Abstract

This study aimed to describe the community food environment surrounding schools and its association with territorial socio-environmental vulnerability in the city with the highest intraurban social inequity index in Brazil. Methods: this ecological observational study includes data on the presence and type of food retail in a 400 m buffer surrounding public and private schools in Recife. We have also described the Health Vulnerability Index (HVI) of census tracts and conducted multivariate analyses. Results: through factor analysis, we observed two grouping patterns of food retail. The “diverse food outlets” pattern was positively associated with middle HVI (β 0.14, 95% confidence interval [CI] - 0.11; 0.16) and higher HVI areas (β 0.15, 95%CI - 0.11; 0.17), while “the large food retail chains” pattern was inversely associated with middle HVI (β -0.42, 95% CI - 0.53; -0.30) and high HVI areas (β -0.32, 95%CI - 0.45; -0.18) and positively associated with private schools (β 0.15, 95%CI - 0.030; 0.27). Conclusion: the greatest variety in food retail is in high HVI areas, and large food retail chains prevail around private schools, especially in low HVI areas.

Key words:
School food environment; Supermarkets; Child and adolescent health; Socioeconomic status

Resumo

Este trabalho objetivou descrever o ambiente alimentar comunitário no entorno das escolas e sua associação com a vulnerabilidade socioambiental territorial na cidade com maior índice de desigualdade social intraurbana do Brasil. Métodos: estudo ecológico observacional, inclui dados sobre a presença e o tipo de varejo de alimentos em uma área de 400 m no entorno de escolas públicas e privadas de Recife. Descrevemos o Índice de Vulnerabilidade à Saúde (IVS) dos setores censitários e realizamos análises multivariadas. Resultados: por meio da análise fatorial, observamos dois padrões de agrupamento de estabelecimentos. O padrão “Diversos pontos de venda de alimentos” foi associado positivamente com IVS médio (β 0,14; intervalo de confiança [IC] 95% - 0,11; 0,16) e áreas de IVS mais alto (β 0,15; IC95% - 0,11; 0,17), enquanto o padrão “Grandes redes varejistas de alimentos” foi inversamente associado às áreas de IVS médio (β -0,42; IC95% - 0,53; -0,30) e alto IVS (β -0,32; IC95% - 0,45; -0,18) e positivamente associado com escolas particulares (β 0,15; IC95% - 0,030; 0,27). Conclusão: a maior variedade de estabelecimentos está em áreas de alto IVS, e grandes redes varejistas de alimentos predominam no entorno de escolas particulares, especialmente em áreas de baixo IVS.

Palavras-chave:
Ambiente alimentar escolar; Supermercados; Saúde da criança e do adolescente; Status socioeconômico

Introduction

The food environment can be characterized by the physical and perceived availability of food outside the home and access to it and represents the mediating scenario of food consumption¹1 Story M, Nanney MS, Schwartz MB. Schools and obesity prevention: creating school environments and policies to promote healthy eating and physical activity. Milbank Q 2009; 300(1):71-100.^,22 Swinburn BA, Kraak VI, Allender S, Atkins VJ, Baker PI, Bogard JR, Brinsden H, Calvillo A, De Schutter O, Devarajan R, Ezzati M, Friel S, Goenka S, Hammond RA, Hastings G, Hawkes C, Herrero M, Hovmand PS, Howden M, Jaacks LM, Kapetanaki AB, Kasman M, Kuhnlein HV, Kumanyika SK, Larijani B, Lobstein T, Long MW, Matsudo VKR, Mills SDH, Morgan G, Morshed A, Nece PM, Pan A, Patterson DW, Sacks G, Shekar M, Simmons GL, Smit W, Tootee A, Vandevijvere S, Waterlander WE, Wolfenden L, Dietz WH. The global syndemic of obesity, undernutrition, and climate change: the Lancet Commission report. Lancet 2019; 393(10173):791-846., where the effects of the physical, constructed, and social context condition the individual’s eating behavior and the health of the population²2 Swinburn BA, Kraak VI, Allender S, Atkins VJ, Baker PI, Bogard JR, Brinsden H, Calvillo A, De Schutter O, Devarajan R, Ezzati M, Friel S, Goenka S, Hammond RA, Hastings G, Hawkes C, Herrero M, Hovmand PS, Howden M, Jaacks LM, Kapetanaki AB, Kasman M, Kuhnlein HV, Kumanyika SK, Larijani B, Lobstein T, Long MW, Matsudo VKR, Mills SDH, Morgan G, Morshed A, Nece PM, Pan A, Patterson DW, Sacks G, Shekar M, Simmons GL, Smit W, Tootee A, Vandevijvere S, Waterlander WE, Wolfenden L, Dietz WH. The global syndemic of obesity, undernutrition, and climate change: the Lancet Commission report. Lancet 2019; 393(10173):791-846.

3 Mei K, Huang H, Xia F, Hong A, Chen X, Zhang C, Qiu G, Chen G, Wang Z, Wang C, Yang B, Xiao Q, Jia P. State-of-the-art of measures of the obesogenic environment for children. Obes Rev 2021; 22(Suppl. 1):e13093.^-44 Mackenbach JD, Nelissen KGM, Dijkstra SC, Poelman MP, Daams JG, Leijssen JB, Nicolaou M. A systematic review on socioeconomic differences in the association between the food environment and dietary behaviors. Nutrients 2019;11(9):2215.. The school food environment includes the spaces, infrastructure, information, and nutritional and commercial conditions, where food is available for obtention and consumption within and beyond the school⁵5 Cruz L. Legal Guide on school food and nutrition - Legislating for a healthy school food environment. Rome: FAO; 2020^,66 Food and Agriculture Organization (FAO). School Food and Nutrition Framework. Rome: FAO; Rome: FAO; 2019.. In order to explore the external (static) dimension of the community food environment⁷7 Turner C, Aggarwal A, Walls H, Herforth A, Drewnowski A, Coates J, Kalamatinou S, Kadiyala S. Concepts and critical perspectives for food environment research: a global framework with implications for action in low- and middle-income countries. Glob Food Sec 2018; 18:93-101., it is necessary to comprehend the factors determining food retail in the territory shared by the population around schools, such as availability, density, quantity, accessibility, and location⁸8 Peres CMDC, Costa BVL, Pessoa MC, Honório OS, Carmo ASD, Silva TPRD, Gardone DS, Meireles AL, Mendes LL. O ambiente alimentar comunitário e a presença de pântanos alimentares no entorno das escolas de uma metrópole brasileira. Cad Saude Publica 2021; 37(5):e00205120.

