Association between food insecurity and chronic noncommunicable diseases in Brazil: a systematic review

Jackson Silva Lima Laurentino Renatha Celiana da Silva Brito Rônisson Thomas de Oliveira-Silva Amanda Soares Thaís da Conceição Pereira Elisiandre Martins de Lima Ana Beatriz Macêdo Venâncio dos Santos Poliana de Araújo Palmeira About the authors

ABSTRACT

Objective:

To analyze the association of food insecurity (FI) with chronic noncommunicable diseases (NCDs) in the Brazilian context.

Methods:

The review protocol was registered with the International Prospective Register of Systematic Reviews (PROSPERO). The searches were conducted in LILACS and PubMed databases (September/2022). Observational studies carried out in the Brazilian population published since 2003 were included, in which: (1) the association of FI with NCDs was analyzed; and (2) the Brazilian Food Insecurity Scale was used. Studies on pregnant women and those that associated FI with cancer, sexually transmitted infections, and musculoskeletal and respiratory diseases were excluded. The studies were subjected to methodological quality assessment.

Results:

A total of 27 cross-sectional studies were included; nine used secondary data from national surveys, and the others used primary data. An association between FI and overweight and obesity in different age groups was verified in the studies.

Conclusion:

The included articles did not produce evidence on other NCDs of interest to health in Brazil such as diabetes and high blood pressure. However, they corroborate the already-known relationship between obesity and FI. Studies on the topic, with a longitudinal design, should be encouraged.

Keywords:
Food insecurity; Chronic noncommunicable diseases; Brazil; Review

INTRODUCTION

Food Insecurity (FI) is expressed by concern, fear, uncertainty, and deprivation in access to quality food in sufficient quantity to maintain a healthy life11 Kepple AW, Segall-Corrêa AM. Conceptualizing and measuring food and nutrition security. Cienc Saude Colet 2011; 16(1): 187-99. https://doi.org/10.1590/S1413-81232011000100022
https://doi.org/10.1590/S1413-8123201100...
. According to the Food and Agriculture Organization of the United Nations (FAO) 2022 report, it is estimated that between 702 and 828 million people experienced hunger in 2021, totaling around 9.8% of the world population22 FAO, IFAD, UNICEF, WFP, WHO. The State of Food Security and Nutrition in the World. Repurposing food and agricultural policies to make healthy diets more affordable. Rome: FAO; 2022. https://doi.org/10.4060/cc0639en
https://doi.org/10.4060/cc0639en...
. In Brazil, high rates of FI are observed, with data showing that around 125.2 million Brazilians were suffering from some degree of FI and 33 million were facing food deprivation in 202233 II Inquérito Nacional sobre Insegurança Alimentar no Contexto da Pandemia da COVID-19 no Brasil [Internet]. São Paulo: REDE PENSSAN; 2022 [cited on Apr. 17, 2023]. Available at: https://olheparaafome.com.br/wp-content/uploads/2022/06/Relatorio-II-VIGISAN-2022.pdf
https://olheparaafome.com.br/wp-content/...
.

Exposure to FI is associated with negative health outcomes, such as poor nutrition and Chronic Noncommunicable Diseases (NCDs), representing one of the most important public health issues to be faced44 Cabral NLA, Pequeno NPF, Roncalli AG, Marchioni DML, Lima SCVC, Lyra CO. Proposta metodológica para avaliação da insegurança alimentar sob a ótica de suas múltiplas dimensões. Cienc Saude Colet 2022; 27(7): 2855-66. https://doi.org/10.1590/1413-81232022277.11752021
https://doi.org/10.1590/1413-81232022277...
. In this sense, FI has been associated with important metabolic risk factors and NCDs such as overweight and obesity55 Schlüssel MM, Silva AAM, Pérez-Escamilla R, Kac G. Household food insecurity and excess weight/obesity among Brazilian women and children: a life-course approach. Cad Saude Pública 2013; 29(2): 219-26. https://doi.org/10.1590/S0102-311X2013000200003
https://doi.org/10.1590/S0102-311X201300...
,66 Santos LVTS, Cáceres LA, Pelogo GF. Insegurança alimentar, consumo de alimentos e estado nutricional de mulheres de Campo Grande, Mato Grosso do Sul. Interações (Campo Grande) 2019; 20(3): 831-44. https://doi.org/10.20435/inter.v0i0.1814
https://doi.org/10.20435/inter.v0i0.1814...
, dyslipidemia77 Arenas DJ, Zhou S, Thomas A, Wang J, Arroyo GV, Bash K. Negative health outcomes associated with food insecurity status in the United States of America: a systematic review of peer-reviewed studies. NutriXiv Preprints; 2018. https://doi.org/10.31232/osf.io/uk9xw
https://doi.org/10.31232/osf.io/uk9xw...
, diabetes (DM)88 Mahmood MR, Najafipour H, Mohsenpour MA, Amiri M. The relationship between food insecurity with cardiovascular risk markers and metabolic syndrome components in patients with diabetes: a population-based study from Kerman coronary artery disease risk study. J Res Med Sci 2017; 22: 118. https://doi.org/10.4103/jrms.JRMS_12_17
https://doi.org/10.4103/jrms.JRMS_12_17...
, and systemic arterial hypertension (SAH)99 Vasconcelos SML, Torres NCP, Silva PMC, Santos TMP, Silva JVL, Omena CMB, et al. Insegurança alimentar em domicílios de indivíduos portadores de hipertensão e/ou diabetes. Int J Cardiovasc Sci 2015; 28(2): 114-21.. The deprivation and difficulty accessing healthy foods among people on FI lead to lower consumption of fruits and vegetables and an increase in the consumption of lower-cost foods with high calorie density, such as processed and ultra-processed foods, generating malnutrition. This factor contributes to the development of health problems such as NCDs1010 Nkambule SJ, Moodley I, Kuupiel D, Mashamba-Thompson TP. Association between food insecurity and key metabolic risk factors for diet-sensitive non-communicable diseases in sub-Saharan Africa: a systematic review and meta-analysis. Sci Rep 2021; 11(1): 5178. https://doi.org/10.1038/s41598-021-84344-0
https://doi.org/10.1038/s41598-021-84344...
,1111 Aiyer JN, Raber M, Bello RS, Brewster A, Caballero E, Chennisi C, et al. A pilot food prescription program promotes produce intake and decreases food insecurity. Transl Behav Med 2019; 9(5): 922-30. https://doi.org/10.1093/tbm/ibz112
https://doi.org/10.1093/tbm/ibz112...
.

