein35 Barrera et al., found that never breastfed infants or those who stopped at <4 M were more likely (odds ratio 2.27; 95%CI 1.62–3.18) to be introduced to CF early than infants who breastfed ≥4 M.Reference Barrera, Hamner, Perrine and Scanlon36 We also observed this outcome in infants who did not receive EBF for 6 M. In addition, 25% of children started CF < 4 M, being this an inadequate practice.Reference Fewtrell, Bronsky and Campoy10,11 We found some reports showing similar prevalence, evidencing that it is still a fairly common practice. The BeeBOFT study in the Netherlands (n = 2157) found that 21.4% of infants had received early CF.Reference Wang, van Grieken and van der Velde34 Data from the Nurture study observed that almost one-third of infants had an inadequate practice (31.7%).Reference Vadiveloo, Tovar, Østbye and Benjamin-Neelon37 In a recent NHANES analysis, 16.3% of infants had an early CF introduction.Reference Barrera, Hamner, Perrine and Scanlon36

We observed that an early start of CF was associated with a higher WC. Other studies have reported a possible effect of this early start on the risk of obesity.Reference Pearce, Taylor and Langley-Evans14,Reference English, Obbagy and Wong38 However, results are still inconsistent.Reference Durmusx, Heppe and Gishti28,Reference Araújo de França, Restrepo-Méndez, Loret de Mola and Victora39 Most studies have assessed adiposity using BMI, without direct measurements of fat mass. The start of CF <4 M has been associated with a higher risk of a higher BMI between the first and second year of life,Reference Moss and Yeaton4,Reference Sun, Foskey and Allen40 greater adiposity at 7 years,Reference Wilson, Forsyth and Greene41 larger increase of subscapular skinfold thickness at 9 M in premature children,Reference Morgan, Lucas and Fewtrell42 and increased risk of overweight, obesity, and altered WC in adulthood.Reference Schack-Nielsen, Sørensen, Mortensen and Michaelsen43

A meta-analysis found that the introduction of complementary foods <4 M is associated with an increased risk of overweight or obesity (by means of BMI) during childhood.Reference Wang, Wu and Xiong44 Huh et al. analyzed this association in separate models for breastfed or formula-fed infants, finding that the risk of obesity increased in the latter and not in the former.Reference Huh, Rifas-Shiman, Taveras, Oken and Gillman45

Gingras and cols. found that starting CF < 4 M was associated with higher WC and higher trunk fat mass (measured by DXA) in school-aged children and adolescents, for both breastfed and formula-fed children (with a larger effect in the latter) and adjusted for infant and maternal variables.Reference Gingras, Aris and Rifas-Shiman46

In our study, we did not observe any associations of feeding variables (EBF, CF) with BMI. In some European countries, it has been documented that the increase in WC greatly exceeded that of BMI, leading to the assumption that the prevalence of obesity in children has been underestimated. Fredriks et al. suggest that central body fat accumulation has increased more abruptly than total body mass as a result of height and weight.Reference Fredriks, Van Buuren, Fekkes, Verloove-Vanhorick and Wit47 Therefore, the prevalence of overweight and obesity may have been underestimated, since BMI does not distinguish between fat and fat-free mass. Probably, BMI is less accurate when estimating metabolic risk than FM.Reference Araújo de França, Restrepo-Méndez, Loret de Mola and Victora39,Reference Roswall, Bergman and Almqvist-Tangen48 There is a strong correlation between total body fat and risk of obesity-related diseases in adults.Reference Flegal, Kit, Orpana and Graubard49,Reference Berrington de Gonzalez, Hartge and Cerhan50 Good correlations have been reported in school-aged childrenReference Boeke, Oken and Kleinman51,Reference Mei, Grummer-Strawn and Pietrobelli52 with weaker correlations for preschoolersReference Mei, Grummer-Strawn and Pietrobelli52 and even more for neonates.Reference De Cunto, Paviotti and Ronfani53 Within the first year of life, BMI could be limited as a surrogate for adiposity and adiposity changes.Reference Bell, Wagner and Perng54 Obesity in children (>7 years old) could be misclassified when using BMI that when using fat mass.Reference Craig, Reilly and Bland55,Reference Freedman, Ogden, Blanck, Borrud and Dietz56 The screening ability of BMI varied on the extremes of fat mass and across ethnic groups.Reference Freedman, Ogden, Blanck, Borrud and Dietz56

