Prevalence of the Metabolic Syndrome and its components in the Brazilian adult population

Laís Vanessa Assunção Oliveira Bruna Nicole Soares dos Santos Ísis Eloah Machado Deborah Carvalho Malta Gustavo Velasquez-Melendez Mariana Santos Felisbino-Mendes About the authors

Abstract

We estimated the prevalence of the Metabolic Syndrome (MetS) and its components in the Brazilian population according to sociodemographic factors. This is a cross-sectional population-based study that used laboratory data from the National Health Survey. We estimated the prevalence of MetS and its components with 95% confidence intervals and the unadjusted and adjusted prevalence ratio (PR) with the Poisson regression. MetS prevalence ratio was 38.4%. High waist circumference (WC) (65.5%) and low HDL cholesterol (49.4%) were the most prevalent components, including in the youngest people. MetS and its components were more frequent among women (41.8%), individuals with low schooling (47.5%), and older adults (66.1%). In the adjusted analysis, females (PR = 1.16; 95% CI 1.08-1.24), older adults (PR = 3.69; 95% CI 3.26-4.17), and low schooling (PR = 1.32; 95% CI 1.17-1.49) were associated with MetS. MetS was prevalent in the Brazilian population, especially among women, individuals with low schooling, and older adults. High WC and low HDL cholesterol were the most prevalent components, with the aggravating high prevalence factor in young adults. These findings reveal the need to consider laboratory data for a more accurate analysis of this condition, which can be challenging at the national level.

Key words
Metabolic syndrome; Waist circumference; Dyslipidemias; Risk factors; Chronic disease

Introduction

Metabolic Syndrome (MetS) is characterized by complex metabolic changes and has been widely studied worldwide for its adverse repercussions on individual health and its strong association with cardiovascular diseases11 Neergaard JS, Laursen JM, Hansen HB, Christiansen C, Beck-nielsen H, Karsdal MA, Brix S, Henriksen K. Metabolic syndrome and subsequent risk of type 2 diabetes and cardiovascular disease in elderly women. Medicine 2016; 95:36(e4806). and type 2 diabetes11 Neergaard JS, Laursen JM, Hansen HB, Christiansen C, Beck-nielsen H, Karsdal MA, Brix S, Henriksen K. Metabolic syndrome and subsequent risk of type 2 diabetes and cardiovascular disease in elderly women. Medicine 2016; 95:36(e4806).,22 Neto JCGL, Xavier MA, Borges JWP, Araújo MFM, Damasceno MMC, Freitas RWJF. Prevalence of Metabolic Syndrome in individuals with Type 2 Diabetes Mellitus. Rev Bras Enferm 2017; 70(2):265-270.. It involves the aggregation of arterial hypertension, abdominal obesity, dyslipidemia, and impaired glucose metabolism33 Alberti K, Eckel R, Grundy S, Zimmet P, Cleeman J, Donato K, Fruchart JC, James WPT, Loria CM, Smith Junior SC, International Diabetes Federation Task Force on Epidemiology and Prevention; Hational Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; International Association for the Study of Obesity. Harmonizing the metabolic syndrome: A joint interim statement of the international diabetes federation task force on epidemiology and prevention; National heart, lung, and blood institute; American heart association; World heart federation; International. Circulation 2009; 120(16):1640-1645.. In general, studies estimate the prevalence of MetS from the consensus defined by the Adult Treatment Panel III (ATP III)44 Executive Summary of the Third Report of the National Cholesterol Education Program (NCEP). Expert Panel on Detection, Evaluation, and Treat-ment of High Blood Cholesterol in Adults (Adult Treatment Panel III). JAMA 2001; 285(19):2486-2497., although a recommendation for standardized criteria and better comparison of studies33 Alberti K, Eckel R, Grundy S, Zimmet P, Cleeman J, Donato K, Fruchart JC, James WPT, Loria CM, Smith Junior SC, International Diabetes Federation Task Force on Epidemiology and Prevention; Hational Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; International Association for the Study of Obesity. Harmonizing the metabolic syndrome: A joint interim statement of the international diabetes federation task force on epidemiology and prevention; National heart, lung, and blood institute; American heart association; World heart federation; International. Circulation 2009; 120(16):1640-1645. is already in place.