9 Díez J, Cebrecos A, Rapela A, Borrell LN, Bilal U, Franco M. Socioeconomic inequalities in the retail food environment around schools in a Southern European context. Nutrients 2019; 11(7):1511.^-1010 Carmo AS, Assis MM, Cunha CF, Oliveira TRPR, Mendes LL. The food environment of Brazilian public and private schools. Cad Saude Publica. 2018;34(12):e00014918.. These aspects of food retail enable and encourage the school community to make food choices that contribute to a healthy or unhealthy diet⁵5 Cruz L. Legal Guide on school food and nutrition - Legislating for a healthy school food environment. Rome: FAO; 2020.

Beyond the limits of location and permanence at home, the food environment becomes more complex when it includes commuting routes considering work, study, and leisure activities of individuals¹¹11 High Level Panel of Experts. Nutrition and food systems. Rome: HPE; 2017.^,1212 Duran AC, Almeida SL, Latorre MDR, Jaime PC. The role of the local retail food environment in fruit, vegetable and sugar-sweetened beverage consumption in Brazil. Public Health Nutr 2015; 19(6):1093-1102.. Of these, the school, on the community level, brings together social determinants of the individual outside the home in the food context⁴4 Mackenbach JD, Nelissen KGM, Dijkstra SC, Poelman MP, Daams JG, Leijssen JB, Nicolaou M. A systematic review on socioeconomic differences in the association between the food environment and dietary behaviors. Nutrients 2019;11(9):2215.^,1313 Williams JL. Spaces between home and school: the effect of eating location on adolescent nutrition. Ecol Food Nutr 2015; 55(1):65-86.

14 Peres CMC, Gardone DS, Costa BVL, Duarte CK, Pessoa MC, Mendes LL. Retail food environment around schools and overweight: a systematic review. Nutr Rev 2020; 78(10):841-856.^-1515 Glanz K, Sallis JF, Saelens BE, Frank LD. Healthy nutrition environments: concepts and measures. Am J Health Promot 2005; 19(5):330-333.. Studies have investigated environmental characteristics of school surroundings in different countries such as Mexico¹⁶16 Barrera LH, Rothenberg SJ, Barquera S, Cifuentes E. The Toxic Food Environment Around Elementary Schools and Childhood Obesity in Mexican Cities. Am J Prev Med 2016; 51(2):264-270. and the USA¹⁷17 Rummo PE, Wu E, Mcdermott ZT, Schwartz AE. Relationship between retail food outlets near public schools and adolescent obesity in New York City. Health Place 2021; 65:102408., for example, where the massive presence of street food vendors and kiosks was associated with excess weight among students. In Brazil, these studies are concentrated in the South and Southeast regions, and they identified a higher density of retail selling mostly foods of low nutritional value⁸8 Peres CMDC, Costa BVL, Pessoa MC, Honório OS, Carmo ASD, Silva TPRD, Gardone DS, Meireles AL, Mendes LL. O ambiente alimentar comunitário e a presença de pântanos alimentares no entorno das escolas de uma metrópole brasileira. Cad Saude Publica 2021; 37(5):e00205120.^,1818 Henriques P, Alvarenga CRT, Ferreira DM, Dias PC, Soares DDSB, Barbosa RMS, Burlandy L. Food environment surrounding public and private schools: an opportunity or challenge for healthy eating? Cien Saude Colet 2021; 26(8):3135-3145.^,1919 Motter AF, Vasconcelos FAG, Correa EN, Andrade DF. Retail food outlets and the association with overweight/obesity in schoolchildren from Florianópolis, Santa Catarina State, Brazil. Cad Saude Publica 2015; 31(3):620-632..

Some studies have also claimed possible social inequities in the structure of school and community food environments³3 Mei K, Huang H, Xia F, Hong A, Chen X, Zhang C, Qiu G, Chen G, Wang Z, Wang C, Yang B, Xiao Q, Jia P. State-of-the-art of measures of the obesogenic environment for children. Obes Rev 2021; 22(Suppl. 1):e13093.^,99 Díez J, Cebrecos A, Rapela A, Borrell LN, Bilal U, Franco M. Socioeconomic inequalities in the retail food environment around schools in a Southern European context. Nutrients 2019; 11(7):1511.^,1717 Rummo PE, Wu E, Mcdermott ZT, Schwartz AE. Relationship between retail food outlets near public schools and adolescent obesity in New York City. Health Place 2021; 65:102408.^,2020 Mölenberg FJM, Mackenbach JD, Poelman MP, Santos S, Burdorf A, van Lenthe FJ. Socioeconomic inequalities in the food environment and body composition among school-aged children: a fixed-effects analysis. Int J Obes 2021; 45(12):2554-2561.. A cohort carried out in the Netherlands revealed that poor children were surrounded by more unhealthy food outlets over the years, in a fast process of deterioration of the neighborhood’s food environment with repercussions in a slight increase in body mass index (BMI) only among socially vulnerable children after the introduction of fast-food restaurants²⁰20 Mölenberg FJM, Mackenbach JD, Poelman MP, Santos S, Burdorf A, van Lenthe FJ. Socioeconomic inequalities in the food environment and body composition among school-aged children: a fixed-effects analysis. Int J Obes 2021; 45(12):2554-2561.. Socioeconomic aspects of the school neighborhood⁸8 Peres CMDC, Costa BVL, Pessoa MC, Honório OS, Carmo ASD, Silva TPRD, Gardone DS, Meireles AL, Mendes LL. O ambiente alimentar comunitário e a presença de pântanos alimentares no entorno das escolas de uma metrópole brasileira. Cad Saude Publica 2021; 37(5):e00205120.^,2121 Watts AW, Mason SM, Loth K, Larson N, Neumark-Sztainer D. Socioeconomic differences in overweight and weight-related behaviors across adolescence and young adulthood: 10-year longitudinal findings from Project EAT. Prev Med (Baltim) 2016; 87:194-199.^,2222 Virtanen M, Kivimäki H, Ervasti J, Oksanen T, Pentti J, Kouvonen A, Halonen JI, Kivimäki M, Vahtera J. Fast-food outlets and grocery stores near school and adolescents' eating habits and overweight in Finland. Eur J Public Health 2015; 25(4):650-655. and the school’s sector (public or private)¹⁰10 Carmo AS, Assis MM, Cunha CF, Oliveira TRPR, Mendes LL. The food environment of Brazilian public and private schools. Cad Saude Publica. 2018;34(12):e00014918.^,1616 Barrera LH, Rothenberg SJ, Barquera S, Cifuentes E. The Toxic Food Environment Around Elementary Schools and Childhood Obesity in Mexican Cities. Am J Prev Med 2016; 51(2):264-270.^,1919 Motter AF, Vasconcelos FAG, Correa EN, Andrade DF. Retail food outlets and the association with overweight/obesity in schoolchildren from Florianópolis, Santa Catarina State, Brazil. Cad Saude Publica 2015; 31(3):620-632.^,2323 Giacomelli SC, Londero AM, Benedetti FJ, Saccol ALF. Comércio informal e formal de alimentos no âmbito escolar de um município da região central do Rio Grande do Sul. Braz J Food Technol 2017; 20:e2016136. are associated with the quality of the school food environment⁴4 Mackenbach JD, Nelissen KGM, Dijkstra SC, Poelman MP, Daams JG, Leijssen JB, Nicolaou M. A systematic review on socioeconomic differences in the association between the food environment and dietary behaviors. Nutrients 2019;11(9):2215.^,2424 Passos CM, Maia EG, Levy RB, Martins APB, Claro RM. Association between the price of ultra-processed foods and obesity in Brazil. Nutr Metab Cardiovasc Dis 2020; 30(4):589-598.^,2525 Rossi CE, Costa LCF, Machado MS, Andrade DF, Vasconcelos FAG. Factors associated with food consumption in schools and overweight/obesity in 7 to 10-year-old schoolchildren in the state of Santa Catarina, Brazil. Cien Saude Colet 2019; 24(2):443-454..