WC could be a better indicator for the detection of metabolic risk. WC, a simple measurement which is part of the characteristic criteria for metabolic syndrome, has been recognized as a useful marker of risk in adults, independent of BMI. It could be considered a good predictor of visceral adipose tissue, such as BMI is for subcutaneous adipose tissue, even in the pediatric population.Reference Brambilla, Bedogni and Moreno57 In children, WC has shown a good correlation with visceral adiposity.Reference Bassali, Waller, Gower, Allison and Davis58 Taylor et al. found that WC correctly discriminated children (3–5 years old) with low- and high-fat mass in approximately 90% of the cases.Reference Taylor, Williams and Grant59 On the other hand, WLR identified children (4–17 years old) with adverse cardiovascular risk factors (heart rate, LDL cholesterol, triglycerides, and total cholesterol) better than BMI.Reference Kahn, Imperatore and Cheng60 Greater gain in WC, particularly within the first 6 M and between 24 and 36 M of life, was more positively associated with blood pressure at 36 M than gains in other anthropometric measures (such as skinfolds).Reference Nowson, Crozier and Robinson61 Obese children (7–11 years old) with a WC ≥ 90° are at a greater risk of dyslipidemia and insulin resistance than obese children with WC < 90°.Reference Bassali, Waller, Gower, Allison and Davis58 These results could support the assessment of WC as a routine practice in infants in order to identify those with a higher metabolic risk.Reference Fredriks, Van Buuren, Fekkes, Verloove-Vanhorick and Wit47

Another relevant aspect for consideration is the type of food offered when starting CF. It is recommended to avoid added sugars and sugary drinks, delaying its introduction until after 2 years.Reference Fewtrell, Bronsky and Campoy10,Reference Ogata and Hayes62,Reference Gidding, Dennison and Birch63 However, a common practice in early childhood is the prompt introduction of sugar. Different studies have reported that juices and other sugary drinks are consumed frequently at this stage of life.Reference Grummer-Strawn, Scanlon and Fein35,Reference Deming, Afeiche, Reidy, Eldridge and Villalpando-Carrión64 Data from 2011 to 2014 NHANES showed that 10% of the infants (<6 M) consumed any amount of 100% juice.Reference Demmer, Cifelli, Houchins and Fulgoni65 On the other hand, the BeeBOFT study found that at 6 M, infants consumed sweet beverages daily (20.2%) or at least once a week (41%).Reference Wang, van Grieken and van der Velde34 Results from the Nurture Cohort Study indicated that 6% (0–6 M) and 38% (6–12 M) of babies were consuming juice.Reference Kay, Welker, Jacquier and Story66 In toddlers (12–24 M), according to the FITS study and 2005–2012 NHANES, juice was the second and third most commonly consumed beverage, respectively.Reference Grimes, Szymlek-Gay and Nicklas67,Reference Tovar, Vadiveloo, Ostbye and Benjamin-Neelon68

In Brazil, Dallazen found that the prevalence of introduction of sugar <4 M was 35.5% in counties with low socioeconomic status.Reference Dallazen, Silva and Gonçalves69 Our results showed that 53.6% of children started CF with some type of sugar and, if CF started early, the probability of being exposed to it was greater. It has been documented that with an early start of CF, there is an increased exposure to added sugars as age increasesReference Wang, van Grieken and van der Velde34,Reference Bournez, Ksiazek and Charles70Reference Pan, Li and Park72 and a decrease in the consumption of fruits and vegetables, among other healthy foods.Reference Grummer-Strawn, Scanlon and Fein35,Reference Nowson, Crozier and Robinson61,Reference Pan, Li and Park72,Reference Bielemann, Santos, Costa, Matijasevich and Santos73 This is of utmost relevance due to the fact that these early feeding practices are factors influencing an infant´s current and future health.