Brazil left the United Nations (UN) Hunger Map in 2014, through Food and Nutritional Security strategies employed since the mid-1990s. However, in 2018, data from the Consumer Expenditure Survey1212 Instituto Brasileiro de Geografia e Estatística. Pesquisa de orçamento familiares 2017-2018: análise da segurança alimentar no Brasil. Rio de Janeiro: IBGE; 2020. indicated the increase in FI in Brazil. Conversely, the FAO report, published in 2022, showed the country's return to the hunger map, as a result of the crisis in the political, social, and economic spheres linked to the new coronavirus (COVID-19) pandemic22 FAO, IFAD, UNICEF, WFP, WHO. The State of Food Security and Nutrition in the World. Repurposing food and agricultural policies to make healthy diets more affordable. Rome: FAO; 2022. https://doi.org/10.4060/cc0639en
https://doi.org/10.4060/cc0639en...
. Added to the scenario of FI evolution in Brazil is the increase in NCDs in the country, which corresponded to around 76% of total deaths in 20191313 Malta DC, Duncan BB, Schmidt MI, Teixeira RA, Ribeiro ALP, Felisbino-Mendes MS, et al. Trends in mortality due to non-communicable diseases in the Brazilian adult population: national and subnational estimates and projections for 2030. Popul Health Metr 2020; 18(Suppl 1): 16. https://doi.org/10.1186/s12963-020-00216-1
https://doi.org/10.1186/s12963-020-00216...
. The increase in NCDs rates in Brazil has been attributed to exposure to risk factors related to lifestyle, such as physical inactivity, alcohol abuse, tobacco use, overweight, and unhealthy eating habits such as low consumption of fruits and vegetables and high consumption of processed and ultra-processed foods. These factors are combined with social inequalities and health inequities1313 Malta DC, Duncan BB, Schmidt MI, Teixeira RA, Ribeiro ALP, Felisbino-Mendes MS, et al. Trends in mortality due to non-communicable diseases in the Brazilian adult population: national and subnational estimates and projections for 2030. Popul Health Metr 2020; 18(Suppl 1): 16. https://doi.org/10.1186/s12963-020-00216-1
https://doi.org/10.1186/s12963-020-00216...
, generating progressive and worrying scenarios of an increase in NCDs in Brazil.

The Brazilian Food Insecurity Scale (Escala Brasileira de Insegurança Alimentar – EBIA) is the main tool used to measure and monitor FI in Brazil11 Kepple AW, Segall-Corrêa AM. Conceptualizing and measuring food and nutrition security. Cienc Saude Colet 2011; 16(1): 187-99. https://doi.org/10.1590/S1413-81232011000100022
https://doi.org/10.1590/S1413-8123201100...
,1414 Pérez-Escamilla R, Segall-Corrêa AM, Maranha LK, Sampaio MFA, Marín-León L, Panigassi G. An adapted version of the U.S. Department of Agriculture Food Insecurity Module is a valid tool for assessing household food insecurity in Campinas, Brazil. J Nutr 2004; 134(8): 1923-8. https://doi.org/10.1093/jn/134.8.1923
https://doi.org/10.1093/jn/134.8.1923...
, consisting of a scale of experience with food deprivation, validated for the Brazilian population since 20041414 Pérez-Escamilla R, Segall-Corrêa AM, Maranha LK, Sampaio MFA, Marín-León L, Panigassi G. An adapted version of the U.S. Department of Agriculture Food Insecurity Module is a valid tool for assessing household food insecurity in Campinas, Brazil. J Nutr 2004; 134(8): 1923-8. https://doi.org/10.1093/jn/134.8.1923
https://doi.org/10.1093/jn/134.8.1923...
. Since its validation, EBIA has been incorporated into the main national surveys, such as the National Household Sample Survey (Pesquisa Nacional por Amostra de Domicílios – PNAD)1515 Instituto Brasileiro de Geografia e Estatística. Pesquisa Nacional por Amostra de Domicílios. Segurança alimentar [Internet]. 2009 [cited on May 10, 2023]. Available at: https://www.ibge.gov.br/estatisticas/sociais/saude/19898-suplementos-pnad3.html?edicao=10527
https://www.ibge.gov.br/estatisticas/soc...
,1616 Instituto Brasileiro de Geografia e Estatística. Pesquisa Nacional por Amostra de Domicílios. Segurança alimentar [Internet]. 2013 [cited on May 10, 2023]. Available at: https://www.ibge.gov.br/estatisticas/sociais/saude/19898-suplementos-pnad3.html?edicao=10528
https://www.ibge.gov.br/estatisticas/soc...
and, more recently, the Consumer Expenditure Survey (Pesquisa de Orçamentos Familiares – POF, 2017–2018)1212 Instituto Brasileiro de Geografia e Estatística. Pesquisa de orçamento familiares 2017-2018: análise da segurança alimentar no Brasil. Rio de Janeiro: IBGE; 2020. and the National Survey on Food Insecurity within the COVID-19 context (Inquérito de Insegurança Alimentar no Contexto da Pandemia da Covid-19 – VIGISAN)33 II Inquérito Nacional sobre Insegurança Alimentar no Contexto da Pandemia da COVID-19 no Brasil [Internet]. São Paulo: REDE PENSSAN; 2022 [cited on Apr. 17, 2023]. Available at: https://olheparaafome.com.br/wp-content/uploads/2022/06/Relatorio-II-VIGISAN-2022.pdf
https://olheparaafome.com.br/wp-content/...
.

However, despite the accumulation of Brazilian studies on FI, its association with NCDs is not yet well documented in the population. Therefore, the objective of this review was to analyze the association of FI with NCDs in the Brazilian context.

METHODS

This systematic review is registered with the International Prospective Register of Systematic Reviews (PROSPERO), under number CRD42023453178, and followed the recommendations of the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA)1717 Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 2021; 372: n71. https://doi.org/10.1136/bmj.n71
https://doi.org/10.1136/bmj.n71...
.