The MetS phenotype enables easy identification of individuals at risk for NCDs55 Márquez-Sandoval F, Macedo-Ojeda G, Viramontes-Hörner D, Ballart JDF, Salvadó JS, Vizmanos B. The prevalence of metabolic syndrome in Latin America: A systematic review. Public Health Nutrition 2011; 14(10):1702-1713.,66 Vidigal FC, Bressan J, Babio N, Salas-Salvadó J. Prevalence of metabolic syndrome in Brazilian adults: a systematic review. BMC Public Health 2013; 13:1198., which are the leading cause of the Brazilian population’s morbimortality, responsible for 76% of deaths in 2017 in the country77 IHME. Global Burden of Disease Study 2017 (GBD 2017) Results [Internet]. The Institute for Health Metrics and Evaluation (IHME) 2020. [cited 2019 Dez 15]. Available at: Http://vizhub.healthdata.org/gbd-compare%3E
Http://vizhub.healthdata.org/gbd-compare...
. Also, the risk of MetS-related adverse outcomes is known to be synergistically higher than if its component factors are estimated separately66 Vidigal FC, Bressan J, Babio N, Salas-Salvadó J. Prevalence of metabolic syndrome in Brazilian adults: a systematic review. BMC Public Health 2013; 13:1198..

A MetS prevalence of 29.6%66 Vidigal FC, Bressan J, Babio N, Salas-Salvadó J. Prevalence of metabolic syndrome in Brazilian adults: a systematic review. BMC Public Health 2013; 13:1198. was recorded in the Brazilian adult population, reaching more than 40% in the age groups older than 60 years88 Vieira EC, Peixoto MRG, Silveira EA. Prevalência e fatores associados à Síndrome Metabólica em idosos usuários do Sistema Único de Saúde. Rev Bras Epidemiol 2014; 17(4):805-817.. A Brazilian cohort also showed a MetS prevalence of 44%99 Vieira BA, Luft VC, Schmidt MI, Chambless LE, Chor D, Barreto SM, Duncan BB. Timing and type of alcohol consumption and the metabolic syndrome - ELSA-Brasil. PLoS One 2016; 11(9):1-17.. The lowest prevalence (9%) was estimated in a survey with national representativeness, well below that observed in most publications1010 Ramires EKNM, Menezes RCE, Longo-Silva G, Santos TG, Marinho PM, Silveira JAC. Prevalência e Fatores Associados com a Síndrome Metabólica na População Adulta Brasileira: Pesquisa Nacional de Saúde - 2013. Arq Bras Cardiol 2018; 110(5):455-466..

Some of the components were self-reported in these studies, leading to an underestimated prevalence of MetS and its components1010 Ramires EKNM, Menezes RCE, Longo-Silva G, Santos TG, Marinho PM, Silveira JAC. Prevalência e Fatores Associados com a Síndrome Metabólica na População Adulta Brasileira: Pesquisa Nacional de Saúde - 2013. Arq Bras Cardiol 2018; 110(5):455-466.,1111 Sá NNB, Moura EC. Fatores associados à carga de doenças da síndrome metabólica entre adultos brasileiros. Cad Saude Publica 2010; 26(9):1853-1862.. Measuring blood pressure, waist circumference (WC), and three other factors (triglycerides, HDL cholesterol, and fasting glucose) requires direct measurements to obtain more accurate and reliable estimates. Studies with direct measures were only carried out in restricted populations and small samples with or without random sampling88 Vieira EC, Peixoto MRG, Silveira EA. Prevalência e fatores associados à Síndrome Metabólica em idosos usuários do Sistema Único de Saúde. Rev Bras Epidemiol 2014; 17(4):805-817.,1212 Bortoletto MSS, Souza RKT de, Cabrera MAS, González AD. Síndrome metabólica, componentes e fatores associados em adultos de 40 anos ou mais de um município da Região Sul do Brasil. Cad Saúde Coletiva 2016; 24(1):32-40.. Another relevant aspect found was that population subgroups that were more vulnerable from the sociodemographic viewpoint and with inadequate lifestyles had higher MetS1010 Ramires EKNM, Menezes RCE, Longo-Silva G, Santos TG, Marinho PM, Silveira JAC. Prevalência e Fatores Associados com a Síndrome Metabólica na População Adulta Brasileira: Pesquisa Nacional de Saúde - 2013. Arq Bras Cardiol 2018; 110(5):455-466.,1111 Sá NNB, Moura EC. Fatores associados à carga de doenças da síndrome metabólica entre adultos brasileiros. Cad Saude Publica 2010; 26(9):1853-1862.,1313 Pimenta AM, Gazzinelli A, Velásquez-Meléndez G. Prevalência da síndrome metabólica e seus fatores associados em área rural de Minas Gerais (MG, Brasil). Cien Saude Colet 2011; 16(7):3297-3306..

