Adiposity and feeding practices in the first two years of life among toddlers in Guadalajara, Mexico

We attended outpatient pediatric consultations at the New Civil Hospital “Dr. Juan I. Menchaca”, and at the private practices of three pediatric clinics in Guadalajara, Mexico. The purpose was to recruit toddlers between 12 and 24 months who attended a healthy-child control program and met the inclusion criteria (e.g., healthy, full-term, and birth weight appropriate for gestational age) [21]. Subsequently, we invited the mothers or legally responsible persons to participate in the study; if they chose to participate, we requested signatures indicating informed consent, and we continued with evaluations of the toddlers involved.

One hundred fifty toddlers were included, four of whom were eliminated because it was not possible to conduct BIA measurements because these toddlers removed the electrodes, and the analysis could not be continued.

BIA was performed on all participants by the same researcher using the same analyzer (Quadscan 4000, Body stat® Isla de Man) using 50-kHz measurements as follows: two electrodes were placed on the back of the right hand (at the wrist and metacarpus) and two on the dorsum of the foot (at the metatarsus and ankle). A red cable was connected to the distal electrode, and a black cable was connected to the proximal electrode. The measurements were obtained after two hours of fasting, and the state of hydration of each toddler on the previous day or factors that could affect this state (e.g., vomiting or diarrhea) were monitored with the participant in a supine position on a covered mattress free of electrically conductive materials and at room temperature [22, 23]. Adiposity values (kg and %) were obtained directly at the end of the BIA analyses; subsequently, the Z scores were calculated using kg values of adiposity and using Butte’s reference values (mean and standard deviation). To evaluate the type of feeding during the first semester of postnatal life and the introduction of CF, a questionnaire adapted from Perales [20] was used. The BF criteria were as follows: Full breastfeeding (FBF) was defined as when the infant was exclusively breastfed or predominantly breastfed during the first months of postnatal life. Exclusive breastfeeding (EBF) was defined as FBF with the administration of only additional drops or syrups of vitamins, minerals or medicines. Predominant breastfeeding (PrBF) consisted of FBF along with consumption of water, water-based drinks, juice and oral hydration, ritual liquids (herbal teas), drops or syrups of vitamins, minerals or medications. Partial breastfeeding (PBF) was considered to occur when, in addition to breastfeeding, babies received an HMS based on cow's milk or milk of vegetable origin at least once a day during the first six months of postnatal life [24].

Two 24-h dietary recalls were obtained (one during the week and the other on a weekend) by the same trained researcher [25]. The mother or caregiver of each toddler was questioned about all foods and beverages consumed during the previous 24-h period. The amount of each food or ingredient consumed was estimated using household measurements (including spoons, cups, slices, and handfuls) and food replicates. Subsequently, the energy, macronutrient and micronutrient intakes were calculated using Nutrimind software® (CDMX, Mexico). Information for both surveys was obtained directly through interviews with the mother or person in charge of feeding the toddler.

Data preparation was carried out using Microsoft Excel® for organization, error detection and to eliminate repetitive or incomplete information, and the data was later analyzed with SPSS® software (Southfield, MI).

Descriptive quantitative statistics were obtained (mean and standard deviation or median and range) considering the normality of the data distributions that were obtained with the Kolmogorov–Smirnov tests. ANOVA,> Kruskal–Wallis and Mann–Whitney U tests were used for the contrast analysis of quantitative variables. For the qualitative variables, we used frequency and percent, and for comparisons between two groups, we used chi square (X²) analyses. Afterward, linear regression tests were conducted to identify the relationships between adiposity and feeding practices during the first two years.

Informed consent was obtained from all persons who were legally responsible for the participants, and the research protocol was approved by the ethics and research committee of the New Civil Hospital of Guadalajara “Dr. Juan I. Menchaca”, with registration number 0326/19 HCJIM. The approval date was November 14, 2019.

Among all toddlers, 59% (n = 86) received full breastfeeding (FBF), 34.2% (n = 50) received PBF, and only 6.8% (n = 10) consumed HMS; most of them received a formula designed for infants. There were no differences by sex. A total of 53.4% of toddlers received exclusive breastfeeding (EBF), and even though the frequencies were higher in females than in males (57.3% vs. 49.3%, respectively), there were no significant differences. The median duration of FBF (EBF and PrBF) was six months, and for PBF was four months, with no significant differences by sex (data are not shown in the tables).