Exposure to spaces filled with unhealthy food outlets in contexts of financial stress and lower maternal education may contribute to the deepening of health inequities by limiting the consumer’s ability to handle an unhealthy food environment¹³13 Williams JL. Spaces between home and school: the effect of eating location on adolescent nutrition. Ecol Food Nutr 2015; 55(1):65-86.^,2020 Mölenberg FJM, Mackenbach JD, Poelman MP, Santos S, Burdorf A, van Lenthe FJ. Socioeconomic inequalities in the food environment and body composition among school-aged children: a fixed-effects analysis. Int J Obes 2021; 45(12):2554-2561.. On the other hand, evidence specifically on the association between socioeconomic inequities and the school food environment is still unclear⁴4 Mackenbach JD, Nelissen KGM, Dijkstra SC, Poelman MP, Daams JG, Leijssen JB, Nicolaou M. A systematic review on socioeconomic differences in the association between the food environment and dietary behaviors. Nutrients 2019;11(9):2215.. Therefore, this work aims to describe the food environment in the surroundings of public and private schools of the state capital with the highest intraurban social inequity index in Brazil, Recife, as well as its association with the socioeconomic and environmental vulnerability of the territory.

Methodology

Study design and characteristics

This is an ecological observational study performed with secondary data from preschools, elementary/middle schools, and/or high schools, as well as food retail and socioeconomic variables of the population of the city of Recife, state of Pernambuco, Brazil.

Study area

The study was carried out in the city of Recife, state capital of Pernambuco, with an estimated population of 1,537,704 inhabitants in 2020 and a demographic density of 7,039,64 inhabitants per square kilometer²⁶26 Instituto Brasileiro de Geografia e Estatística (IBGE). Censo Demográfico 2010: características da população e dos domicílios. Rio de Janeiro: IBGE; 2011.. Recife is the Brazilian state capital with the highest intra-urban social inequality index, with a Gini coefficient of 0.612 (higher than the national coefficient), and is located in the state with the third highest income inequality in the country according to the Summary of Social Indicators 2020²⁷27 Instituto Brasileiro de Geografia e Estatística (IBGE). Síntese de indicadores sociais: uma análise das condições de vida da população brasileira. Rio de Janeiro: IBGE; 2020..

Variables

Outcome: food environment in school surroundings

For assessing the food environment, we used the 2019 database from the Pernambuco State Department of Finance. This database contained the following information: retail name, address, and National Classification of Economic Activities (CNAE) (available at: https://doi.org/10.48331/scielodata.J4JHY9). CNAE is an instrument developed by the National Classification Commission (CONCLA) that aims to characterize the economic activities performed by companies²⁸28 Instituto Brasileiro de Geografia e Estatística (IBGE). Classificação nacional de atividades econômicas. Rio de Janeiro: IBGE; 2007..

We included the following food retail: butcher shops, street vendors, bars, prepared meal delivery services, hypermarkets, grocery stores, cafeterias, dairies, corner stores, minimarkets, bakeries, fish markets, restaurants, supermarkets, and food, beverage, and candy retailers.

Retails were georeferenced through the Geographic Information System (GIS) using addresses available in the database. The unit of analysis adopted in this study was the 400 m Euclidean buffer surrounding schools, corresponding to a possible daily path taken by students in 5-minute walks²⁹29 Blow J, Gregg R, Davies IG, Patel S. Type and density of independent takeaway outlets: a geographical mapping study in a low socioeconomic ward, Manchester. BMJ Open 2019; 9(7):e023554.^,3030 Charreire H, Casey R, Salze P, Simon C, Chaix B, Banos A, Badariotti D, Weber C, Oppert JM. Measuring the food environment using geographical information systems: a methodological review. Public Health Nutr 2010; 13(11):1773-1785..

Exposures

School characteristics

Secondary data of public and private schools from all over Recife were collected from the National Institute for Educational Studies and Research “Anísio Teixeira” (INEP), referring to 2019. Schools were georeferenced using their addresses and the GIS.

Variables included in the analyses were: the school sector (public or private) and educational stage offered by the school (preschool only; elementary/middle school only; high school only; preschool and elementary/middle school; elementary/middle school and high school, or all stages).