Obtaining more reliable estimates of the prevalence of MetS in the Brazilian adult population depends on the use of biochemical and anthropometric data with national representation. However, few population studies use these types of data. Besides the scarcity of studies, we note the use of different criteria to define MetS in the scientific literature, hindering comparability between different populations.

Another aspect to be considered in this context is the high estimated global burden of NCDs in the country1414 Marinho F, Passos VMA, Malta DC, França EB, Abreu DMX, Araújo VEM, Bustamante-Teixeira MT, Camargos PAM, Cunha CC, Duncan BB, Felisbino-Mendes MS, Guerra MR, Guimarães MDC, Lotufo PA, Marcenes W, PPV Oliveira, Pedroso MM, Ribeiro AL, Schmidt MI, Teixeira RA, Vasconcelos AMN, Barreto ML, Bensenor IM, Brant LCC, Claro RM, Pereira AC, Cousin E, Curado MP, Santos KPB, Faro A, Ferri CP, Furtado JM, Gall J, Glenn SD, Goulart AC, LH Ishitani, Kieling C, Ladeira RM, Machado IE, Martins SCO, Martins-Melo FR, Melo APS, Miller-Petrie MK, Mooney MD, Nunes BP, Palone MRT, Pereira CC, Rasella D, Ray SE, Roever L, Saldanha RF, Santos IS, Schneider IJC, Silva DAS, Silveira DGA, Soares Filho AM, Sousa TCM, Szwarcwald CL, Traebert J, Velasquez-Melendez G, Wang Y, Lozano R, Murray CJL, Naghavi M. Burden of disease in Brazil, 1990-2016: a systematic subnational analysis for the Global Burden of Disease Study 2016. Lancet 2018; 392(10149):760-775., which requires measuring the magnitude of MetS and its distribution according to sociodemographic factors, such as gender, age, schooling, and household situation, to assess possible inequalities in this condition. Thus, this study aimed to estimate MetS prevalence in the Brazilian population according to sociodemographic factors, using a consensus standardized by several committees and accepted internationally33 Alberti K, Eckel R, Grundy S, Zimmet P, Cleeman J, Donato K, Fruchart JC, James WPT, Loria CM, Smith Junior SC, International Diabetes Federation Task Force on Epidemiology and Prevention; Hational Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; International Association for the Study of Obesity. Harmonizing the metabolic syndrome: A joint interim statement of the international diabetes federation task force on epidemiology and prevention; National heart, lung, and blood institute; American heart association; World heart federation; International. Circulation 2009; 120(16):1640-1645..

Methods

Design and study population

This is an analytical cross-sectional study that used data from the 2013 National Health Survey (PNS), including data on laboratory tests collected between 2014 and 2015. The National Health Survey carried out in 2013 was a nationwide home-based survey developed in a partnership between the Ministry of Health, the Oswaldo Cruz Foundation (Fiocruz), and the Brazilian Institute of Geography and Statistics (IBGE). The PNS sample was selected by clusters in three stages through simple random sampling: census tracts, a fixed number of private households, and a resident aged 18 years or older were selected for each household, with an equiprobability of selection among individuals residing in the same household, to answer the individual questionnaire1515 Malta DC, Duncan BB, Schmidt MI, Machado IE, Silva AG, Bernal RTI, Pereira CA, Damacena GN, Stopa SR, Rosenfeld LG, Szwarcwald CL. Prevalência de diabetes mellitus determinada pela hemoglobina glicada na população adulta brasileira, Pesquisa Nacional de Saúde. Rev Bras Epidemiol 2019; 22(Supl. 2):E190006.SUPL.2.,1616 Damacena GN, Szwarcwald CL, Malta DC, Júnior PRBS, Vieira MLFP, Pereira CA, Morais Neto OL, Silva Júnior JB. O processo de desenvolvimento da Pesquisa Nacional de Saúde no Brasil, 2013. Epidemiol Serv Saúde 2015; 24(2):197-206.. A total of 81,167 households was visited, of which 69,994 had residents1616 Damacena GN, Szwarcwald CL, Malta DC, Júnior PRBS, Vieira MLFP, Pereira CA, Morais Neto OL, Silva Júnior JB. O processo de desenvolvimento da Pesquisa Nacional de Saúde no Brasil, 2013. Epidemiol Serv Saúde 2015; 24(2):197-206.. In all, 64,348 household interviews and 60,202 individual interviews with the selected household residents1616 Damacena GN, Szwarcwald CL, Malta DC, Júnior PRBS, Vieira MLFP, Pereira CA, Morais Neto OL, Silva Júnior JB. O processo de desenvolvimento da Pesquisa Nacional de Saúde no Brasil, 2013. Epidemiol Serv Saúde 2015; 24(2):197-206.,1717 Szwarcwald CL, Malta DC, Souza Júnior PRB, Almeida WS, Damacena GN, Pereira CA, Rosenfeld LG. Exames laboratoriais da Pesquisa Nacional de Saúde: metodologia de amostragem, coleta e análise dos dados. Rev Bras Epidemiol 2019; 22(Supl. 2): E190004.SUPL.2. were conducted.