Search strategy

The bibliographic search was carried out in the two main indexing databases of Brazilian scientific production, the Latin American and Caribbean Health Sciences Literature (LILACS) and the National Library of Medicine – PubMed (date of the last query: September 14, 2022). The following terms were developed by the authors in the databases: "Food Supply" (MeSH Terms); OR "Food Insecurity" (MeSH Terms); OR "Food Security" (MeSH Terms); OR "Household Food Security" (Title/Abstract); OR "Household Food Insecurity" (Title/Abstract); AND "Chronic Disease" (MeSH Terms); OR "Noncommunicable diseases" (MeSH Terms); OR "Overnutrition" (MeSH Terms); OR "Obesity" (MeSH Terms); OR "Glucose Metabolism Disorders" (MeSH Terms); OR "Lipid Metabolism Disorders" (MeSH Terms); OR "Hypertension" (MeSH Terms); OR "Body Mass Index" (MeSH Terms); OR "Health Status" (MeSH Terms); OR "Risk Factors" (MeSH Terms); OR "Pulmonary Disease, Chronic Obstructive" (MeSH Terms); OR "Renal Insufficiency, Chronic" (MeSH Terms); AND "Brazil" (MeSH Terms); OR "Brazil" (Title/Abstract); OR "Brazilian" (Title/Abstract).

The search included studies published between 2003 (EBIA validation in Brazil) and September 2022 (final data search), in Portuguese, English, and Spanish. After the bibliographic search, duplicate articles were excluded with the aid of the EndNote software.

Inclusion/exclusion criteria and risk of bias assessment

The inclusion criteria were applied in two stages. First, two independent researchers evaluated the title and abstract of the articles, according to the following inclusion criteria:

  1. Studies that analyzed the association (through association tests) of FI with NCDs or FI with risk indicators for NCDs;

  2. Studies carried out in the Brazilian population including all age groups of children, adolescents, adults, and older adults;

  3. Studies that used EBIA to measure FI (EBIA has dichotomous questions that adapt to family composition, with eight questions for households without individuals <18 years old and 14 questions for households >18 years old, both were included);

  4. Studies that used validated measures for diagnosing NCDs and risk indicators for NCDs; and

  5. Observational studies: cross-sectional and longitudinal.

In the second stage, the articles that met the inclusion criteria were read in full and evaluated for compliance with the criteria of the Quality Assessment Tool for Quantitative Studies (QATFQS)1818 Effective Public Health Practice Project. Quality assessment tool for quantitative studies [Internet]. Hamilton: Effective Public Health Practice Project; 1998 [cited on Sept. 10, 2023]. Available at: https://merst.healthsci.mcmaster.ca/ephpp/
https://merst.healthsci.mcmaster.ca/ephp...
, which classifies studies according to their quality as "strong," "moderate," and "weak." This instrument was chosen because it is relevant for the evaluation of cross-sectional observational studies. Studies with a "weak" classification were excluded.

Methodological, qualitative, and quantitative studies with an ecological or case-control design did not meet the inclusion criteria. Studies on pregnant women and those that associated FI with sexually transmitted infections, cancer, musculoskeletal diseases (arthritis, osteoporosis), and respiratory diseases (asthma) were also excluded. In addition, preprint articles were excluded.

In the inclusion stage, agreement between researchers was assessed using the Kappa index1919 Shrout PE. Measurement reliability and agreement in psychiatry. Stat Methods Med Res 1998; 7(3): 301-17. https://doi.org/10.1177/096228029800700306
https://doi.org/10.1177/0962280298007003...
. Agreement was determined when both researchers chose to exclude or include the same article.

Data extraction

Data extraction was carried out by two independent researchers. Information to be extracted was previously established by the researchers, namely: authors; year of publication; study objective; study location (city/state); study design; study population and year of data collection; type of sample (probabilistic and non-probabilistic); data source (primary or secondary); type of statistical analyses; main results on the association of FI with NCDs; hypotheses and justifications used by the authors to explain the association of FI with NCDs.

The hypotheses and justifications used by the authors to explain the association of FI with NCDs were used to propose a conceptual model on the paths of association between FI and NCDs.

During the data extraction process, it was noted that two of the included articles2020 Pimentel PG, Sichieri R, Salles-Costa R. Food insecurity, socioeconomic conditions and anthropometric indicators in children living in the Metropolitan Region of Rio de Janeiro, Brazil. Rev Bras Estud 2009; 26(2): 283-94. https://doi.org/10.1590/S0102-30982009000200008
https://doi.org/10.1590/S0102-3098200900...
,2121 Vieira PD, Frota MTBA, Rocha EMB, Szarfarc SC, Bezerra IMP, Nascimento VG, et al. Nutritional profile of women assisted by the program of Family Health Strategy in Maranhão State, Brazil. J Hum Growth Dev 2020; 30(1): 24-31. https://doi.org/10.7322/jhgd.v30.9963
https://doi.org/10.7322/jhgd.v30.9963...
used EBIA responses as a continuous variable for the analyses, which is not appropriate. These, therefore, were excluded. The results were synthesized and presented in a descriptive way.

RESULTS

In the initial search, we identified 222 articles. With the application of the inclusion and exclusion criteria, 188 articles were excluded (19 due to duplication and 169 for not meeting the inclusion criteria). After quality assessment, this review included 27 articles (Figure 1). In the inclusion stage, the Kappa index was 1.0, indicating perfect agreement.

Figure 1
Flowchart of the selection process of studies included in the systematic review on food insecurity and chronic noncommunicable diseases in Brazil, 2023.

Among the 27 articles, nine were carried out with national samples of the population. The other studies used regional samples, with n=9 in the Northeast region, n=5 in the Southeast, n=2 in the Midwest, and n=2 in the South (Supplementary Material).

The articles were published between 2012 and 2022 and the data were collected between 2005 and 2019. All analyzed articles have a cross-sectional design, 66.7% (n=18) used primary data and 33.3% (n=9) used secondary data from two national surveys: the National Survey of Demography and Health (Pesquisa Nacional de Demografia e Saúde – PNDS) (n= 8) and the Consumer Expenditure Survey – POF (n=1). Most studies used a probabilistic sample (85.2%).

The population groups included in the studies were: adolescents (n=8), children (n=7), women with children (n=4), adults (n=4), adult women (n=2), adults and older adults (n=1), older adults (n=1), and adults and older adults diagnosed with DM and/or SAH users of a Health Center (Unidade Básica de Saúde – UBS) (n=1).

Risk indicators for NCDs were: body mass index (BMI) (n=21), weight-for-age index (n=2), weight-for-height index (n=2), waist circumference (WC) (n=2), blood pressure (BP) (n=1), and capillary triglycerides analysis (n=1).

