Artigos

Introduction
In recent decades, technological advances in caring for preterm neonates with very low birth weight or other clinical conditions have significantly increased children’s survival during hospitalization.1 The current challenge focuses on reducing the morbidities these children can develop in the short and long term, especially those related to feeding.2
The current infant feeding setting portrays that the eating habits of children born full-term or not are still below ideal,3,4,5 and seem to follow the trend of the general Brazilian population. During the last few years, a decline in the consumption of fresh and minimally processed foods and healthy culinary preparations and a significant increase in the participation of ultra-processed food products (UPF)6 have been observed in Brazil, especially among households with low socioeconomic status.7 More specifically for children under five, the National Survey of Children’s Food and Nutrition (ENANI) showed a high prevalence of UPF consumption and no consumption of fruits and vegetables.5 A report published by UNICEF8 evidenced that this setting worsened during the Covid-19 pandemic among households receiving cash transfer programs with children under six.
UPF are industrial formulations manufactured from substances derived from foods and additives, with minimal amounts of whole foods9. Research worldwide has showed associations between UPF consumption with dietary nutrient profiles related to an increased risk of obesity and non-communicable diseases in adults10 and children.3,11
Especially during the critical phase of the pandemic, international and national reports have highlighted the severity of the overlap between the economic and health crises, with a sharp increase in food insecurity cases in several regions of the world, especially from 2019 to 2020.12
This period was also marked to reduce the risk of Covid-19 transmission by interruptions or reduced coverage of various food and nutrition programs, such as the school feeding program, and the restriction of non-essential services, access to schools, and outpatient health services. These strategies were necessary to decrease the risk of Covid-19 transmission when the coronavirus vaccine regimen had not yet been initiated.13 In this regard, clinical and nutritional care in follow-up services also had to be restricted.
We should add that, even before the pandemic, studies conducted with premature infants or other NICU children have shown that this public also has inadequate eating habits, especially in the first two years 3,14. The early introduction of sugar and UPF, especially wheat-based foods, insufficient breastfeeding time, and early introduction of cow’s milk and dairy products are some examples.
Given the poor dietary quality established among children discharged from Neonatal Intensive Care Units (NICUs) and the potential deterioration of the feeding situation due to restricted food and health access, we aimed to assess the association between feeding practices and household food insecurity status (HFI) during the Covid-19 pandemic among children discharged from the NICU.

Methodology
Population and study design
This cross-sectional study was conducted in a non-probability sample of children from Neonatal Intensive Care Units (NICU), aged between 1 and 9 years, assisted in three high-risk follow-up outpatient clinics in reference health units located in Rio de Janeiro: Fernandes Figueira Institute (IFF/Oswaldo Cruz Foundation), Gaffrée e Guinle University Hospital (HUGG/ Federal University Hospital of the State of Rio de Janeiro), and Pedro Ernesto University Hospital (HUPE/University of the State of Rio de Janeiro).
This study classified children born below 37 weeks of gestational age and full-term infants returning from the NICU as high-risk. Those with conditions that interfered with anthropometric assessment (edema, anasarca, limb amputation, hydrocephalus, and dehydration) or with feeding (severe malformations, chromosomal disorders, chronic non-progressive encephalopathy, or severe neuropathy) were excluded.
The data were collected from August 2020 to June 2021, the critical period of the Covid-19 pandemic. The vaccination scheme was still incipient, only intended for adults, and outpatient care was restricted to avoid crowding and the increased virus spread risk. All children assisted in the three centers in this period and met the eligibility criteria were included in this research, so the sample size was not calculated. The Research Ethics Committee of the Federal University of the State of Rio de Janeiro approved the study under Protocol n° 4593341). The Informed Consent Form or the Informed Assent Form was obtained from each guardian or participant.

Data collection
Children’ socioeconomic, demographic, and dietary data, and households’ socioeconomic and demographic data were collected during interviews with parents/caregivers using a structured questionnaire by the researcher and his team. Clinical data regarding the neonatal period were collected from the children’s medical records. The maternal and head of household educational level and ownership/availability or access to goods and services.15 We also assessed whether family budget changes impacted food purchase during the pandemic through specific questions (1- Has your household income been affected during the pandemic? 2- If so, was there a lack of money to buy food in your home?) and those already included in the Brazilian Food Insecurity Measurement Scale (BFIMS).
Anthropometric measurements of weight and height by trained health professionals from each of the outpatient clinics of the tertiary health care units were collected to evaluate the nutritional status. The z scores of anthropometric indicators, body mass index for age (BMI/A), and height for age (H/A), were calculated from these data. The nutritional status of children was classified per the growth curves of the World Health Organization.16,17 Gestational age at birth was estimated from the last menstrual period (LMP) date, considering the interval, in weeks, until the delivery date. Gestational age at birth estimated the child’s correct age until two years of chronological age.
Regarding birth weight adequacy, children born with a weight below the 10th percentile were considered small for gestational age (SGA), those with a weight between the 10th and 90th percentiles were adequate for gestational age (AGA), and those with a weight above the 90th percentile were large for gestational age (LGA).18 SGA and LGA were grouped as not SGA for statistical analysis.