Our results showed that a higher education level is associated with BMI. Socioeconomic characteristics have been an important confounding issue when studying obesity, although mixed results have been documented. In low- and middle-income countries, such as Mexico, it has been observed that children from more educated families have higher levels of childhood obesity.Reference Dinsa, Goryakin, Fumagalli and Suhrcke74 In Brazil, Victora reported that children from the highest income families were heavier at birth and weighed 20% more than those from the lowest income families.Reference Victora, Barros, Vaughan, Martines and Beria75 On the contrary, Grjibovski did not find association between maternal education and weight-for-length z-scores at birth and at 12 M in Russian infants.Reference Grjibovski, Bygren, Yngve and Sjostrom76

We found a relatively high prevalence of stunting at birth in our sample, this could be related to the fact that birth length was obtained from the medical record, which could represent an element of bias, since neonatal measurements cannot always be performed by a well-trained professional. Subsequent data (1 M, 3 M, and 6 M) shows a prevalence of stunting below 4% (data not shown). Furthermore, the adjusted linear regression models performed in this analysis included birth weight (measured using a digital scale, requires less training) as a way of controlling for the infant’s health status at birth, where it was nonsignificant.

Among the strengths of this study, we highlight its longitudinal design. This allowed for a better definition and classification of BF exposure during the first 6 M, based on the information collected from their mothers at 1 M, 3 M, and 6 M of life. We also document the type of food introduced when starting CF, data which is very scarce in the literature. The fact that the sample is derived from a cohort, allowed to eliminate important factors associated with neonatal and infant adiposity (gestational diabetes, preeclampsia, and prematurity) and to control for confounding variables (pregestational BMI, parity, education level, birth weight, EBF, energy intake, or protein).

Some limitations of this analysis include a small sample size considering the multifactorial etiology of obesity. Although the dropout rate (28.7%) was acceptable for a long-term cohort study, there is a possibility that this could have resulted in bias. Nevertheless, we did not find any significant differences in maternal/infant (at birth) variables between those who continued and those who did not. Even though there was an association between energy intake and WC, children’s diet at 12 M was evaluated with a single 24 HR; ideally, several 24 HR are required to decrease the error due to the high variability (intra/inter) in consumption. It was not possible to define the exact time (weeks) of introduction of specific food groups in CF, it was only feasible to report if it happened before or after 4 M, with no data after 6 M.

Conclusions

We found inadequate infant feeding practices in this group of Mexican infants, such as low percentage of EBF, early start of CF, and early introduction of sugars. These practices may be associated with increased adiposity. Starting solid foods <4 M of age was associated with increased abdominal fat at 12 M. It is imperative that families receive appropriate healthy eating education and counseling during the first months of their children´s life to promote behavioral change and achieve a healthy diet from early stages.

Acknowledgments

None.

Financial support

This research received financial support from the Instituto Nacional de Perinatología “Isidro Espinosa de los Reyes” (Protocol number: 212250-49511).

Conflicts of interest

AM Rodríguez-Cano and O Perichart-Perera are speakers of the Nestlé Nutrition Institute in Mexico. There is no conflict of interest of any kind in this manuscript regarding this institution. The rest of the authors have no conflicts of interest to disclose.

Ethical standards

The authors assert that all procedures contributing to this work comply with the ethical standards of Ley General de Salud en Materia de Investigación para la Salud and with the Helsinki Declaration of 1975, as revised in 2008, and has been approved by the Institutional Review Board and Ethics Committee (reference number: 212250-49511).