To analyze the associations of FI with risk indicators for NCDs (Table 1)55 Schlüssel MM, Silva AAM, Pérez-Escamilla R, Kac G. Household food insecurity and excess weight/obesity among Brazilian women and children: a life-course approach. Cad Saude Pública 2013; 29(2): 219-26. https://doi.org/10.1590/S0102-311X2013000200003
https://doi.org/10.1590/S0102-311X201300...
,99 Vasconcelos SML, Torres NCP, Silva PMC, Santos TMP, Silva JVL, Omena CMB, et al. Insegurança alimentar em domicílios de indivíduos portadores de hipertensão e/ou diabetes. Int J Cardiovasc Sci 2015; 28(2): 114-21.,2222 Kac G, Velásquez-Melendez G, Schlüssel M, Segall-Côrrea A, Silva A, Pérez-Escamilla R. Severe food insecurity is associated with obesity among Brazilian adolescent females. Public Health Nutr 2012; 15(10): 1854-60. https://doi.org/10.1017/S1368980011003582
https://doi.org/10.1017/S136898001100358...
3333 Poblacion AP, Cook JT, Marín-León L, Segall-Corrêa AM, Silveira JAC, Konstantyner T, et al. Food insecurity and the negative impact on Brazilian children's health-why does food security matter for our future prosperity? Brazilian National Survey (PNDS 2006/07). Food Nutr Bull 2016; 37(4): 585-98. https://doi.org/10.1177/0379572116664167
https://doi.org/10.1177/0379572116664167...
, most authors applied multivariate analysis models: Poisson Regression (n=12), Logistic Regression (n=7), Linear Regression (n=3), and Structural Equation Model (n=1). In five articles, the association was performed using the chi-square test (χ2 test).

Table 1
General characteristics and main results of the studies included in the systematic review that demonstrated associations between food insecurity and chronic noncommunicable diseases, 2023.

For analysis purposes, the included articles categorized EBIA into: 2 categories (Food Security [FS] x FI, 9 articles; FS/mild FI x moderate/severe FI, 4 articles; FS x moderate/severe FI, 2 articles; FS x moderate FI, 1 article; FS x mild FI, 1 article; FS/mild/moderate FI x severe FI, 1 article), 3 categories (FS x mild FI x moderate/severe FI, 3 articles), and 4 categories (FS x mild FI x moderate FI x severe FI, 6 articles).

Regarding the association of FI with NCDs, in Table 1 we present a summary of the general characteristics and main results of the included articles that presented associations. According to the studies, there was an association of FI with overweight and overweight/obesity in different age groups of the life cycle and between men and women, assessed mainly through BMI. As for how the FI variable was used in the analyses, 18 studies used it as an exposure variable/risk factor55 Schlüssel MM, Silva AAM, Pérez-Escamilla R, Kac G. Household food insecurity and excess weight/obesity among Brazilian women and children: a life-course approach. Cad Saude Pública 2013; 29(2): 219-26. https://doi.org/10.1590/S0102-311X2013000200003
https://doi.org/10.1590/S0102-311X201300...
,2222 Kac G, Velásquez-Melendez G, Schlüssel M, Segall-Côrrea A, Silva A, Pérez-Escamilla R. Severe food insecurity is associated with obesity among Brazilian adolescent females. Public Health Nutr 2012; 15(10): 1854-60. https://doi.org/10.1017/S1368980011003582
https://doi.org/10.1017/S136898001100358...
2424 Santos NF, Lira PIC, Tavares FCLP, Leal VS, Oliveira JS, Pessoa JT, et al. Overweight in adolescents: food insecurity and multifactoriality in semiarid regions of Pernambuco. Rev Paul Pediatr 2019; 38: e2018177. https://doi.org/10.1590/1984-0462/2020/38/2018177
https://doi.org/10.1590/1984-0462/2020/3...
,2626 Pequeno NPF, Cabral NLA, Oliveira AGRC, Crispim SP, Rocha C, Marchioni DM, et al. Chronic diseases and emotional disorders are associated with low perception of quality of life in food insecurity/security. Front Public Health 2022; 10: 893601. https://doi.org/10.3389/fpubh.2022.893601
https://doi.org/10.3389/fpubh.2022.89360...
2828 Velásquez-Melendez G, Schlüssel MM, Brito AS, Silva AA, Lopes-Filho JD, Kac G. Mild but not light or severe food insecurity is associated with obesity among Brazilian women. J Nutr 2011; 141(5): 898-902. https://doi.org/10.3945/jn.110.135046
https://doi.org/10.3945/jn.110.135046...
,3131 Gubert MB, Spaniol AM, Segall-Corrêa AM, Pérez-Escamilla R. Understanding the double burden of malnutrition in food insecure households in Brazil. Matern Child Nutr 2017; 13(3): e12347. https://doi.org/10.1111/mcn.12347
https://doi.org/10.1111/mcn.12347...
,3232 Vicenzi K, Henn RL, Weber AP, Backes V, Paniz VMV, Donatti T, et al. Insegurança alimentar e excesso de peso em escolares do primeiro ano do Ensino Fundamental da rede municipal de São Leopoldo, Rio Grande do Sul, Brasil. Cad Saúde Pública 2015; 31(5): 1084-94. https://doi.org/10.1590/0102-311X00055914
https://doi.org/10.1590/0102-311X0005591...
,3434 Domingos TB, Pereira AF, Yokoo EM, Salles-Costa R. Low fruit consumption and omission of daily meals as risk factors for increased blood pressure in adults. Br J Nutr 2016; 116(4): 683-91. https://doi.org/10.1017/S0007114516002397
https://doi.org/10.1017/S000711451600239...
4242 Pinheiro MM, Oliveira JS, Leal VS, Lira PIC, Souza NP, Campos FACS. Prevalence of overweight and associated factors in women in reproductive age in Northeast Brazil. Rev Nutr 2016; 29(5): 679-89. https://doi.org/10.1590/1678-98652016000500006
https://doi.org/10.1590/1678-98652016000...
and 9 studies as an outcome variable99 Vasconcelos SML, Torres NCP, Silva PMC, Santos TMP, Silva JVL, Omena CMB, et al. Insegurança alimentar em domicílios de indivíduos portadores de hipertensão e/ou diabetes. Int J Cardiovasc Sci 2015; 28(2): 114-21.,2525 Costa NS, Santos MO, Carvalho CPO, Assunção ML, Ferreira HS. Prevalence and factors associated with food insecurity in the context of the economic crisis in Brazil. Curr Dev Nutr 2017; 1(10): e000869. https://doi.org/10.3945/cdn.117.000869
https://doi.org/10.3945/cdn.117.000869...
,2929 Dias MS, Dumith SC, Vaz JS, Susin LRO. Insegurança alimentar em um município do extremo sul do Rio Grande do Sul, 2016: um estudo de base populacional. Epidemiol Serv Saúde 2020; 29(2): e2019204. https://doi.org/10.5123/S1679-49742020000200007
https://doi.org/10.5123/S1679-4974202000...
,3030 Souza BFNJ, Marín-León L. Insegurança alimentar em idosos: estudo transversal com usuários de restaurante popular. Rev Nutr 2013; 26(6): 679-91. https://doi.org/10.1590/S1415-52732013000600007
https://doi.org/10.1590/S1415-5273201300...
,3333 Poblacion AP, Cook JT, Marín-León L, Segall-Corrêa AM, Silveira JAC, Konstantyner T, et al. Food insecurity and the negative impact on Brazilian children's health-why does food security matter for our future prosperity? Brazilian National Survey (PNDS 2006/07). Food Nutr Bull 2016; 37(4): 585-98. https://doi.org/10.1177/0379572116664167
https://doi.org/10.1177/0379572116664167...
,4343 Gubert M, Spaniol A, Bortolini G, Pérez-Escamilla, R. Household food insecurity, nutritional status and morbidity in Brazilian children. Public Health Nutr 2016; 19(12): 2240-5. https://doi.org/10.1017/S1368980016000239
https://doi.org/10.1017/S136898001600023...
4646 Guerra LDS, Espinosa MM, Bezerra ACD, Guimarães LV, Lima-Lopes MA. Insegurança alimentar em domicílios com adolescentes da Amazônia Legal Brasileira: prevalência e fatores associados. Cad Saúde Pública 2013; 29(2): 335-48. https://doi.org/10.1590/S0102-311X2013000200020
https://doi.org/10.1590/S0102-311X201300...
.