Socioeconomic characteristics

The Health Vulnerability Index (HVI), a synthetic indicator, was used for categorizing census tracts according to socioeconomic and environmental deprivation variables³¹31 Prefeitura de Belo Horizonte. Índice de Vulnerabilidade à Saúde 2012 [Internet]. 2013. [acessado 2022 jun 10]. Disponível em: https://prefeitura.pbh.gov.br/sites/default/files/estrutura-de-governo/saude/2018/publicacaoes-da-vigilancia-em-saude/indice_vulnerabilidade2012.pdf
https://prefeitura.pbh.gov.br/sites/defa... . The HVI was developed to represent life conditions of the population and has been applied as a proxy for socioeconomic vulnerability³²32 Leite MA, Assis MM, Carmo AS, Costa BVL, Claro RM, Castro IR, Cardoso LO, Netto MP, Mendes LL. Is neighborhood social deprivation in a Brazilian city associated with the availability, variety, quality and price of food in supermarkets? Public Health Nutr 2019; 22(18):3395-3404.

33 Leite MA, Assis MM, Carmo AS, Nogueira MC, Netto MP, Mendes LL. Inequities in the urban food environment of a Brazilian city. Food Secur 2021; 13(3):539-549.^-3434 Assis MM, Leite MA, Carmo AS, Andrade ACS, Pessoa MC, Netto MP, Cândido APC, Mendes LL. Food environment, social deprivation and obesity among students from Brazilian public schools. Public Health Nutr 2019; 22(11):1920-1927..

Indicators forming the HVI were selected according to their discriminatory power for spatial inequities in a way that, the higher their value, the higher the expected vulnerability. These are water supply; sanitation; solid waste management; ratio of residents per household; number of illiterate persons and per capita income of up to a minimum wage per household; average monthly nominal income of responsible individuals; and black, mixed-race, or indigenous residents³¹31 Prefeitura de Belo Horizonte. Índice de Vulnerabilidade à Saúde 2012 [Internet]. 2013. [acessado 2022 jun 10]. Disponível em: https://prefeitura.pbh.gov.br/sites/default/files/estrutura-de-governo/saude/2018/publicacaoes-da-vigilancia-em-saude/indice_vulnerabilidade2012.pdf
https://prefeitura.pbh.gov.br/sites/defa... . All information was extracted from the 2010 demographic census²⁶26 Instituto Brasileiro de Geografia e Estatística (IBGE). Censo Demográfico 2010: características da população e dos domicílios. Rio de Janeiro: IBGE; 2011. (last Brazilian census).

The enumeration area was used as the neighborhood unit, functioning as the minimal political-administrative unit used by IBGE for collecting statistical data of interest to the population²⁷27 Instituto Brasileiro de Geografia e Estatística (IBGE). Síntese de indicadores sociais: uma análise das condições de vida da população brasileira. Rio de Janeiro: IBGE; 2020.. This way, the food environment of school surroundings was defined from where the school was located and its respective enumeration area.

After calculating the HVI, each sector was classified according to the number of standard deviations (SD) from the overall mean, with a good index when presenting negative deviations, according to the following categorization: low risk - values lower than the mean HVI; middle risk - HVI values within 0.5 SD of the mean (mean ± 0.5 SD); high risk - values higher than the mean HVI³¹31 Prefeitura de Belo Horizonte. Índice de Vulnerabilidade à Saúde 2012 [Internet]. 2013. [acessado 2022 jun 10]. Disponível em: https://prefeitura.pbh.gov.br/sites/default/files/estrutura-de-governo/saude/2018/publicacaoes-da-vigilancia-em-saude/indice_vulnerabilidade2012.pdf
https://prefeitura.pbh.gov.br/sites/defa... .

Statistical analysis

For collecting school location data, we applied the addresses available at the INEP listing to the online Google Street View tool for obtaining geographic coordinates. Latitude and longitude values for each address were collected from the WGS84 Coordinate System and, by using the QGIS 2.10.1 software, transformed to the Universal Transverse Mercator (UTM) projected coordinate system, zone 23S, SIRGAS datum 2000.

School and HVI characteristics were described by means of absolute frequencies, and their associations were tested using the chi-squared test. Food retail types were analyzed by median values and interquartile ranges since they did not present normal distributions. Their associations with the covariables were verified through a Kruskal Wallis test and Dunnett’s post-hoc test.

A choropleth map was constructed for presenting the distribution of grouping factors according to the buffers. In order to graphically demonstrate the distribution of food retail in the city of Recife, a Kernel density map was created. All maps were built with QGIS 2.14.9 software.

Starting from the presence of food retail within the buffer surrounding schools, we explored possible grouping patterns according to food retail type by using Principal Component Analysis (PCA). Firstly, we assessed the method’s applicability through a Kaiser-Meyer-Olkin test (KMO > 7) and Bartlett’s test of sphericity (p < 0.05). For identifying patterns to be retained, we used the Kaiser criterion, that is, eigen values greater than 1. We also analyzed the eigenvalue graph for each factor (scree plot) and the theoretical plausibility of factors themselves. With the aim of generating a pattern structure that would be more easily interpretable, we performed an orthogonal rotation by maximizing higher factor loadings and minimizing lower loadings via the Varimax method. The food retail pattern composition grouped components with the highest factor loadings. Food retail with factor loadings greater than 0.5 was retained in the matrix.

The generated factor scores were analyzed as a continuous variable. Multiple linear regression was employed for testing the association between the school sector, HVI, and grouping patterns of food retail, adjusting for the unit number within the buffer. In all association analyses, we considered a significance level of 5%. Statistical analyses were conducted using SPSS 15.0.

Results

Out of 1511 schools, four were excluded because they were not located within the Recife geographic field, 34 were excluded due to being an adult and vocational schools, 448 for stating that their activities were suspended, and 18 because they were in 15 sectors with no HVI information; altogether, the study was performed considering 1,007 schools.

The spatial distribution of schools per sector and the HVI of census tracts are represented in Figure 1. We verified a higher concentration of schools, of both private and public sectors, in more central areas of low and middle HVI, whereas less schools were verified in the outskirts to the North, West, and East of the city. In areas with high HVI, we verified a lower density of schools.