A subsample of 25% of the census sectors surveyed was planned to collect biological material from the residents selected in the third stage of the PNS. In this study, it consisted of 8,952 people. This sample included post-stratification weights by gender, age, schooling, and region to obtain population estimates and establish representativeness of the Brazilian adult population1717 Szwarcwald CL, Malta DC, Souza Júnior PRB, Almeida WS, Damacena GN, Pereira CA, Rosenfeld LG. Exames laboratoriais da Pesquisa Nacional de Saúde: metodologia de amostragem, coleta e análise dos dados. Rev Bras Epidemiol 2019; 22(Supl. 2): E190004.SUPL.2..

Data collection

In 2013, the selected adults were informed about blood and urine collection and measurements. In the first phase, weight, height, blood pressure, WC were measured for all subjects selected for individual interviews. In 2014 and 2015, a new visit was made to the participants’ homes selected for the collection of biological material. The biological material was collected by employees of partner laboratories of the Ministry of Health, accredited in the context of the Proadi-SUS (Support Program for Institutional Development of the Unified Health System)1717 Szwarcwald CL, Malta DC, Souza Júnior PRB, Almeida WS, Damacena GN, Pereira CA, Rosenfeld LG. Exames laboratoriais da Pesquisa Nacional de Saúde: metodologia de amostragem, coleta e análise dos dados. Rev Bras Epidemiol 2019; 22(Supl. 2): E190004.SUPL.2..

Study variables

MetS prevalence was estimated by the simultaneous presence of at least three of the five factors defined based on an international committee’s criteria33 Alberti K, Eckel R, Grundy S, Zimmet P, Cleeman J, Donato K, Fruchart JC, James WPT, Loria CM, Smith Junior SC, International Diabetes Federation Task Force on Epidemiology and Prevention; Hational Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; International Association for the Study of Obesity. Harmonizing the metabolic syndrome: A joint interim statement of the international diabetes federation task force on epidemiology and prevention; National heart, lung, and blood institute; American heart association; World heart federation; International. Circulation 2009; 120(16):1640-1645.. HDL cholesterol <50mg/dl female / < 40mg/dl male; blood pressure ≥ 130/85 mmHg, WC ≥80cm female/ ≥ 90cm male33 Alberti K, Eckel R, Grundy S, Zimmet P, Cleeman J, Donato K, Fruchart JC, James WPT, Loria CM, Smith Junior SC, International Diabetes Federation Task Force on Epidemiology and Prevention; Hational Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; International Association for the Study of Obesity. Harmonizing the metabolic syndrome: A joint interim statement of the international diabetes federation task force on epidemiology and prevention; National heart, lung, and blood institute; American heart association; World heart federation; International. Circulation 2009; 120(16):1640-1645. were considered. In this study, instead of fasting blood glucose, we used the values of glycated hemoglobin ≥ 5.6 mmol/L1818 Kawamoto R, Kikuchi A, Akase T, Ninomiya D, Kumagi T. Usefulness of waist-to-height ratio in screening incident metabolic syndrome among Japanese community-dwelling elderly individuals. PLoS One 2019; 14(4):e0216069., and total cholesterol ≥ 200 mg/dl, replacing triglycerides44 Executive Summary of the Third Report of the National Cholesterol Education Program (NCEP). Expert Panel on Detection, Evaluation, and Treat-ment of High Blood Cholesterol in Adults (Adult Treatment Panel III). JAMA 2001; 285(19):2486-2497., since fasting was not required to perform PNS laboratory collection, a necessary condition for serum fasting glucose and triglyceride levels. Besides the diagnosis of MetS, these components and their simultaneous occurrence were analyzed individually.