In adolescents, authors of the studies found an association between overweight and severe FI55 Schlüssel MM, Silva AAM, Pérez-Escamilla R, Kac G. Household food insecurity and excess weight/obesity among Brazilian women and children: a life-course approach. Cad Saude Pública 2013; 29(2): 219-26. https://doi.org/10.1590/S0102-311X2013000200003
https://doi.org/10.1590/S0102-311X201300...
and an association between severe FI2222 Kac G, Velásquez-Melendez G, Schlüssel M, Segall-Côrrea A, Silva A, Pérez-Escamilla R. Severe food insecurity is associated with obesity among Brazilian adolescent females. Public Health Nutr 2012; 15(10): 1854-60. https://doi.org/10.1017/S1368980011003582
https://doi.org/10.1017/S136898001100358...
, moderate/severe FI2323 Santana DD, Barros EG, Salles-Costa R, Veiga GV. Mudanças na prevalência de excesso de peso em adolescentes residentes em área de alta vulnerabilidade à insegurança alimentar. Ciênc Saúde Colet 2021; 26(12): 6189-98. https://doi.org/10.1590/1413-812320212612.26092020
https://doi.org/10.1590/1413-81232021261...
, and FS/mild FI2424 Santos NF, Lira PIC, Tavares FCLP, Leal VS, Oliveira JS, Pessoa JT, et al. Overweight in adolescents: food insecurity and multifactoriality in semiarid regions of Pernambuco. Rev Paul Pediatr 2019; 38: e2018177. https://doi.org/10.1590/1984-0462/2020/38/2018177
https://doi.org/10.1590/1984-0462/2020/3...
and overweight. An association between overweight and FI (FS x FI) was also found in women2525 Costa NS, Santos MO, Carvalho CPO, Assunção ML, Ferreira HS. Prevalence and factors associated with food insecurity in the context of the economic crisis in Brazil. Curr Dev Nutr 2017; 1(10): e000869. https://doi.org/10.3945/cdn.117.000869
https://doi.org/10.3945/cdn.117.000869...
and in adults and older adults, regardless of sex2626 Pequeno NPF, Cabral NLA, Oliveira AGRC, Crispim SP, Rocha C, Marchioni DM, et al. Chronic diseases and emotional disorders are associated with low perception of quality of life in food insecurity/security. Front Public Health 2022; 10: 893601. https://doi.org/10.3389/fpubh.2022.893601
https://doi.org/10.3389/fpubh.2022.89360...
.

Regarding obesity, an association of this condition was found with all levels of FI2727 Domingos T, Sichieri R, Salles-Costa, R. Sex differences in the relationship between food insecurity and weight status in Brazil. Br J Nutr 2022; 1-19. https://doi.org/10.1017/S0007114522001192
https://doi.org/10.1017/S000711452200119...
and moderate FI55 Schlüssel MM, Silva AAM, Pérez-Escamilla R, Kac G. Household food insecurity and excess weight/obesity among Brazilian women and children: a life-course approach. Cad Saude Pública 2013; 29(2): 219-26. https://doi.org/10.1590/S0102-311X2013000200003
https://doi.org/10.1590/S0102-311X201300...
in women. Furthermore, an association between the moderate FI variable2828 Velásquez-Melendez G, Schlüssel MM, Brito AS, Silva AA, Lopes-Filho JD, Kac G. Mild but not light or severe food insecurity is associated with obesity among Brazilian women. J Nutr 2011; 141(5): 898-902. https://doi.org/10.3945/jn.110.135046
https://doi.org/10.3945/jn.110.135046...
and obesity in women was observed. An association between obesity and FI was also identified among those responsible for the household2929 Dias MS, Dumith SC, Vaz JS, Susin LRO. Insegurança alimentar em um município do extremo sul do Rio Grande do Sul, 2016: um estudo de base populacional. Epidemiol Serv Saúde 2020; 29(2): e2019204. https://doi.org/10.5123/S1679-49742020000200007
https://doi.org/10.5123/S1679-4974202000...
and it was associated with mild FI in older adults3030 Souza BFNJ, Marín-León L. Insegurança alimentar em idosos: estudo transversal com usuários de restaurante popular. Rev Nutr 2013; 26(6): 679-91. https://doi.org/10.1590/S1415-52732013000600007
https://doi.org/10.1590/S1415-5273201300...
. In addition, we noticed an association between severe FI and the double burden of malnutrition, that is, an overweight mother and stunted children in the same household3131 Gubert MB, Spaniol AM, Segall-Corrêa AM, Pérez-Escamilla R. Understanding the double burden of malnutrition in food insecure households in Brazil. Matern Child Nutr 2017; 13(3): e12347. https://doi.org/10.1111/mcn.12347
https://doi.org/10.1111/mcn.12347...
.