Table 1 shows that most schools were in areas with middle HVI (39.5%). These areas concentrated the high proportions of public and private schools: 38.9% and 40%, respectively. Those with low and middle HVI presented a higher proportion of private schools 40.4%. Moreover, in areas with low and middle HVI, we observed a higher availability of diverse educational stages, especially complete secondary education (high school and all stages).

Table 2 illustrates the food environment in school surroundings according to HVI, enumeration area, and school sector. Higher median numbers of total food retail, cafeterias, restaurants, bars, food retailers, and supermarkets were found around schools located in low HVI areas, while a higher median number of minimarkets, beverage shops, and street vendors was found in middle HVI sectors. Cafeterias, prepared meal delivery services, restaurants, and bars presented higher median values around private schools.

Table 3 describes the composition of patterns identified by the PCA. The assumption for conducting analyzes was satisfied (KMO = 0.939; Bartlett p < 0.001). Pattern 1 comprised a greater diversity of food retail (50.81% of explained variance). Food retail with higher factor loadings was prepared meal delivery services, beverage retailers, restaurants, cafeterias, bars, and minimarkets, but also included those who commercialized unprocessed or minimally processed foods for preparing meals, such as grocery stores, dairies, butcher shops, and fish markets. Pattern 1 was renamed as “diverse food outlets”, referring to the diversity of traditional food retailers³⁵35 Organização Pan-Americana de Saúde OPAS. Alimentos e bebidas ultraprocessados na américa latina: tendências, efeito na obesidade e implicações para políticas públicas. Brasília: OPAS; 2018. at outlets³⁵35 Organização Pan-Americana de Saúde OPAS. Alimentos e bebidas ultraprocessados na américa latina: tendências, efeito na obesidade e implicações para políticas públicas. Brasília: OPAS; 2018.^,3636 Lake AA. Neighborhood food environments: food choice, foodscapes and planning for health. Proceedings Nutr Soc 2018; 77(3):239-246.. Pattern 2 (explained variance of 9.34%) grouped food retail belonging to large retail corporations and transnational brands (super and hypermarkets and convenience stores) and was, therefore, identified as “large food retail chains”³⁵35 Organização Pan-Americana de Saúde OPAS. Alimentos e bebidas ultraprocessados na américa latina: tendências, efeito na obesidade e implicações para políticas públicas. Brasília: OPAS; 2018..

After adjusting for the density of food retail within the buffer, we verified that the diverse food outlets pattern was positively associated with middle (β 0.14, 95%CI 0.11; 0.16) and high HVI areas (β 0.15, 95%CI 0.11; 0.17) with a discrete linear trend, whereas the large food retail chains pattern was inversely associated with middle (β -0.42 95%CI -0.53; -0.30) and high HVI areas (β -0.32, 95%CI -0.45; -0.18) and positively associated with private schools (β 0.15, 95%CI 0.030; 0.27) (Table 4).

Discussion

This study revealed 2 different grouping patterns of food retail surrounding schools. One of them included diverse food outlets, mostly commercializing food for consumption after little or no preparation, which was associated with census tracts of high HVI. Meanwhile, the other pattern comprised stores belonging to large retail chains and was inversely associated with census tracts of higher HVI and positively associated with private schools.

Within the diverse food outlet pattern, the presence of a kind of establishment selling food for consumption after little or no preparation was related to the presence of similar food retail around schools. There appears to be a trend of accumulation of various food outlets in cities³⁶36 Lake AA. Neighborhood food environments: food choice, foodscapes and planning for health. Proceedings Nutr Soc 2018; 77(3):239-246.^,3737 Machado PP, Claro RM, Martins APB, Costa JC, Levy RB. Is food store type associated with the consumption of ultra-processed food and drink products in Brazil? Public Health Nutr 2017; 21(1):201-209.. Although a diverse pattern may allow the physical availability of healthy and unhealthy foods, the ultra-processed food consumption pattern may prevail in a more vulnerable population since socioeconomic inequities may compromise their ability to handle an environment with healthy and unhealthy food options⁴4 Mackenbach JD, Nelissen KGM, Dijkstra SC, Poelman MP, Daams JG, Leijssen JB, Nicolaou M. A systematic review on socioeconomic differences in the association between the food environment and dietary behaviors. Nutrients 2019;11(9):2215.^,1313 Williams JL. Spaces between home and school: the effect of eating location on adolescent nutrition. Ecol Food Nutr 2015; 55(1):65-86.^,2020 Mölenberg FJM, Mackenbach JD, Poelman MP, Santos S, Burdorf A, van Lenthe FJ. Socioeconomic inequalities in the food environment and body composition among school-aged children: a fixed-effects analysis. Int J Obes 2021; 45(12):2554-2561.. In Belo Horizonte⁸8 Peres CMDC, Costa BVL, Pessoa MC, Honório OS, Carmo ASD, Silva TPRD, Gardone DS, Meireles AL, Mendes LL. O ambiente alimentar comunitário e a presença de pântanos alimentares no entorno das escolas de uma metrópole brasileira. Cad Saude Publica 2021; 37(5):e00205120. and Niterói¹⁸18 Henriques P, Alvarenga CRT, Ferreira DM, Dias PC, Soares DDSB, Barbosa RMS, Burlandy L. Food environment surrounding public and private schools: an opportunity or challenge for healthy eating? Cien Saude Colet 2021; 26(8):3135-3145., in the Southeast region of Brazil, cafeterias were the most frequent food outlets surrounding schools.