In the total studied population, the average age at which complementary foods were introduced was 5.8 ± 0.7 months. The average age at which fruits were introduced was 6 ± 1.1 months, vegetables at 6.1 ± 1.1 months, cereals at 6.9 ± 1.5 months and fortified cereals at 6.7 ± 1.6 months of age. Legumes and red meat were introduced at eight months, and chicken, fish and eggs were introduced between eight and nine months. The age at which added sugars, ultra-processed foods and natural fruit juices were introduced occurred before twelve months of age. The average age of introduction of soft drinks was 14 ± 4 months, and for processed juices, it was 12 ± 3 months. By sex, there were no significant differences in the ages at which complementary foods were introduced. (Data are not shown in the tables).

Toddlers who consumed HMS received complementary foods later than those who received full breastfeeding (FBF) or PBF. Post hoc tests showed that the age of introduction of oilseeds was earlier among those who received FBF vs. PBF. Likewise, toddlers who consumed FBF received vegetables, red meat, chicken, and oilseeds earlier than those who received HMS. Among toddlers who received PBF, vegetables, red meat, chicken, and oilseeds were introduced at earlier ages than among those who received HMS (Table 1).

At total of 61.7% of toddlers consumed sugary drinks; the most frequently consumed were juices (60%), soft drinks (13%) and fruit waters (27%). The consumption frequency was three times a week, and the median consumption amount was 55 (0–120) mL/d. Ninety-one percent of toddlers consumed ultra-processed foods, and those most frequently consumed were cookies (75%), sweet bread (22%) and sweets (8%). The consumption frequency was three times a week, and the median consumption amount was 1 (0–1) portion per day. There were no differences by sex or by type of feeding during the first semester of postnatal life. (Data are not shown in the tables).

Regarding intake by toddlers, analyzing the 24-dietary recall data during the week showed that the median energy consumption was 923 kcal/d. Regarding the macronutrient distributions, the median were 53% carbohydrates (CH), 14% proteins and 32% fats. Toddlers consumed 7 g/d of saturated fat (3–11 g/d) and 157 mg/d of cholesterol (44–305 mg/d), the sodium intake was 367 mg/d (228–589 mg/d) and the intake of added sugars was 8.5 g/d (0–24 g/d), all of which are expressed as median and interquartile range values. There were no significant differences by sex in energy, macro- or micronutrient intake for each weekday. On weekends, the 24 dietary recall data points showed that males had higher CH consumption than females (51 g vs. 49 g; p = 0.039), protein (34 g vs. 30 g, p = 0.032) and fiber (11 g vs. 7 g, p = 0.002). (Data are not shown in the tables).

After dividing the toddlers by the type of feeding they received in the first semester of postnatal life, toddlers who received HMS had higher intakes of energy, saturated fat and CH than those who received FBF or PBF (Table 2).

Girls had lower adiposity Z scores than boys (Table 3). The adiposity indicators based on the type of feeding toddlers received in the first semester of postnatal life did not show any significant differences among those who received FBF, PBF or HMS. (Data are not shown in the tables).

In the entire studied population, there was a direct relation between adiposity (%) and duration of FBF (r = 0.610, R² = 0.372, p = 0.021) with adiposity expressed as Z scores and duration of FBF (r = 0.560, R² = 0.313, p = 0.037). There were no significant relationships between adiposity and PBF duration, onset age of HMS, or feeding duration with HMS. In girls, there was a significant direct relation between adiposity (%) and FBF duration (r = 0.841, R² = 0.707, p = 0.009). For boys, there were no significant relationships. (Data are not shown in the tables).

Table 4 shows the linear regression results between adiposity and introduction of complementary foods in the entire studied population and by sex. There were different linear regression trends depending on the way in which the adiposity was expressed (e.g., kg, % or Z score). When the adiposity was expressed in %, there were more significant relations among females.