Conversely, the lower prevalence of abdominal obesity and hypertriglyceridemia in users with hypertension and/or DM seen at UBS was associated with FI99 Vasconcelos SML, Torres NCP, Silva PMC, Santos TMP, Silva JVL, Omena CMB, et al. Insegurança alimentar em domicílios de indivíduos portadores de hipertensão e/ou diabetes. Int J Cardiovasc Sci 2015; 28(2): 114-21., and the lower prevalence of overweight and obesity was associated with moderate and severe FI in men2929 Dias MS, Dumith SC, Vaz JS, Susin LRO. Insegurança alimentar em um município do extremo sul do Rio Grande do Sul, 2016: um estudo de base populacional. Epidemiol Serv Saúde 2020; 29(2): e2019204. https://doi.org/10.5123/S1679-49742020000200007
https://doi.org/10.5123/S1679-4974202000...
. FI was associated with lower probability of being overweight in schoolchildren over 5 years of age3232 Vicenzi K, Henn RL, Weber AP, Backes V, Paniz VMV, Donatti T, et al. Insegurança alimentar e excesso de peso em escolares do primeiro ano do Ensino Fundamental da rede municipal de São Leopoldo, Rio Grande do Sul, Brasil. Cad Saúde Pública 2015; 31(5): 1084-94. https://doi.org/10.1590/0102-311X00055914
https://doi.org/10.1590/0102-311X0005591...
, and underweight was associated with moderate/severe FI in children under 5 years of age3333 Poblacion AP, Cook JT, Marín-León L, Segall-Corrêa AM, Silveira JAC, Konstantyner T, et al. Food insecurity and the negative impact on Brazilian children's health-why does food security matter for our future prosperity? Brazilian National Survey (PNDS 2006/07). Food Nutr Bull 2016; 37(4): 585-98. https://doi.org/10.1177/0379572116664167
https://doi.org/10.1177/0379572116664167...
.

Among the included articles, 13 did not demonstrate an association between FI and indicators related to NCDs3434 Domingos TB, Pereira AF, Yokoo EM, Salles-Costa R. Low fruit consumption and omission of daily meals as risk factors for increased blood pressure in adults. Br J Nutr 2016; 116(4): 683-91. https://doi.org/10.1017/S0007114516002397
https://doi.org/10.1017/S000711451600239...
4646 Guerra LDS, Espinosa MM, Bezerra ACD, Guimarães LV, Lima-Lopes MA. Insegurança alimentar em domicílios com adolescentes da Amazônia Legal Brasileira: prevalência e fatores associados. Cad Saúde Pública 2013; 29(2): 335-48. https://doi.org/10.1590/S0102-311X2013000200020
https://doi.org/10.1590/S0102-311X201300...
, eight of which were carried out with children and adolescents3737 Kac G, Schlüssel MM, Pérez-Escamilla R, Velásquez-Melendez G, Silva AAM. Household food insecurity is not associated with BMI for age or weight for height among Brazilian children aged 0–60 months. PLoS One 2012; 7(9): e45747. https://doi.org/10.1371/journal.pone.0045747
https://doi.org/10.1371/journal.pone.004...
4343 Gubert M, Spaniol A, Bortolini G, Pérez-Escamilla, R. Household food insecurity, nutritional status and morbidity in Brazilian children. Public Health Nutr 2016; 19(12): 2240-5. https://doi.org/10.1017/S1368980016000239
https://doi.org/10.1017/S136898001600023...
,4646 Guerra LDS, Espinosa MM, Bezerra ACD, Guimarães LV, Lima-Lopes MA. Insegurança alimentar em domicílios com adolescentes da Amazônia Legal Brasileira: prevalência e fatores associados. Cad Saúde Pública 2013; 29(2): 335-48. https://doi.org/10.1590/S0102-311X2013000200020
https://doi.org/10.1590/S0102-311X201300...
. These articles are presented in Supplementary Material.

With the hypotheses and justifications used by the authors of the included studies to explain the association of FI with obesity, we proposed a theoretical model with the main paths of this association, presented in Figure 2.

Figure 2
Conceptual model of the paths used in the included articles to explain the association of food insecurity with obesity and other chronic noncommunicable diseases. Systematic review, 2023.

DISCUSSION

The main objective of this systematic review was to use the successful history of studies on FI to determine and document evidence on the association of FI with NCDs in the context of the Brazilian population. According to the findings, there is an association between FI and overweight in adolescents, adults, and older adults of both sexes and with obesity in women and older adults.

The association of FI with NCDs has been addressed in systematic reviews. Miguel et al.4747 Miguel ES, Lopes SO, Araújo SP, Priore SE, Alfenas RCG, Hermsdorff HHM. Association between food insecurity and cardiometabolic risk in adults and the elderly: a systematic review. J Glob Health 2020; 10(2): 020402. https://doi.org/10.7189/jogh.10.020402
https://doi.org/10.7189/jogh.10.020402...
studied the relationship between FI and cardiometabolic risk factors in adults and older adults. The review included 11 studies with proxy measures for NCDs, showing the existence of a direct association between FI and conditions such as overweight, hypertension, DM, dyslipidemia, and stress. Regarding DM, Abdurahman et al.4848 Abdurahman AA, Chaka EE, Nedjat S, Dorosty AR, Majdzadeh R. The association of household food insecurity with the risk of type 2 diabetes mellitus in adults: a systematic review and meta-analysis. Eur J Nutr 2019; 58(4): 1341-50. https://doi.org/10.1007/s00394-018-1705-2
https://doi.org/10.1007/s00394-018-1705-...
identified that FI was associated with type 2 DM; however, they highlighted that in Canada the choice of the FI measurement instrument influences the effect on the chance of developing DM. Conversely, Beltrán et al.4949 Beltrán S, Arenas DJ, Pharel M, Montgomery C, Lopez-Hinojosa I, DeLisser HM. Food insecurity, type 2 diabetes, and hyperglycaemia: a systematic review and meta-analysis. Endocrinol Diabetes Metab 2022; 5(1): e00315. https://doi.org/10.1002/edm2.315
https://doi.org/10.1002/edm2.315...
found no association between DM and FI. For cardiovascular diseases, Liu and Eicher-Miller5050 Liu Y, Eicher-Miller HA. Food insecurity and cardiovascular disease risk. Curr Atheroscler Rep 2021; 23(6): 24. https://doi.org/10.1007/s11883-021-00923-6
https://doi.org/10.1007/s11883-021-00923...
observed an association of FI with hypertension, coronary heart disease, and heart attack in North Americans over 17 years of age.