In our study, this pattern was associated with census tracts of higher socio-environmental vulnerability (high HVI). This food outlet pattern including street vendors, cafeterias, and kiosks has been described as prevalent around schools and representative of the sale of unhealthy foods in this environment⁸8 Peres CMDC, Costa BVL, Pessoa MC, Honório OS, Carmo ASD, Silva TPRD, Gardone DS, Meireles AL, Mendes LL. O ambiente alimentar comunitário e a presença de pântanos alimentares no entorno das escolas de uma metrópole brasileira. Cad Saude Publica 2021; 37(5):e00205120.^,1616 Barrera LH, Rothenberg SJ, Barquera S, Cifuentes E. The Toxic Food Environment Around Elementary Schools and Childhood Obesity in Mexican Cities. Am J Prev Med 2016; 51(2):264-270.^,1717 Rummo PE, Wu E, Mcdermott ZT, Schwartz AE. Relationship between retail food outlets near public schools and adolescent obesity in New York City. Health Place 2021; 65:102408.. This was also observed in Madrid⁹9 Díez J, Cebrecos A, Rapela A, Borrell LN, Bilal U, Franco M. Socioeconomic inequalities in the retail food environment around schools in a Southern European context. Nutrients 2019; 11(7):1511., where the diversity of unhealthy food outlets in a 400 m buffer surrounding schools revealed that less favored areas had 62.0% more unhealthy food outlets around schools than more favored areas. This is concerning because, among adolescents of low socioeconomic status, the presence of cafeterias surrounding the school demonstrates an association with the accumulation of irregular eating habits and excess weight¹⁷17 Rummo PE, Wu E, Mcdermott ZT, Schwartz AE. Relationship between retail food outlets near public schools and adolescent obesity in New York City. Health Place 2021; 65:102408.^,2222 Virtanen M, Kivimäki H, Ervasti J, Oksanen T, Pentti J, Kouvonen A, Halonen JI, Kivimäki M, Vahtera J. Fast-food outlets and grocery stores near school and adolescents' eating habits and overweight in Finland. Eur J Public Health 2015; 25(4):650-655..

Considering the second identified pattern (large food retail chains), although these retailers have a wide variety of foods, they have been shown to be large enterprises of massive ultra-processed food supply⁹9 Díez J, Cebrecos A, Rapela A, Borrell LN, Bilal U, Franco M. Socioeconomic inequalities in the retail food environment around schools in a Southern European context. Nutrients 2019; 11(7):1511.^,1717 Rummo PE, Wu E, Mcdermott ZT, Schwartz AE. Relationship between retail food outlets near public schools and adolescent obesity in New York City. Health Place 2021; 65:102408.^,3535 Organização Pan-Americana de Saúde OPAS. Alimentos e bebidas ultraprocessados na américa latina: tendências, efeito na obesidade e implicações para políticas públicas. Brasília: OPAS; 2018.. The diversity of products within sole food retail does not result in the preference for healthy foods: A study indicates that 60.4% of the energy content of foods purchased in this food retail comes from ultra-processed items³⁷37 Machado PP, Claro RM, Martins APB, Costa JC, Levy RB. Is food store type associated with the consumption of ultra-processed food and drink products in Brazil? Public Health Nutr 2017; 21(1):201-209.. This pattern was more present around private schools and less present in areas of higher socio-environmental vulnerability (middle and high HVI). The “large food retail chains” pattern is a symbol of the nutrition transition and represents the inclusion of ultra-processed foods in the diet of the population¹⁷17 Rummo PE, Wu E, Mcdermott ZT, Schwartz AE. Relationship between retail food outlets near public schools and adolescent obesity in New York City. Health Place 2021; 65:102408.^,3535 Organização Pan-Americana de Saúde OPAS. Alimentos e bebidas ultraprocessados na américa latina: tendências, efeito na obesidade e implicações para políticas públicas. Brasília: OPAS; 2018.. Other studies corroborate our findings, researchers have described higher concentrations of large food retail chains in areas of lower socioeconomic vulnerability³⁸38 Correa EN, Padez CMP, Abreu AH, Vasconcelos FAG. Distribuição geográfica e socioeconômica de comerciantes de alimentos: um estudo de caso de um município no Sul do Brasil. Cad Saude Publica 2017; 33(2):e00145015.^,3939 Kimenju SC, Rischke R, Klasen S, Qaim M. Do supermarkets contribute to the obesity pandemic in developing countries? Public Health Nutr 2015; 18(17):3224-3233., as well as high consumption of ultra-processed foods among Brazilian students at private schools, with higher chances of purchasing snacks at the school cafeteria or surrounding retail⁴⁰40 Silva TPR, Matozinhos FP, Gratão LHA, Rocha LL, Vilela LA, Oliveira TRPR, Cunha CF, Mendes LL. Coexistence of risk factors for cardiovascular diseases among Brazilian adolescents: individual characteristics and school environment. PLoS One 2021; 16(7):e0254838..

In Brazil, the technical study of mapping food deserts⁴¹41 Secretaria-Executiva da Câmara Interministerial de Segurança Alimentar e Nutricional. Mapeamento dos desertos alimentares no Brasil. Brasília: MDS; 2019. established a typology, according to the predominance of acquisition of unprocessed, ultra-processed, or mixed foods, attributed to food retailing depending on regional aspects such as the level of development and food culture. According to this classification⁴¹41 Secretaria-Executiva da Câmara Interministerial de Segurança Alimentar e Nutricional. Mapeamento dos desertos alimentares no Brasil. Brasília: MDS; 2019. for the territory we studied, food retailers of the Diverse food outlets pattern represent establishments of different nature that sell food for immediate consumption or little preparation, predominantly unprocessed and mixed foods, although only in cafeterias and bars, ultra-processed products predominate. While in the Large food retail chains pattern, mixed and ultra-processed foods predominate, in addition to maintaining a commercial profile strongly committed to the dissemination of the consumption of ultra-processed foods¹⁷17 Rummo PE, Wu E, Mcdermott ZT, Schwartz AE. Relationship between retail food outlets near public schools and adolescent obesity in New York City. Health Place 2021; 65:102408.^,1919 Motter AF, Vasconcelos FAG, Correa EN, Andrade DF. Retail food outlets and the association with overweight/obesity in schoolchildren from Florianópolis, Santa Catarina State, Brazil. Cad Saude Publica 2015; 31(3):620-632.^,3535 Organização Pan-Americana de Saúde OPAS. Alimentos e bebidas ultraprocessados na américa latina: tendências, efeito na obesidade e implicações para políticas públicas. Brasília: OPAS; 2018.^,3939 Kimenju SC, Rischke R, Klasen S, Qaim M. Do supermarkets contribute to the obesity pandemic in developing countries? Public Health Nutr 2015; 18(17):3224-3233..