Assessment of the quality of feeding practices and diet
The children’s food intake was assessed by 24-hour recall (R24h) collected in a face-to-face interview by the researchers with the parents/caregivers using the Multiple Pass Method.19 The interviewers recorded all foods and beverages consumed by the children on the day before the interview.
Additionally, questions were designed to investigate children’s feeding practices during the study period and those before 24 months of age. Specific food groups’ weekly frequency and amount of consumption were investigated to evaluate eating practices in the study period (social isolation phase). The food groups or preparations investigated in this study followed the methodology proposed by the National School Health Survey4 and included: 1-dairy; 2-beans and other legumes; 3- vegetables (except potato and manioc/cassava); 4- fresh fruits; 5-processed meats (including sausage and hamburger); 6- cookies in general (“packaged” snacks, salty and sweet cookies); 7- sweets (including chocolate, candies, chewing gum, lollipops, and other sweets) and 8- sweetened beverages (including soda, natural guarana, and carton juices). The first four items were considered healthy eating markers, and the last four were unhealthy eating markers. Regarding frequency of consumption, the participants reported the food groups or preparations consumed by the children in the last 7 days prior to the date of the interview. Inadequate frequency of consumption of healthy foods was considered when under five times a week, and for unhealthy foods when adopted once a week4.
For the investigation of the feeding practices performed in the first 24 months of life, the prevalence of exclusive breastfeeding until the sixth month of life and the children’s age at the time of food introduction were investigated, and more specifically, the child’s age at the time of introduction to sugar, cow’s milk, and UPF. The adequacy of the time of introducing these foods was evaluated under the guidelines proposed by the Food Guide for Children under two.20
Diet quality was evaluated using healthy eating indices and the assessment of the regular intake of different food groups. Two healthy eating indices (HEI) validated for the Brazilian population were used by children’s age range. The HEI proposed by Ribas et al. 21 was used for children up to two, and the one proposed by Horta et al.22 (2019) was adopted for school-age children. The first instrument was based on the nutritional recommendations proposed by FAO23 and the dietary guidelines of the Food Guide for Children under two.20 The second instrument, on the Brazilian Population Food Guide.24 The diet quality per each index was classified as follows: values above 80 points considered the diet as adequate; 50-80 points, diet requiring improvement (regular); and poor diet for a score below 50 points.
Information was also obtained on parents’ perceptions regarding changes in the frequency of food consumption during the pandemic through a structured questionnaire. The foods included were: milk and dairy products, vegetables and legumes, fast snacks, UPF (including ham, mortadella, salami, sausage, instant noodles, packaged snacks, salty crackers), fresh fruits, fried foods (chicken drumstick, kebab, fried pastry, fried potatoes, except potato chips), animal foods (meat, fish, chicken, or egg), beans and other legumes, sweets (candy, candies, chocolates, chewing gum, candies, or lollipops) and sugar-added beverages (soda, guarana, juice boxes). The response options considered were increase, decrease, or no change in consuming the foods or preparations described above.

Assessment of food security and nutritional status
The BFIMS was used to assess food security status of children in the household. The BFIMS is based on a set of questions that reflect conditions and behaviors related to lack of access to food due to financial constraints during the three months before the interview. The scale ranges from 0 to 14 points. Following standard methods for coding responses, households were categorized as: food secure (0 points), marginally food insecure (1to 5 points), moderately food insecure (6 to 9 points), and severely food insecure (10 to 14 points) 25. For analyses purposes, household food security status was dichotomized as food secure or food insecure (marginally food insecure, moderately food insecure, and severely food insecure combined).