References

Mameli, C, Mazzantini, S, Zuccotti, G. Nutrition in the first 1000 days: the origin of childhood obesity. Int J Environ Res Public Health. 2016; 13, 838.CrossRefGoogle ScholarPubMed
Adair, LS. How could complementary feeding patterns affect the susceptibility to NCD later in life? Nutr Metab Cardiovasc Dis. 2012; 22, 765769.CrossRefGoogle ScholarPubMed
Andersen, GS, Girma, T, Wells, JCK, et al. Fat and fat-free mass at birth: air displacement plethysmography measurements on 350 Ethiopian newborns. Pediatr Res. 2011; 70, 501506.CrossRefGoogle ScholarPubMed
Moss, BG, Yeaton, WH. Early childhood healthy and obese weight status: potentially protective benefits of breastfeeding and delaying solid foods. Matern Child Health J. 2014; 18, 12241232.CrossRefGoogle ScholarPubMed
World Health Organization. Indicators for Assessing Infant and Young Child Feeding Practices: Conclusions of a Consensus Meeting Held 6–8 November 2007 in Washington D.C., USA, 2008. World Health Organization, Genova.Google Scholar
Ip, S, Chung, M, Raman, G, et al. Breastfeeding and Maternal and Infant Health Outcomes in Developed Countries. Evidence Report/Technology Assessment No. 153 (Prepared by Tufts-New England Medical Center Evidence-based Practice Center, under Contract No. 290-02-0022). AHRQ Publication No. 07-E007, 2007. Agency for Healthcare Research and Quality, Rockville.Google Scholar
Hauck, FR, Thompson, JMD, Tanabe, KO, Moon, RY, Vennemann, MM. Breastfeeding and reduced risk of sudden infant death syndrome: a meta-analysis. Pediatrics. 2011; 128, 103110.CrossRefGoogle ScholarPubMed
Horta, BL, Loret de Mola, C, Victora, CG. Long-term consequences of breastfeeding on cholesterol, obesity, systolic blood pressure and type 2 diabetes: a systematic review and meta-analysis. Acta Paediatr. 2015; 104, 3037.CrossRefGoogle ScholarPubMed
Yan, J, Liu, L, Zhu, Y, Huang, G, Wang, PP. The association between breastfeeding and childhood obesity: a meta-analysis. BMC Public Health. 2014; 14, 1267.CrossRefGoogle ScholarPubMed
Fewtrell, M, Bronsky, J, Campoy, C, et al. Complementary feeding: a position paper by the European Society for Paediatric Gastroenterology, Hepatology, and Nutrition (ESPGHAN) committee on nutrition. J Pediatr Gastroenterol Nutr. 2017; 64, 119132.CrossRefGoogle ScholarPubMed
Secretaria de Salud. Norma Oficial Mexicana NOM-043-SSA2-2012, Servicios básicos de salud. Promoción y educación para la salud en materia alimentaria. Criterios para brindar orientación. México; 2013.Google Scholar
Burdette, HL, Whitaker, RC, Hall, WC, Daniels, SR. Breastfeeding, introduction of complementary foods, and adiposity at 5 y of age. Am J Clin Nutr. 2006; 83, 550558.CrossRefGoogle ScholarPubMed
Moorcroft, KE, Marshall, JL, McCormick, FM. Association between timing of introducing solid foods and obesity in infancy and childhood: A systematic review. Matern Child Nutr. 2011; 7, 326.CrossRefGoogle ScholarPubMed
Pearce, J, Taylor, MA, Langley-Evans, SC. Timing of the introduction of complementary feeding and risk of childhood obesity: a systematic review. Int J Obes. 2013; 37, 12951306.CrossRefGoogle ScholarPubMed
World Health Organization. Obesidad y sobrepeso. Centro de prensa OMS. 2020.Google Scholar
Lobstein, T, Brinsden, H. Atlas of Childhood Obesity, 2019. World Obesity Federation. London.Google Scholar