In agreement with reports by studies performed in the South³⁸38 Correa EN, Padez CMP, Abreu AH, Vasconcelos FAG. Distribuição geográfica e socioeconômica de comerciantes de alimentos: um estudo de caso de um município no Sul do Brasil. Cad Saude Publica 2017; 33(2):e00145015. and Southeast regions of Brazil⁸8 Peres CMDC, Costa BVL, Pessoa MC, Honório OS, Carmo ASD, Silva TPRD, Gardone DS, Meireles AL, Mendes LL. O ambiente alimentar comunitário e a presença de pântanos alimentares no entorno das escolas de uma metrópole brasileira. Cad Saude Publica 2021; 37(5):e00205120.^,3232 Leite MA, Assis MM, Carmo AS, Costa BVL, Claro RM, Castro IR, Cardoso LO, Netto MP, Mendes LL. Is neighborhood social deprivation in a Brazilian city associated with the availability, variety, quality and price of food in supermarkets? Public Health Nutr 2019; 22(18):3395-3404.^,4242 Duran AC, Diez-Roux AV, Latorre MRDO, Jaime PC. Neighborhood socioeconomic characteristics and differences in the availability of healthy food stores and restaurants in Sao Paulo, Brazil. Health Place 2013; 23:39-47.^,4343 Jaime PC, Duran AC, Sarti FM, Lock K. Investigating environmental determinants of diet, physical activity, and overweight among adults in Sao Paulo, Brazil. J Urban Health 2011; 88(3):567-581., our results indicate that large supermarket chains aim to provide for the richest population in Recife, in the Northeast region, and their location in socioeconomically privileged regions and near private schools may be intentional. Being more present around private schools, hypermarkets do not represent an advantage for students because they promote an obesogenic food environment through their predominantly ultra-processed product profile²⁴24 Passos CM, Maia EG, Levy RB, Martins APB, Claro RM. Association between the price of ultra-processed foods and obesity in Brazil. Nutr Metab Cardiovasc Dis 2020; 30(4):589-598..

In this same social stratum of supermarket target consumers, we find the highest prevalence of excess weight in children of the Northeast region, with lower percentage values than the South region⁴⁴44 Guedes DP, Mello ERB. Prevalência de sobrepeso e obesidade em crianças e adolescentes brasileiros: revisão sistemática e metanálise. ABCS Health Sci 2021; 46:e021301.

45 Conde WL, Mazzeti CMS, Silva JC, Santos IKS, Santos AMR. Nutritional status of Brazilian schoolchildren: National Adolescent School-Based Health Survey 2015. Rev Bras Epidemiol 2018; 21(Supl. 1):E180008.supl.1.^-4646 Bloch KV, Klein CH, Szklo M, Kuschnir MC, Abreu GA, Barufaldi LA, Veiga GV, Schaan B, Silva TL, Vasconcellos MT, Moraes AJ, Borges AL, Oliveira AM, Tavares BM, Oliveira CL, Cunha CF, Giannini DT, Belfort DR, Santos EL, Leon EB, Fujimori E, Oliveira ER, Magliano ES, Vasconcelos FA, Azevedo GD, Brunken GS, Guimarães IC, Faria Neto JR, Oliveira JS, Carvalho KM, Gonçalves LG, Monteiro MI, Santos MM, Jardim PC, Ferreira PA, Montenegro Jr RM, Gurgel RQ, Vianna RP, Vasconcelos SM, Goldberg TB. ERICA: prevalences of hypertension and obesity in Brazilian adolescents. Rev Saude Publica 2016; 50(Supl. 1):9s.. This higher prevalence is found among students with higher family incomes⁴⁷47 Leal VS, Lira PIC, Oliveira JS, Menezes RC, Sequeira LA, Arruda Neto MA, Andrade SL, Batista Filho M. Excesso de peso em crianças e adolescentes no estado de Pernambuco, Brasil: prevalência e determinantes. Cad Saude Publica 2012; 28(6):1175-1182. when compared to those with less access to goods and services in the Northeast region of Brazil. However, nutritional implications to students from more favored areas are frequently described under the light of the ostensive supply of ultra-processed foods among a wide variety of foods available at super and hypermarkets²⁴24 Passos CM, Maia EG, Levy RB, Martins APB, Claro RM. Association between the price of ultra-processed foods and obesity in Brazil. Nutr Metab Cardiovasc Dis 2020; 30(4):589-598.. Meanwhile, for students from high HVI areas, the social inequity component determines that they will be exposed to a higher density of food retail but with scarce diversity and unhealthy options in each of the various retailers in the neighborhood⁹9 Díez J, Cebrecos A, Rapela A, Borrell LN, Bilal U, Franco M. Socioeconomic inequalities in the retail food environment around schools in a Southern European context. Nutrients 2019; 11(7):1511.^,2020 Mölenberg FJM, Mackenbach JD, Poelman MP, Santos S, Burdorf A, van Lenthe FJ. Socioeconomic inequalities in the food environment and body composition among school-aged children: a fixed-effects analysis. Int J Obes 2021; 45(12):2554-2561.^,2222 Virtanen M, Kivimäki H, Ervasti J, Oksanen T, Pentti J, Kouvonen A, Halonen JI, Kivimäki M, Vahtera J. Fast-food outlets and grocery stores near school and adolescents' eating habits and overweight in Finland. Eur J Public Health 2015; 25(4):650-655..

Limitations and potentialities

Some limitations of this work should be mentioned, such as the control of confounding variables when conducting an ecological study, which prevents the analysis of each individual within the studied universe. For minimizing errors, we chose the city territory as the unit of analysis in order to obtain variable homogeneity associated with the determination of environments. The use of secondary data for assessing socio-environmental vulnerability and geographically locating schools and food retail may lead to imprecise or outdated information. For reducing interferences of data temporality, we used the most recently available demographic and school census. Due to the absence of a budget for updating the decennial census, the 2010 edition remained the most recent. To reliably assess the data, we also checked the coordinates virtually. Another limitation in measuring the food environment is related to the special restriction imposed by choosing the Euclidean buffer, although this boundary delimitation technique is frequently adopted for analyzing the community food environment around schools⁸8 Peres CMDC, Costa BVL, Pessoa MC, Honório OS, Carmo ASD, Silva TPRD, Gardone DS, Meireles AL, Mendes LL. O ambiente alimentar comunitário e a presença de pântanos alimentares no entorno das escolas de uma metrópole brasileira. Cad Saude Publica 2021; 37(5):e00205120.^,1414 Peres CMC, Gardone DS, Costa BVL, Duarte CK, Pessoa MC, Mendes LL. Retail food environment around schools and overweight: a systematic review. Nutr Rev 2020; 78(10):841-856.^,2929 Blow J, Gregg R, Davies IG, Patel S. Type and density of independent takeaway outlets: a geographical mapping study in a low socioeconomic ward, Manchester. BMJ Open 2019; 9(7):e023554.^,3030 Charreire H, Casey R, Salze P, Simon C, Chaix B, Banos A, Badariotti D, Weber C, Oppert JM. Measuring the food environment using geographical information systems: a methodological review. Public Health Nutr 2010; 13(11):1773-1785..