Beltrán et al.5151 Beltrán S, Pharel M, Montgomery CT, López-Hinojosa IJ, Arenas DJ, DeLisser HM. Food insecurity and hypertension: a systematic review and meta-analysis. PLoS One 2020; 15(11): e0241628. https://doi.org/10.1371/journal.pone.0241628
https://doi.org/10.1371/journal.pone.024...
found an association between FI in adults with self-reported hypertension, but this association was not found when the authors made the diagnosis by measuring blood pressure or reviewing medical records. Arenas et al.5252 Arenas DJ, Beltrán S, Montgomery C, Pharel M, Lopez-Hinojosa I, Vilá-Arroyo G, et al. A systematic review and meta-analysis of food insecurity and dyslipidemia. J Am Board Fam Med 2022; 35(4): 656-67. https://doi.org/10.3122/jabfm.2022.04.210413
https://doi.org/10.3122/jabfm.2022.04.21...
studied the association of FI with dyslipidemia, and the results did not show an association between FI and dyslipidemia measured by laboratory lipid analysis, but individuals on FI were more likely to self-report previous diagnoses of dyslipidemia. Finally, on the international scene, the association of FI with obesity has also been documented in previous systematic reviews5353 Farrell P, Thow AM, Abimbola S, Faruqui N, Negin J. How food insecurity could lead to obesity in LMICs: when not enough is too much: a realist review of how food insecurity could lead to obesity in low-and middle-income countries. Health Promot Int 2018; 33(5): 812-26. https://doi.org/10.1093/heapro/dax026
https://doi.org/10.1093/heapro/dax026...
5656 Eskandari F, Lake AA, Rose K, Butler M, O'Malley C. A mixed-method systematic review and meta-analysis of the influences of food environments and food insecurity on obesity in high-income countries. Food Sci Nutr 2022; 10(11): 3689-723. https://doi.org/10.1002/fsn3.2969
https://doi.org/10.1002/fsn3.2969...
.

In this review, dedicated to studying the Brazilian population, despite the broad search spectrum, the significant majority of available studies addressed nutritional status and analyses of the condition of overweight and obesity related to FI, thus highlighting the small volume of studies with a population at risk or affected by hypertension, DM, dyslipidemia, and cardiovascular diseases. In addition, we observed little diversity of risk indicators, with most studies using only BMI.

As noted in this review, authors of other reviews have documented the association of FI with overweight/obesity in the Brazilian population. Morais et al.5757 Morais DC, Dutra LV, Franceschini SCC, Priore SE. Insegurança alimentar e indicadores antropométricos, dietéticos e sociais em estudos brasileiros: uma revisão sistemática. Ciênc Saúde Colet 2014; 19(5): 1475-88. https://doi.org/10.1590/1413-81232014195.13012013
https://doi.org/10.1590/1413-81232014195...
,5858 Morais DC, Lopes SO, Priore SE. Indicadores de avaliação da Insegurança Alimentar e Nutricional e fatores associados: revisão sistemática. Ciênc Saúde Colet 2020; 25(7): 2687-700. https://doi.org/10.1590/1413-81232020257.23672018
https://doi.org/10.1590/1413-81232020257...
observed an association between FI and overweight and obesity in the Brazilian population; however, with regard to the rural population, Trivellato et al.5959 Trivellato PT, Morais DC, Lopes SO, Miguel ES, Franceschini SCC, Priore SE. Insegurança alimentar e nutricional em famílias do meio rural brasileiro: revisão sistemática. Ciênc Saúde Colet 2019; 24(3): 865-74. https://doi.org/10.1590/1413-81232018243.05352017
https://doi.org/10.1590/1413-81232018243...
found no association between nutritional status (overweight, underweight, and/or chronic malnutrition) and FI.

In Figure 2 we illustrate a theoretical model containing the main paths followed by the authors of the included studies to explain the association of FI with obesity, namely:

  1. Malnutrition;

  2. Coping mechanisms and coexistence with FI; and

  3. Sedentary lifestyle.

The path most used by the authors to explain this association was malnutrition, that is, in families that experience FI there is the purchase and consumption of low-cost foods, such as processed and ultra-processed foods, and, consequently, an increase in energy, sugar, fat, and salt intake.

The second path most used by the authors is based on the existence of coping mechanisms and coexistence with FI within families, such as the hunger-satiety cycle, characterized by restrictive periods of underconsumption followed by compensatory periods of overconsumption. This mechanism predisposes metabolic and psychological alterations, such as fear, uncertainty, restriction, deprivation, anxiety, and depression, configuring acute and chronic stress conditions that alter eating behavior and favor the development of obesity.

The least used path was sedentary lifestyle, which theorizes that the state of physical inactivity of people on FI, resulting from their socioeconomic status, favors the development of obesity. In the three paths used in the included articles, obesity appears as a factor that mediates the development process of other NCDs.