In the entire studied population and by sex, there were no significant relationships between adiposity and energy and nutrient intake on weekdays. However, when analyzing weekend days, we found that there were direct relations between adiposity (Z scores) and sugar (kcal) (r = 0.186; R² = 0.03, p = 0.024) in the entire studied population and in females (r = 0.233; R² = 0.05 p = 0.044). (Data are not shown in the tables).

We divided the toddlers by the type of feeding they received in the first semester of postnatal life; among those who received FBF or PBF, we did not find any significant relationships between adiposity (%, kg or Z score) and energy or nutrient intake. However, among those who received HMS, we found various relationships between adiposity (kg) and consumption of sugar-sweetened beverages, % of fats and % of CH. (Table 5).

In the present study, 53.4% of infants received EBF in the first six months of life, which is a higher frequency than that reported for Mexico (28.6%) [3]. The median duration of EBF and PrBF were six months, which adheres to the recommendations of the WHO [26], and the frequency of EBF adheres to the Global Nutrition Targets 2025 recommendation to increase the EBF rate by 50% during the first six months [27].

The age of CF introduction adheres to the recommended starting age of months [18, 19], and this is consistent with data obtained for Mexican toddlers by Perales [20]. When analyzing the order of introduction of food groups, it was observed that fruits, vegetables, cereals and fortified cereals were introduced at six months, which adheres to the recommendation that this group of foods should be started at the beginning of CF [28, 29]. Nevertheless, sugary drinks and ultra-processed foods were introduced before 12 and 24 months, respectively. These findings are consistent with other studies of Mexican toddlers [20, 30], and they represent a focus of attention regarding the important deviations found in the feeding habits of toddlers [26].

An interesting finding was that toddlers who received FBF (exclusive and predominant) and PBF in the first semester of postnatal life received vegetables, red meat, chicken, and oilseeds at younger ages than those who received HMS. BF is associated with healthier dietary behaviors, and mothers who offer breastfeeding are more likely to offer healthy foods [17, 31]. We did not find any significant differences between those who received FBF vs. PBF, so it seems that the effect of breastfeeding in any of its forms is a strong incentive for adequate CF.

The importance of diet from six to 24 months has been described because this period corresponds to the formation of eating habits that contribute to overall health [32]. A finding that could be a focus of attention was the consumption of ultra-processed foods from 12 to 24 months, since 91% of infants consumed one portion per day approximately three times a week. This result is consistent with the increased consumption of ultra-processed foods among Mexican children and agrees with data obtained by Perales [20] for Mexican toddlers. Consumption of ultra-processed foods before the age of two years can lead to malnutrition, as they have a higher energy density, excessive amounts of fat and saturated fat, higher concentrations of sugar and/or sodium and lower contents of fiber, protein and micronutrients [33, 34]. Another finding was that more than half of the toddlers in our study (61.7%) consumed sugary drinks three times a week, with volumes of approximately 120 mL per day. These findings agree with what has been reported in other studies [35, 36].

The energy and macronutrient intakes on weekdays and weekend days among toddlers were adequate when considering the recommendations (e.g., energy 1000 kcal/d, proteins 10%-14%, CH 45%-65% and fats 30%-40%) [32, 37]. Likewise, the consumption levels of saturated fat and cholesterol were adequate [38, 39]. However, the consumption of added sugars (8 g/d) was excessive since consumption of these substances is not recommended for children under 24 months [40].

Regarding energy and nutrient intakes according to the type of feeding in the first semester of postnatal life among toddlers aged 12 to 24 months, we found that those who received FBF had lower energy consumption levels than those who received PBF and HMS. A possible explanation could be related to appetite regulation in breastfeeding infants due to the presence of regulatory hormones present in HM [41]. Another finding of interest was that toddlers who received HMS had higher intakes of energy, saturated fat, CH and sodium than those who received FBF or PBF. These findings are consistent with those reported by Chaparro [42], who found that infants who received BF during their first year of life had healthier dietary behaviors than children who received HMS.

In the entire studied population, the adiposity values obtained by BIA (kg or percentage) were considered normal according to the reference of Butte [6]. Females had lower Z adiposity scores than males (p = 0.05). A possible explanation could be that in Mexico, malnutrition syndrome is more frequent in females, with important epidemiological and socio-anthropological implications, due to a potential discriminatory effect toward the female gender [43]. In contrast to this finding, it has been reported that females have more adiposity than males, which persists throughout life [44, 45].