Blood pressure

The most appropriate cuff was used for blood pressure measurement, according to the individual’s left arm circumference, by measuring the midpoint between the acromion and olecranon bones1919 Instituto Brasileiro de Geografia e Estatística (IBGE). Pesquisa Nacional de Saúde 2013: Manual de Antropometria. Rio de Janeiro: IBGE; 2013.. A digital device routinely calibrated (G-TECH model MA 100) was employed. Measurements were carried out with individuals at rest, who had not smoked or ingested any drink, except water, in the 30 minutes before the measurement, and had not performed any physical activity during one hour before the measurement. Also, individuals were asked to empty their bladder before measurement. BP measurements were taken with the subjects in a seated position after resting for at least five minutes. The subjects were instructed to remain relaxed and supported against the back of the chair, without crossing their legs and leaving their left arm bare and supported at their chest or heart level. Three BP measurements were performed with two-minute intervals1919 Instituto Brasileiro de Geografia e Estatística (IBGE). Pesquisa Nacional de Saúde 2013: Manual de Antropometria. Rio de Janeiro: IBGE; 2013..

Waist circumference

WC was measured at the midpoint between the last rib and the iliac crest with a measuring tape, with no clothing around the waist. The respondent remained with arms flexed and crossed in front of the chest, feet apart, and abdomen relaxed. The respondent was asked to inhale and release the air from the lungs, remaining so until the measurement was taken1919 Instituto Brasileiro de Geografia e Estatística (IBGE). Pesquisa Nacional de Saúde 2013: Manual de Antropometria. Rio de Janeiro: IBGE; 2013..

Blood collection

Blood collection was performed according to the Brazilian Society of Clinical Pathology Laboratory Medicine recommendations for collecting venous blood, whose technique is available on the research website on the biological material collection page2020 Fundação Instituto Oswaldo Cruz (Fiocruz). Pesquisa nacional de saúde. Rio de Janeiro: Fiocruz; 2013.. Peripheral blood was collected at any time of the day, without fasting1717 Szwarcwald CL, Malta DC, Souza Júnior PRB, Almeida WS, Damacena GN, Pereira CA, Rosenfeld LG. Exames laboratoriais da Pesquisa Nacional de Saúde: metodologia de amostragem, coleta e análise dos dados. Rev Bras Epidemiol 2019; 22(Supl. 2): E190004.SUPL.2.. Glycated hemoglobin was determined using high-performance liquid chromatography (HPLC) of a sample collected in a tube containing ethylenediaminetetraacetic acid (EDTA). Samples for analysis of total cholesterol and fractions were collected in serum gel tubes, waiting 30 minutes for clot retraction and subsequent centrifugation. An automated colorimetric enzymatic method performed the evaluation.

Data analysis

The prevalence of MetS and its components was estimated according to sociodemographic characteristics, and 95% confidence intervals were calculated. The sociodemographic variables were gender (male and female), age (18-39, 40-59, and 60 and over), schooling in years of study (12 or more, 9-11, and 0-8), ethnicity/skin color (white, yellow/indigenous, and black/brown) and place of residence (urban and rural). MetS prevalence ratio unadjusted and adjusted by sociodemographic variables was estimated using Poisson regression2121 Barros AJD, Hirakata VN. Alternatives for logistic regression in cross-sectional studies: an empirical comparison of models that directly estimate the prevalence ratio. BMC Med Res Methodol 2003; 3(1):21.. All analyses were performed using the Stata 14.0 statistical program, Survey module, considering the sample weight for population estimates.