Data Analysis
Simple frequencies and 95% confidence intervals were estimated for the socioeconomic (including purchasing power), demographic and anthropometric characteristics of the population studied according to food insecurity status. Pearson’s chi-square test was used to compare proportions between the groups (food security and food insecurity). The associations between HFI (dependent variable) and demographic, socioeconomic, and dietary factors (independent variables) were assessed using logistic regression models. Crude and adjusted odds ratios were estimated for sex, age group, social class, gestational age (GA), and GA adequacy. The analyses were performed using SPSS (Statistical Package for the Social Sciences) software, version 22.0. The significance level adopted was 5%.

Results
We included in this study 147 children assisted in three high-risk outpatient clinics during the pandemic. Of these, 45% came from HUPE, 32% from HUGG, and 23% from IFF. Table 1 shows the studied population’s socioeconomic, demographic, and anthropometric characteristics per food insecurity status. Most children were female, white, aged 1-6, and with a history of prematurity. Of this sample, 24.4% (n=36) were born small for gestational age.
We found that 47.6% (95% CI: 39.6-55.8) of the households were in HFI situation (Table 1). Of this total, 19.7% had marginal HFI, 16.3% had moderate HFI, and 11.6% had severe HFI. Additionally, 65.3% (n=96) of all families surveyed reported that they did not have money to buy food at home during the pandemic, and this prevalence was higher among families in HFI (n=63) (p<0.01) (data not shown).
Regarding maternal characteristics, 54.1% (n=79) of mothers completed high school, and 34.9% (n=51) had an advanced age at delivery (above 35). Almost all the investigated households were of low and very low economic class (97.3%), characterizing the socioeconomic profile of the sample (Table 1).
No statistical difference was observed between the nutritional status and food insecurity condition (p>0.05), although 25.9% (n=38) of children were overweight and 12.2% (n=18) were stunted.
Regarding the feeding practices performed during the first year of life, the prevalence of exclusive breastfeeding until six months was 31.5%, and the mean age of children at food introduction was 6.4±1.6 months. The frequency of introducing sugar and UPF before 12 months was 51.4% and 84.3%, respectively, while that of cow’s milk before nine months of age was 27% (data not shown).
Multivariate logistic regression revealed associations with HFI only for the variables gestational age (GA) and birth weight adequacy for GA. Households whose children were born preterm (OR: 3.94; 95% CI:1.64-9.48) or small for gestational age (SGA) (OR: 2.52; 95%CI: 1.09-5.79) were more likely to be in HFI than those households whose children were born full-term or not SGA, respectively. Children aged 7-9 years were more likely to be food insecure than children under two (OR: 3.5; 95% CI 0.96-12.7) (Table 1).
Parents’ perception of the change in food consumption frequency during the pandemic was that of lower meat and milk consumption and an higher UPF intake, more prevalent among households of children in a situation of HFI (p<0.05) (Figure 1). The associations between the frequency of regular consumption of healthy and unhealthy foods and HFI status are shown in Table 2. Regular consumption of fruits (OR: 0.40; 95% CI: 0.17-0.94) and vegetables (OR: 0.40; 95% CI: 0.19-0.82) was less frequent among children whose households were in HFI situation, while this relationship was inverse for regular consumption of sweetened beverages (OR: 2.06; 95% CI: 1.02-6.62) and processed meats (OR: 3.1; 95% CI: 1.02-9.46).
Table 2 shows the association between diet quality and household food insecurity. The median total score of HEI was 65.5 points (interquartile range: 54.6;74.6) (data not shown). About 81.3% of the sample had a diet quality profile below the desired level (80 points), with 71.4% needing improvement. A deteriorated diet quality as measured by HEI was observed among children in HFI versus security food (OR:2.4; 95% CI 0.43-14.0), although this association did not reach statistical significance.