Shamah-Levy, T, Cuevas-Nasu, L, Rivera-Dommarco, J, Hernández-Ávila, M. Encuesta Nacional de Nutrición y Salud de Medio Camino 2016 (ENSANUT MC 2016), 2016. Informe final de resultados. Cuernavaca, México.Google Scholar
INSP, INEGI, SSA. Encuesta Nacional de Salud y Nutrición 2018 Presentación de resultados. México; 2018.Google Scholar
González de Cosío, T, Escobar-Zaragoza, L, González-Castell, LD, Rivera-Dommarco, JA. Prácticas de alimentación infantil y deterioro de la lactancia materna en México. Salud Publica Mex. 2013; 55, S170S179.Google Scholar
Pantoja-Mendoza, IY, Meléndez, G, Guevara-Cruz, M, Serralde-Zúñiga, AE. Review of complementary feeding practices in Mexican children. Nutr Hosp. 2014; 31, 552558.Google ScholarPubMed
Romero-Velarde, E, Villalpando-Carrión, S, Pérez-Lizaur, AB, et al. Consenso para las prácticas de alimentación complementaria en lactantes sanos. Bol Med Hosp Infant Mex. 2016; 73, 338356.Google Scholar
Rodríguez-Ramírez, S, Muñoz-Espinosa, A, Rivera, JA, González-Castell, D, González de Cosío, T. Mexican children under 2 years of age consume food groups high in energy and low in micronutrients. J Nutr. 2016; 146, 1916S1923S.CrossRefGoogle ScholarPubMed
Sánchez-Pimienta, TG, Batis, C, Lutter, CK, Rivera, JA. Sugar-sweetened beverages are the main sources of added sugar intake in the Mexican population. J Nutr. 2016; 146, 1888S1896S.CrossRefGoogle ScholarPubMed
Perichart-Perera, O, Muñoz-Manrique, C, Reyes-López, A, et al. Metabolic markers during pregnancy and their association with maternal and newborn weight status. PLoS One. 2017; 12(7), e0180847.CrossRefGoogle ScholarPubMed
World Health Organization. Diet, Nutrition, and the Prevention of Chronic Diseases: Report of a Joint WHO/FAO Expert Consultation, Vol. 916, 2003. World Health Organization, Geneva.Google Scholar
Lohman, TG, Roche, AF, Martorell, R. Anthropometric Standardization Reference Manual, Abridged edition, 1991. Human Kinetics, Champaign, IL.Google Scholar
World Health Organization. WHO Child Growth Standards: Length/Height-for-Age, Weight-for-Age, Weight-for-Length, Weight-for-Height and Body Mass Index-for-Age: Methods and Development, 2006. World Health Organization, Geneva.Google Scholar
Durmusx, B, Heppe, DHM, Gishti, O, et al. General and abdominal fat outcomes in school-age children associated with infant breastfeeding patterns. Am J Clin Nutr. 2014; 99, 13511358.CrossRefGoogle Scholar
Horta, BL, Victora, CG, WHO. Methodological issues. In Long-Term Effects of Breastfeeding: A Systematic Review (eds. Horta BL, Victora CG), 2013; pp. 37. World Health Organization, Geneva, Switzerland.Google Scholar
Robinson, SM, Marriott, LD, Crozier, SR, et al. Variations in infant feeding practice are associated with body composition in childhood: a prospective cohort study. J Clin Endocrinol Metab. 2009; 94, 27992805.CrossRefGoogle ScholarPubMed
Toschke, AM, Martin, RM, Von Kries, R, et al. Infant feeding method and obesity: Body mass index and dual-energy X-ray absorptiometry measurements at 9–10 y of age from the Avon Longitudinal Study of Parents and Children (ALSPAC). Am J Clin Nutr. 2007; 85, 15781585.CrossRefGoogle Scholar
Hunsberger, M, Lanfer, A, Reeske, A, et al. Infant feeding practices and prevalence of obesity in eight European countries – the IDEFICS study. Public Health Nutr. 2013; 16, 219227.CrossRefGoogle ScholarPubMed