Ethical aspects

The PNS was approved by the National Research Ethics Committee of the National Health Council, Ministry of Health1616 Damacena GN, Szwarcwald CL, Malta DC, Júnior PRBS, Vieira MLFP, Pereira CA, Morais Neto OL, Silva Júnior JB. O processo de desenvolvimento da Pesquisa Nacional de Saúde no Brasil, 2013. Epidemiol Serv Saúde 2015; 24(2):197-206.. Adult participation in the research was voluntary, and the confidentiality of information was assured. The individuals selected for the research provided informed consent for all research procedures, including interviews and blood and urine collection1717 Szwarcwald CL, Malta DC, Souza Júnior PRB, Almeida WS, Damacena GN, Pereira CA, Rosenfeld LG. Exames laboratoriais da Pesquisa Nacional de Saúde: metodologia de amostragem, coleta e análise dos dados. Rev Bras Epidemiol 2019; 22(Supl. 2): E190004.SUPL.2..

Results

The mean age of the studied population was 45.6 years (95% CI 45.1-46.0), with 52.9% (95% CI 51.5-54.3) females, 49.3% (95% CI % 47.9-50.7) reported 0-8 years of study, followed by 33.8% (95% CI 32.5-35.2) with 9-11 years of study, and 21.0% (95% CI 19.9-22.1) lived in rural areas.

Table 1 shows the prevalence of the components individually, the number of simultaneous factors, and the MetS by gender. MetS prevalence in the Brazilian population was 38.4% (95% CI 37.0-39.8). More than 70% of women had high WC (74.1%; 95% CI 72.4-75.7), and more than half had low HDL cholesterol (55.2%; 95% CI 53.4-57.1). These prevalence levels were higher than those found for men with elevated WC (56.0%; 95% CI 53.8-58.2) and low HDL cholesterol (42.9%; 95% CI 40.7-45.1). Women also had a higher prevalence of hypercholesterolemia and glycated hemoglobin ≥ 5.6 mmol/L. There was no difference in the prevalence of blood pressure ≥ 130/85 mmHg by gender. Women had a higher MetS prevalence (PR = 1.20 95% CI 1.12-1.30) than men (Figure 1). Women had a higher MetS prevalence (PR = 1.16 95% CI 1.08-1.24) than men, even after adjusting for gender, age, schooling, ethnicity/skin color, and place of residence (Figure 1).

Table 1
Prevalence of individual components, number of simultaneous factors, and diagnosis of the metabolic syndrome in the adult Brazilian population according to gender, PNS 2013, and PNS Laboratory 2014-2015.

Figure 1
Unadjusted (black) and adjusted (gray) Prevalence Ratio (PR) for Metabolic syndrome according to gender (A), and schooling (B), age (C), ethnicity/skin color (D), and place of residence (E), PNS 2013 and PNS Laboratory 2014-2015.

When analyzing MetS prevalence by age, we observed that the older the age, the greater the prevalence of MetS: 18-39 years (16.7%; 95% CI 15.0-18.6), 40-59 years (45.7%; 95% CI 43.5-48.0), 60 years or older (66.1%; 95% CI 63.5-68.6) (Table 2). The PR among individuals aged 40-59 years and 60 years and over was 2.73 (95% CI 2.42-3.08) and 3.95 (95% CI 3.52-4.44) compared to younger individuals (18-39 years), respectively. After adjustments, this relationship remained with little attenuation (Figure 1).

Table 2
Prevalence of individual components, number of simultaneous factors, and diagnosis of the metabolic syndrome in the Brazilian adult population according to age group, PNS 2013, and PNS Laboratory 2014-2015.

We observed that the lower the level of education, the higher the prevalence of MetS components. The prevalence of pressure values ≥ 130/85mmHg was almost twice in individuals with 0-8 years of study (41.9%; 95% CI 40.1-43.7) compared to those with 9-11 years (23.7%; 95% CI 21.7-25.9) and 12 years and over (21.4%; 95% CI 18.6-24.4). The less educated group had a higher MetS prevalence (47.5%; 95% CI 45.6-49.4), followed by 9-11 years (30.6%; 95% CI 28.3-33.1) and 12 years and over (27.4%; 95% CI 24.3-30.7) (Table 3). People with less schooling (0-8 years of study) had almost twice the prevalence of MetS than those with more schooling (12 years of study and over) (PR=1.73; 95% CI 1.53-1.96). In the fully adjusted model, this relationship remained at around 30% higher occurrence (PR = 1.32; 95% CI 1.17-1.49) (Figure 1).