There were no significant differences in adiposity according to the type of feeding that the studied toddlers received in the first semester of postnatal life. A possible explanation could be that changes in adiposity according to the type of feeding they received (e.g., FBF, PBF or HMS) occurred in a more significant manner in the first six months of life [11, 14]. Infants receiving BF appeared to have increased fat mass at 2, 4, and/or 6 months of age [11, 14], and BF is likely to protect infants with greater increases in fat mass in the first six months of life vs. infants who received HMS [11]. In addition, it has been stated that in the first months of life, higher fat mass could be part of an optimal phenotype influenced by BF, which could be related to protection against obesity development in later life stages [14, 15].

In the study sample, there was a direct relationship between adiposity and FBF duration. This could indicate that the longer the BF duration, the higher the adiposity in toddlers aged 12–24 months, which could be explained simply by changes in adiposity as toddler ages increase [8]. Alternatively, BF infants have been shown to have significant increases in fat mass accumulations during the first six months. However, these accumulations decrease or disappear after six months and tend to reverse at 12 months of age [8, 14, 44]. In contrast to this finding, an inverse relationship has been reported between BF duration and the indicators of adiposity and obesity [9, 10, 46‐48]. This could be because breastfeeding plays a protective role against the development of obesity due to the presence of hormones in human milk that are responsible for regulating appetite [41].

In females, there was a direct relationship between adiposity and FBF duration, while in males, there was no significant difference. Similar to this finding, it has been reported that there are more associations among females between BF and variables related to adiposity [46]. It is not clear why this relationship is stronger in females than in males. However, one possible explanation is that the effects of hormones that are potentially involved in the metabolic effects of BF in infants could be influenced by sex [46].

We did not find any relationships between adiposity and age of CF introduction. This finding is consistent with that reported by Rodríguez [14] since they did not report a relationship between CF and fat mass. A possible explanation could be that the age of CF introduction adhered to the recommendations and that there were no early introductions (before four months). These findings reaffirm the behavior of avoiding early CF introduction because it is associated with higher adiposity and a higher risk of overweight or obesity in later life stages [49‐52]. Interestingly, for females, there were inverse relationship between adiposity and the ages at which eggs, fish, and cheese were introduced. Proteins play a role in body composition, and it has been stated that high protein intake in childhood could increase the plasma and tissue concentrations of insulinogenic amino acids and the growth mediators of insulin and IGF-1, increasing adiposity [53].

In the entire studied sample and especially in males, there was relationship between adiposity and the age at which yogurt with added sugars was introduced. This finding emphasizes the importance of avoiding ultra-processed foods for different reasons during the first year of life; for example, the negative impact they have on adiposity, the development of obesity or other chronic-degenerative diseases and the development of inadequate food preferences and eating habits [54].

Another interesting finding was that we found a relationship between adiposity and the amount of added sugar consumed; therefore, this reaffirms that added sugars should be avoided in children under two years of age [40] because they increase the risk of obesity and other adverse health effects [54].

We found that infants who received HMS in the first semester of postnatal life exhibited various relationships between adiposity and the consumption of sugar-sweetened beverages, lipids, saturated fat, cholesterol and added sugars. Therefore, our study confirms that BF could contribute to the development of healthy eating behaviors, with a medium-term effect on food choices and food intake and consequently on adiposity [6, 9].

The main strength of this study was the analysis of adiposity using BIA since its determinations in the pediatric field have become very relevant due to the increasing prevalence of obesity in the early stages of life and its adverse effects on health. The second strength is that the age group we included (toddlers aged 12–24 months) because to date, there are few studies that include toddlers in analyses of adiposity by using BIA measurements. A limitation of this work was the cross-sectional study design because we could not analyze the changes in adiposity from 12 to 24 months of age and because we could not know the protective factors for obesity regarding feeding practices in the first two years of life. Another limitation was that in some cases, type II errors could occur since the group of toddlers that belonged to the HMS group was the smallest. Another limitation was that we did not assess maternal factors such as pre-pregnancy BMI, weight gain during pregnancy, or current maternal factors such as diet, physical activity, and their impact on infant feeding, which could help to understand the origins of obesity.