Roess, AA, Jacquier, EF, Catellier, DJ, et al. Food consumption patterns of infants and toddlers: findings from the Feeding Infants and Toddlers Study (FITS) 2016. J Nutr. 2018; 148, 1525S1535S.CrossRefGoogle ScholarPubMed
Wang, L, van Grieken, A, van der Velde, LA, et al. Factors associated with early introduction of complementary feeding and consumption of non-recommended foods among Dutch infants: the BeeBOFT study. BMC Public Health. 2019; 19, 388.CrossRefGoogle ScholarPubMed
Grummer-Strawn, LM, Scanlon, KS, Fein, SB. Infant feeding and feeding transitions during the first year of life. Pediatrics. 2008; 122, S36S42.CrossRefGoogle ScholarPubMed
Barrera, CM, Hamner, HC, Perrine, CG, Scanlon, KS. Timing of introduction of complementary foods to US Infants, National Health and Nutrition Examination Survey 2009–2014. J Acad Nutr Diet. 2018; 118, 464470.CrossRefGoogle ScholarPubMed
Vadiveloo, M, Tovar, A, Østbye, T, Benjamin-Neelon, SE. Associations between timing and quality of solid food introduction with infant weight-for-length z-scores at 12 months: findings from the nurture cohort. Appetite. 2019; 141, 104299.CrossRefGoogle ScholarPubMed
English, LK, Obbagy, JE, Wong, YP, et al. Timing of introduction of complementary foods and beverages and growth, size, and body composition: a systematic review. Am J Clin Nutr. 2019; 109, 935S955S.CrossRefGoogle ScholarPubMed
Araújo de França, GV, Restrepo-Méndez, MC, Loret de Mola, C, Victora, CG. Size at birth and abdominal adiposity in adults: a systematic review and meta-analysis. Obes Rev. 2014; 15, 7791.CrossRefGoogle ScholarPubMed
Sun, C, Foskey, RJ, Allen, KJ, et al. The impact of timing of introduction of solids on infant body mass index. J Pediatr. 2016; 179, 104110.CrossRefGoogle ScholarPubMed
Wilson, AC, Forsyth, JS, Greene, SA, et al. Relation of infant diet to childhood health: seven year follow up of cohort of children in Dundee infant feeding study. BMJ. 1998; 316, 2125.CrossRefGoogle ScholarPubMed
Morgan, JB, Lucas, A, Fewtrell, MS. Does weaning influence growth and health up to 18 months? Arch Dis Child. 2004; 89, 728733.CrossRefGoogle ScholarPubMed
Schack-Nielsen, L, Sørensen, TI, Mortensen, EL, Michaelsen, KF. Late introduction of complementary feeding, rather than duration of breastfeeding, may protect against adult overweight. Am J Clin Nutr. 2010; 91, 619627.CrossRefGoogle ScholarPubMed
Wang, J, Wu, Y, Xiong, G, et al. Introduction of complementary feeding before 4 months of age increases the risk of childhood overweight or obesity: a meta-analysis of prospective cohort studies. Nutr Res. 2016; 36, 759770.CrossRefGoogle ScholarPubMed
Huh, SY, Rifas-Shiman, SL, Taveras, EM, Oken, E, Gillman, MW. Timing of solid food introduction and risk of obesity in preschool-aged children. Pediatrics. 2011; 127, e544e551.CrossRefGoogle ScholarPubMed
Gingras, V, Aris, IM, Rifas-Shiman, SL, et al. Timing of complementary feeding introduction and adiposity throughout childhood. Pediatrics. 2019; 144, e20191320.CrossRefGoogle ScholarPubMed
Fredriks, AM, Van Buuren, S, Fekkes, M, Verloove-Vanhorick, SP, Wit, JM. Are age references for waist circumference, hip circumference and waist-hip ratio in Dutch children useful in clinical practice? Eur J Pediatr. 2005; 164, 216222.CrossRefGoogle ScholarPubMed