Accordingly, at an international level, researchers also use these paths to explain the association5353 Farrell P, Thow AM, Abimbola S, Faruqui N, Negin J. How food insecurity could lead to obesity in LMICs: when not enough is too much: a realist review of how food insecurity could lead to obesity in low-and middle-income countries. Health Promot Int 2018; 33(5): 812-26. https://doi.org/10.1093/heapro/dax026
https://doi.org/10.1093/heapro/dax026...
,5454 Moradi S, Mirzababaei A, Dadfarma A, Rezaei S, Mohammadi H, Jannat B, et al. Food insecurity and adult weight abnormality risk: a systematic review and meta-analysis. Eur J Nutr 2019; 58(1): 45-61. https://doi.org/10.1007/s00394-018-1819-6
https://doi.org/10.1007/s00394-018-1819-...
,6060 Nettle D, Andrews C, Bateson M. Food insecurity as a driver of obesity in humans: the insurance hypothesis. Behav Brain Sci 2017; 40: e105. https://doi.org/10.1017/S0140525X16000947
https://doi.org/10.1017/S0140525X1600094...
,6161 Carvajal-Aldaz D, Cucalon G, Ordonez C. Food insecurity as a risk factor for obesity: a review. Front Nutr 2022; 9: 1012734. https://doi.org/10.3389/fnut.2022.1012734
https://doi.org/10.3389/fnut.2022.101273...
. The relationship between FI and malnutrition is documented in the literature. Authors describe that the presence of FI is accompanied by less variety of foods, greater energy intake, and monotonous diets, that is, it is not just the absence of food, but also access to low-quality foods4747 Miguel ES, Lopes SO, Araújo SP, Priore SE, Alfenas RCG, Hermsdorff HHM. Association between food insecurity and cardiometabolic risk in adults and the elderly: a systematic review. J Glob Health 2020; 10(2): 020402. https://doi.org/10.7189/jogh.10.020402
https://doi.org/10.7189/jogh.10.020402...
,5757 Morais DC, Dutra LV, Franceschini SCC, Priore SE. Insegurança alimentar e indicadores antropométricos, dietéticos e sociais em estudos brasileiros: uma revisão sistemática. Ciênc Saúde Colet 2014; 19(5): 1475-88. https://doi.org/10.1590/1413-81232014195.13012013
https://doi.org/10.1590/1413-81232014195...
,6262 Panigassi G, Segall-Corrêa AM, Marin-León L, Pérez-Escamilla R, Maranha LK, Sampaio MFA. Insegurança alimentar intrafamiliar e perfil de consumo de alimentos. Rev Nutr 2008; 21(supl): 135s-144s. https://doi.org/10.1590/S1415-52732008000700012
https://doi.org/10.1590/S1415-5273200800...
,6363 Castro MA, Fontanelli MM, Nogueira-de-Almeida CA, Fisberg M. Food insecurity reduces the chance of following a nutrient-dense dietary pattern by Brazilian adults: insights from a nationwide cross-sectional survey. Nutrients 2022; 14(10): 2126. https://doi.org/10.3390/nu14102126
https://doi.org/10.3390/nu14102126...
.

Researchers point to the presence of obesity as the main path and mediator that connects FI to the development of other NCDs such as DM and SAH. Nonetheless, authors highlight the importance of analyzing the potential negative effects of FI on health, regardless of obesity5050 Liu Y, Eicher-Miller HA. Food insecurity and cardiovascular disease risk. Curr Atheroscler Rep 2021; 23(6): 24. https://doi.org/10.1007/s11883-021-00923-6
https://doi.org/10.1007/s11883-021-00923...
,6464 Weaver LJ, Fasel CB. A systematic review of the literature on the relationships between chronic diseases and food insecurity. Food Nutr Sci 2018; 9(5): 519. https://doi.org/10.4236/fns.2018.95040
https://doi.org/10.4236/fns.2018.95040...
,6565 Militao EMA, Salvador EM, Uthman OA, Vinberg S, Macassa G. Food insecurity and health outcomes other than malnutrition in southern Africa: a descriptive systematic review. Int J Environ Res Public Health 2022; 19(9): 5082. https://doi.org/10.3390/ijerph19095082
https://doi.org/10.3390/ijerph19095082...
.

It is worth highlighting the need to deepen the debate on the association of FI with NCDs, incorporating into studies variables related to social inequalities, and with regard to access to health, working conditions and the food environment, topics that contribute to expanding the context of discussion and the network of relevant factors for the debate, both on FI and NCDs — especially in the Brazilian scenario, marked by profound social and regional inequality.

Therefore, the association between FI and NCDs is complex. The emergence of a chronic condition, such as obesity, DM, and SAH, results from a broad set of determining factors and is also related to previous and continuous exposure to these determinants. Nevertheless, it is noteworthy that in the studies included in the review, the population's exposure time to FI was not considered, due to the cross-sectional nature of the studies.

Hence, the lack of longitudinal studies that analyze the development of NCDs from exposure to FI is an important scientific gap. Conversely, according to the studies, an association between FI and the risk/presence of NCDs was established, that is, individuals who live with these conditions also suffer from food deprivation, a context that is expressed as an important limiting factor in the implementation and adoption of safety measures of care and treatment of these chronic conditions.

It should be noted that, at a global level, FI measurement methods differ between countries/regions, especially in the FI reference time, also making it difficult to compare evidence. Another complexity related to the analysis of FI and NCDs is the social and economic context of each country, in such a way that differences in agrifood systems, development levels, and the state of nutritional transition must be considered in future studies and for comparison with observed results in Brazil.

The articles included in this review did not produce evidence on other NCDs of interest to public health in Brazil, such as DM and SAH, highlighting an important scientific gap and the need to develop a research agenda on the topic that prioritizes longitudinal studies, aiming to produce evidence of causality in the relationship between FI and NCDs.

The evidence produced here reinforces that access to food must be guaranteed, with health-promoting practices, and provides support for focusing public health interventions and programs on combating FI and promoting, preventing, and controlling NCDs. Health services must be aware of the high prevalence of FI in the Brazilian population and how this scenario can impact the care offered to individuals affected by NCDs. Investments in interventions and public programs related to the topic of the association of FI with NCDs are in line with the UN Sustainable Development Goals, assumed by Brazil for the 2030 Agenda.

Therefore, despite its successful history of studies on FI, in Brazil the association of FI with NCDs remains little addressed. The reviewed studies corroborate evidence of an association between FI and overweight in all age groups, and obesity among women and older adults. Therefore, public interventions and a strong agenda to combat hunger combined with health-promoting practices and nutritional care are necessary, especially in Primary Health Care. We suggest investments are made in studies that address the topic of the association of FI with NCDs, in addition to obesity, mainly with a longitudinal design.

  • FUNDING:

    The graduate degree authors had their scholarships funded by the Coordination for the Improvement of Higher Education Personnel (CAPES).

ACKNOWLEDGMENTS:

The authors would like to thank to the Emergency Graduate Degree Development Program for Strategic Consolidation of Stricto Sensu Graduate Degree Programs, grant No.: 1782/2022, for paying for the editing fees for this article.

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Publication Dates

  • Publication in this collection
    12 Aug 2024
  • Date of issue
    2024

History

  • Received
    20 Jan 2024
  • Reviewed
    18 Apr 2024
  • Accepted
    07 May 2024
Associação Brasileira de Pós -Graduação em Saúde Coletiva São Paulo - SP - Brazil
E-mail: revbrepi@usp.br