Nevertheless, we proposed an innovative analysis for studying the community food environment when compared to analyses that are primarily based on food processing levels³⁷37 Machado PP, Claro RM, Martins APB, Costa JC, Levy RB. Is food store type associated with the consumption of ultra-processed food and drink products in Brazil? Public Health Nutr 2017; 21(1):201-209.^,4848 Zhou Q, Zhao L, Zhang L, Xiao Q, Wu T, Visscher T, Zhao J, Xin J, Yu X, Xue H, Li H, Pan J, Jia P. Neighborhood supermarket access and childhood obesity: a systematic review. Obes Rev 2019; 22(Suppl. 1):e12937. and the classification of food retail regarding the health benefits of the commercialized products⁸8 Peres CMDC, Costa BVL, Pessoa MC, Honório OS, Carmo ASD, Silva TPRD, Gardone DS, Meireles AL, Mendes LL. O ambiente alimentar comunitário e a presença de pântanos alimentares no entorno das escolas de uma metrópole brasileira. Cad Saude Publica 2021; 37(5):e00205120.^,3232 Leite MA, Assis MM, Carmo AS, Costa BVL, Claro RM, Castro IR, Cardoso LO, Netto MP, Mendes LL. Is neighborhood social deprivation in a Brazilian city associated with the availability, variety, quality and price of food in supermarkets? Public Health Nutr 2019; 22(18):3395-3404.^,3838 Correa EN, Padez CMP, Abreu AH, Vasconcelos FAG. Distribuição geográfica e socioeconômica de comerciantes de alimentos: um estudo de caso de um município no Sul do Brasil. Cad Saude Publica 2017; 33(2):e00145015.. Through factor analysis, we first analyzed not only the occurrence of food commercialization of some kind but of commercial retail and how they interact with each other within the territorial distribution. This allowed the analysis of components that are effectively implicated in the correlation between food retail patterns and how the presence of a store may attract or repel other stores. Although the PCA-derived variable for the second pattern represents less than 10% of the variation at points of sale compared to 50% for the result of different exits and implies a lower strength indicative of a linear trend. Factor analysis as an analytic axis of this study is justified by the thesis that commercialization happens according to the consumption demand and consumer profile, but also to the characteristics of competitors in the area³⁶36 Lake AA. Neighborhood food environments: food choice, foodscapes and planning for health. Proceedings Nutr Soc 2018; 77(3):239-246.^,3939 Kimenju SC, Rischke R, Klasen S, Qaim M. Do supermarkets contribute to the obesity pandemic in developing countries? Public Health Nutr 2015; 18(17):3224-3233.^,4949 Farina EMMQ, Nunes R, Monteiro GFA. Supermarkets and their impacts on the agrifood system of Brazil: the competition among retailers. Agribusiness 2005; 21(2):133-147..

Implications to school health

The results of this research demonstrate that the types and grouping patterns of food retail surrounding schools are associated with the sector (public or private) of schools nearby and the socioeconomic characteristics of the enumeration area. After observing these associations and probable impacts on the pattern of food purchase and consumption by the school community, we suggest that laws and public policies considering food outlets within schools should be extended to the school surroundings. This would also expand the positive impacts already observed after the regulation of cafeterias and dining halls⁵⁰50 Food and Agriculture Organization (FAO). School food and nutrition framework [Internet]. 2019. [cited 2022 ago 28]. http://www.fao.org/3/ca4091en/ca4091en.pdf
http://www.fao.org/3/ca4091en/ca4091en.p... ^,5151 Taber D, Chriqui J, Powell L, Perna F, Robinson W, Chaloupka F. Socioeconomic differences in the association between competitive food laws and the school food environment. J School Health 2015; 85(9):578-586. that collaborate with the construction of food environments with restricted exposure to abusive marketing⁵²52 Polacsek M, Boninger F, Molnar A, O'Brien LM. Digital Food and beverage marketing environments in a national sample of middle schools: implications for policy and practice. J School Health 2019; 89(9):739-751. and ultra-processed foods.

Considering the purchase of food and beverages as an exercise of autonomy by schoolchildren that allows a certain escape from the control exercised by adults (guardians and school)¹³13 Williams JL. Spaces between home and school: the effect of eating location on adolescent nutrition. Ecol Food Nutr 2015; 55(1):65-86., interventions that lend themselves to changing the context of decision-making, through regulation of local commerce, for example, tend to be more effective when reaching society widely⁵³53 Thomas R. Frieden. A framework for public health action: the health impact pyramid. Am J Public Health. 2010; 100(4):590-595. and not just the internal territory of schools. It should be kept in mind that regulating food retail in school surroundings is a more complex matter than doing so with school cafeterias and dining halls, considering that neighboring retail provides food for the population and not exclusively for the school community. On a local level, restrictions to ultra-processed food marketing aimed at children with ludic characteristics; incentives to the supply of unprocessed or minimally processed foods through attractive product placement and favorable prices for socio-environmentally vulnerable populations; and a responsive relationship between actions that promote healthy eating within schools and the external environment where students navigate are initial actions that may favor a healthier food environment for students.

Conclusions

This study described the community food environment surrounding private and public schools and its association with socio-environmental vulnerability conditions. Our main result revealed a higher diversity of food retail in areas of higher vulnerability, whereas the presence of large chain stores predominated in census tracts of less vulnerable, mainly surrounding private schools. Based on these findings, the coexistence of food retailers around schools is configured not only by commercial relations but in association with the social and economic aspects of the community that shares a certain territory. Future research should advance from the NOVA classification of foods to explore the types of retail grouped in the same neighborhood. Understanding the commercial scenario should enable the promotion of education for realistic practice of better food choices, whether in the diversity of foods or of the retailers, for the various social groups distributed throughout the city.

References

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