Roswall, J, Bergman, S, Almqvist-Tangen, G, et al. Population-based waist circumference and waist-to-height ratio reference values in preschool children. Acta Paediatr Int J Paediatr. 2009; 98, 16321636.CrossRefGoogle ScholarPubMed
Flegal, KM, Kit, BK, Orpana, H, Graubard, BI. Association of all-cause mortality with overweight and obesity using standard body mass index categories. JAMA. 2013; 309, 71.CrossRefGoogle ScholarPubMed
Berrington de Gonzalez, A, Hartge, P, Cerhan, JR, et al. Body-mass index and mortality among 1.46 million white adults. N Engl J Med. 2010; 363, 22112219.CrossRefGoogle ScholarPubMed
Boeke, CE, Oken, E, Kleinman, KP, et al. Correlations among adiposity measures in school-aged children. BMC Pediatr. 2013; 13, 99.CrossRefGoogle ScholarPubMed
Mei, Z, Grummer-Strawn, LM, Pietrobelli, A, et al. Validity of body mass index compared with other body-composition screening indexes for the assessment of body fatness in children and adolescents. Am J Clin Nutr. 2002; 75, 978985.CrossRefGoogle ScholarPubMed
De Cunto, A, Paviotti, G, Ronfani, L, et al. Can body mass index accurately predict adiposity in newborns? Arch Dis Child Fetal Neonatal Ed. 2014; 99, F238F239.CrossRefGoogle ScholarPubMed
Bell, KA, Wagner, CL, Perng, W, et al. Validity of body mass index as a measure of adiposity in infancy. J Pediatr. 2018; 196, 168174.CrossRefGoogle ScholarPubMed
Craig, E, Reilly, J, Bland, R. Body fatness or anthropometry for assessment of unhealthy weight status? Comparison between methods in South African children and adolescents. Public Health Nutr. 2012; 16, 20052013.CrossRefGoogle ScholarPubMed
Freedman, DS, Ogden, CL, Blanck, HM, Borrud, LG, Dietz, WH. The abilities of body mass index and skinfold thicknesses to identify children with low or elevated levels of dual-energy X-ray absorptiometry-determined body fatness. J Pediatr. 2013; 163, 160166.CrossRefGoogle ScholarPubMed
Brambilla, P, Bedogni, G, Moreno, LA, et al. Crossvalidation of anthropometry against magnetic resonance imaging for the assessment of visceral and subcutaneous adipose tissue in children. Int J Obes. 2006; 30, 2330.CrossRefGoogle ScholarPubMed
Bassali, R, Waller, JL, Gower, B, Allison, J, Davis, CL. Utility of waist circumference percentile for risk evaluation in obese children. Int J Pediatr Obes. 2010; 5, 97101.CrossRefGoogle ScholarPubMed
Taylor, RW, Williams, SM, Grant, AM, et al. Waist circumference as a measure of trunk fat mass in children aged 3 to 5 years. Int J Pediatr Obes. 2008; 3, 226233.CrossRefGoogle ScholarPubMed
Kahn, HS, Imperatore, G, Cheng, YJ. A population-based comparison of BMI percentiles and waist-to-height ratio for identifying cardiovascular risk in youth. J Pediatr. 2005; 146, 482488.CrossRefGoogle ScholarPubMed
Nowson, CA, Crozier, SR, Robinson, SM, et al. Association of early childhood abdominal circumference and weight gain with blood pressure at 36 months of age: secondary analysis of data from a prospective cohort study. BMJ Open. 2014; 4, e005412.CrossRefGoogle ScholarPubMed
Ogata, BN, Hayes, D. Position of the academy of nutrition and dietetics: nutrition guidance for healthy children ages 2 to 11 years. J Acad Nutr Diet. 2014; 114, 12571276.CrossRefGoogle Scholar
Gidding, SS, Dennison, BA, Birch, LL, et al. Dietary recommendations for children and adolescents. Circulation. 2005; 112, 20612075.CrossRefGoogle ScholarPubMed