Discussion
This is the first prospective study conducted during the Covid-19 pandemic with children discharged from NICU accessing outpatient medical care in person. Our findings revealed a deteriorated diet quality, which appears to be related to reduced purchasing power in this study period. We found an increase in the frequency of consumption of UPF, such as sweetened beverages and processed meats, and a reduction in healthy foods, such as fruits and vegetables. Moreover, parents perceived a declining frequency in children’s consumption of meats and milk, and a growing frequency of consumption of cookies and processed meats during the pandemic, with a higher prevalence reported among households in HFI situation.
Almost half of the households were living in food insecurity, and about one-third were already moderately or severely food insecure. Higher HFI prevalence was found among older children born prematurely, and this is a cause of concern as the economic hardship can impact them directly, via their developmental trajectories, and indirectly via their parents’ health and well-being26.
A study conducted by UNICEF with households who were beneficiaries of the national cash transfer program at the time, the Bolsa Família Program (BFP), showed that 54% of the households interviewed said that some child of up to 5 years and 11 months of age living in the household had missed a meal or had not eaten enough food due to lack of financial resources before the pandemic. This rate increased to 72% during the pandemic, revealing that the Covid-19 pandemic significantly affected access to income and food8. The PENSSAN Network’s National Survey also showed the alarming situation of HFI and hunger in the country on Food Insecurity in the Brazilian Covid-19 pandemic. This survey evidenced that 82.5% of households with three or more people under the age of 18 suffer from some food insecurity27. Most households lost the support of school meals and other institutional spaces, focusing on home feeding. This change has increased the incidence of food insecurity27,28.
The high food prices observed in the last two years can explain the declining intake of these products. Data from the IPCA (Extended Consumer Price Index), the main inflation index in the country, showed that lower nutritional quality foods, such as UPF, varied below average inflation in the first months of 2022, while fresh and minimally processed foods accumulated the highest price increases29. It is worth noting that more than half of the families reported that their food purchases were affected during the pandemic due to their lower purchasing power during this period.
The study also showed that parents perceived a lower consumption of meat and milk throughout the pandemic and a higher intake of UPF among households of children in HFI than food secure households. Milk and other animal-source foods are concentrated dietary sources of macro- and micronutrients essential for adequate child growth30.
The importance of diet quality assessment in NICU children also raised interest in other studies before the pandemic3,31,32. Our group’s studies before the pandemic revealed that more than half of the children born preterm (52.8%) needed to improve their diet, while this proportion was 74.1% in our study. The authors mainly attributed this result to the low total vegetable intake and ultra-processed foods in the diet in 78% of the sample. The median score (78.7) obtained from HEI was higher than that found in the present study, suggesting that the diet quality deteriorated in this public during the pandemic.
The association between deteriorated diet quality and HFI status has been shown in other studies of children. A study of Spanish children aged 2-14 found lower diet quality and diversity, with lower intake of dairy products, fruits, and vegetables and higher consumption of sugar-added beverages among children in a situation of HFI33.
Inadequate consumption patterns have been considered one of the main factors responsible for the global increase in the prevalence of obesity and chronic non-communicable diseases (NCDs)7,34. A study with nationally representative samples of children aged 2-19 from eight middle- and high-income countries, including Brazil, showed that increased UPF consumption was associated with increased energy density and free sugar content in the diet and decreased fiber in almost all countries and age groups, suggesting that UPF intake is a potential determinant of obesity among children and adolescents11. More specifically, among households in HFI, a study in Pelotas showed the coexistence of overweight/obesity and weight deficit35, indicating a decrease in the volume and nutritional quality of the food consumed.
Food insecurity and hunger among children and adolescents have immediate and future adverse effects that compromise these young people’s physical and social potential27. Children from vulnerable groups, such as those included in this study (a subgroup that already carries nutritional risks from the intrauterine period), are at risk of worse health status when in HFI condition. Therefore, interventions to ensure access to adequate and healthy food should be a public health priority.
As is typical of cross-sectional studies, the limitations of this study include the impossibility of establishing causal relationships between the variables analyzed. Moreover, because BFIMS is based on the perception and different experiences of the respondents, the influence of memory bias should not be excluded. It is also noteworthy that the high HFI prevalence should be considered when evaluating the associations found in this study, comparable only among populations with similar characteristics. Memory bias may have also impacted food intake data collection from the children’s caregivers or guardians. Some of them may have omitted details or did not answer correctly. However, this bias is minimized by using the 24-Hour Recall Multiple Pass Method19 and analyzing the data using food intake markers, dividing the foods qualitatively (healthy vs. unhealthy foods). However, we should stress that the main strength of our research is that data were collected face-to-face, using validated dietary intake measures, in public health centers with universal coverage, which facilitated the participation of the eligible participants and a high response rate.

Conclusion
This study’s results showed a high prevalence of food insecurity among children with nutritional vulnerabilities. Food insecurity is associated with deteriorated diet quality, marked by a higher frequency of UPF consumption, and a lower frequency of fruit and vegetable consumption. Our findings reinforce the importance of planning timely interventions to combat food insecurity, especially when rapid decision making is crucial, such as during the COVID-19 pandemic. Interventions aimed at improving children’s diet quality, health and wellbeing in food-insecure households could potentially focus on reducing intake of UPF and improving access to healthful minimally processed foods. Adequate political leadership and commitment to enact policies to respond to this issue is crucial for achieving necessary changes.

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