Deming, DM, Afeiche, MC, Reidy, KC, Eldridge, AL, Villalpando-Carrión, S. Early feeding patterns among Mexican babies: findings from the 2012 National Health and Nutrition Survey and implications for health and obesity prevention. BMC Nutr. 2015; 1, 40.CrossRefGoogle Scholar
Demmer, E, Cifelli, CJ, Houchins, JA, Fulgoni, VL. 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.CrossRefGoogle ScholarPubMed
Kay, MC, Welker, EB, Jacquier, EF, Story, MT. Beverage consumption patterns among infants and young children (0–47.9 months): data from the feeding infants and toddlers study, 2016. Nutrients. 2018; 10, 825.CrossRefGoogle Scholar
Grimes, CA, Szymlek-Gay, EA, Nicklas, TA. Beverage consumption among U.S. children aged 0–24 months: national health and nutrition examination survey (NHANES). Nutrients. 2017; 9, 264.CrossRefGoogle Scholar
Tovar, A, Vadiveloo, M, Ostbye, T, Benjamin-Neelon, SE. Maternal predictors of infant beverage consumption: results from the nurture cohort study. Public Health Nutr. 2019; 22, 25912597.CrossRefGoogle ScholarPubMed
Dallazen, C, Silva, SA da, Gonçalves, VSS, et al. Introduction of inappropriate complementary feeding in the first year of life and associated factors in children with low socioeconomic status. Cad Saude Publica. 2018; 34, e00202816.Google ScholarPubMed
Bournez, M, Ksiazek, E, Charles, MA, et al. Frequency of use of added sugar, salt, and fat in infant foods up to 10 months in the nationwide ELFE cohort study: associated infant feeding and caregiving practices. Nutrients. 2019; 11, 733.CrossRefGoogle ScholarPubMed
Neves, AM, Madruga, SW. Alimentação complementar, consumo de alimentos industrializados e estado nutricional de crianças menores de 3 anos em Pelotas, Rio Grande do Sul, Brasil, 2016: um estudo descritivo. Epidemiol e Serviços Saúde. 2019; 28, e2017507.CrossRefGoogle Scholar
Pan, L, Li, R, Park, S, et al. A longitudinal analysis of sugar-sweetened beverage intake in infancy and obesity at 6 years. Pediatrics. 2014; 134, S29.CrossRefGoogle ScholarPubMed
Bielemann, RM, Santos, LP, Costa, CDS, Matijasevich, A, Santos, IS. Early feeding practices and consumption of ultraprocessed foods at 6 y of age: findings from the 2004 Pelotas (Brazil) birth cohort study. Nutrition. 2018; 47, 2732.CrossRefGoogle Scholar
Dinsa, GD, Goryakin, Y, Fumagalli, E, Suhrcke, M. Obesity and socioeconomic status in developing countries: a systematic review. Obes Rev. 2012; 13, 10671079.CrossRefGoogle ScholarPubMed
Victora, CG, Barros, FC, Vaughan, JP, Martines, JC, Beria, JU. Birthweight, socio-economic status and growth of Brazilian infants. Ann Hum Biol. 1987; 14, 4957.CrossRefGoogle ScholarPubMed
Grjibovski, AM, Bygren, LO, Yngve, A, Sjostrom, M. Social variations in infant growth performance in Severodvinsk, Northwest Russia: community-based cohort study. Croat Med J. 2004; 45, 757763.Google ScholarPubMed
Figure 0

Table 1. Baseline anthropometric data at birth and at 12 M

Figure 1

Fig. 1. Food categories used by mothers to start complementary feeding (CF) in infants.

Figure 2

Table 2. Adiposity indicators at 12 M according to maternal and infant variables

Figure 3

Table 3. Association of maternal/infant variables and feeding practices with adiposity indicators at 12 M