Table 3
Prevalence of individual components, number of simultaneous factors, and diagnosis of the metabolic syndrome in the Brazilian adult population according to education, PNS 2013 and PNS Laboratory 2014-2015.

Regarding ethnicity/skin color, no significant difference was noted in the prevalence of MetS among white 39.7% (95% CI 37.5-41.9), black/brown 37.3% (95% CI 35.5-39.0), and yellow/indigenous 31.2% (95% CI 20.8-43.8) (p = 0.6515) (Table 4). The same was observed for place of residence, with MetS prevalence of 38.5% (95% CI 37.0-40.1) in the urban area and 37.7% (95% CI 34.9-40.7) in the rural area (data not shown, available on request).

Table 4
Prevalence of individual components, number of simultaneous factors, and diagnosis of the metabolic syndrome in the adult Brazilian population according to ethnicity/skin color, PNS 2013, and PNS Laboratório 2014-2015.

Discussion

In this study, we estimated that one of every three Brazilians has MetS, and this proportion is even higher among women, less educated individuals, and those with more advanced age, even after adjustments for all the sociodemographic variables studied. It is also noteworthy that the most prevalent factor was high WC – significant abdominal obesity and metabolic deterioration marker2222 Shen C, Zhou Z, Lai S, Tao X, Zhao D, Dong W, Li D, Lan X, Gao J. Urban-rural-specific trend in prevalence of general and central obesity, and association with hypertension in Chinese adults, aged 18-65 years. BMC Public Health 2019; 19(1):661.,2323 Barbosa PJB, Lessa I, Almeida Filho N, Magalhães LBNC, Araújo J. Critério de obesidade Central em População Brasileira: impacto sobre a Síndrome metabólica. Arq Bras Cardiol 2006; 87(4):407-414., commonly used in population studies11 Neergaard JS, Laursen JM, Hansen HB, Christiansen C, Beck-nielsen H, Karsdal MA, Brix S, Henriksen K. Metabolic syndrome and subsequent risk of type 2 diabetes and cardiovascular disease in elderly women. Medicine 2016; 95:36(e4806).,1111 Sá NNB, Moura EC. Fatores associados à carga de doenças da síndrome metabólica entre adultos brasileiros. Cad Saude Publica 2010; 26(9):1853-1862.,1212 Bortoletto MSS, Souza RKT de, Cabrera MAS, González AD. Síndrome metabólica, componentes e fatores associados em adultos de 40 anos ou mais de um município da Região Sul do Brasil. Cad Saúde Coletiva 2016; 24(1):32-40., followed by low HDL cholesterol, a significant predictor of cardiovascular risk44 Executive Summary of the Third Report of the National Cholesterol Education Program (NCEP). Expert Panel on Detection, Evaluation, and Treat-ment of High Blood Cholesterol in Adults (Adult Treatment Panel III). JAMA 2001; 285(19):2486-2497..

MetS prevalence in this study was higher than that found in populations in other Latin American countries, such as in Colombia, Venezuela, Peru, and Mexico55 Márquez-Sandoval F, Macedo-Ojeda G, Viramontes-Hörner D, Ballart JDF, Salvadó JS, Vizmanos B. The prevalence of metabolic syndrome in Latin America: A systematic review. Public Health Nutrition 2011; 14(10):1702-1713., and in the Asia-Pacific region2424 Ranasinghe P, Mathangasinghe Y, Jayawardena R, Hills AP, Misra A. Prevalence and trends of metabolic syndrome among adults in the asia-pacific region: A systematic review. BMC Public Health 2017; 17(1):101., and higher than that found in local studies with specific populations at the national level, such as one study with adults in southern Brazil (24.3%)2525 Moreira FP, Jansen K, Cardoso TA, Mondin TC, Magalhães PV, Kapczinski F, Souza LDM, Silva RA, Oses JP, Wiener CD. Metabolic syndrome and psychiatric disorders: A population-based study. Rev Bras Psiquiatr 2019; 41(1):38-43., with the quilombola population (25.8%)2626 Mussi RFF, Petróski EL. Síndrome metabólica e fatores associados em quilombolas baianos, Brasil. Cien Saude Colet 2019; 24(7):2481-2490. and the rural population (14.9%)1313 Pimenta AM, Gazzinelli A, Velásquez-Meléndez G. Prevalência da síndrome metabólica e seus fatores associados em área rural de Minas Gerais (MG, Brasil). Cien Saude Colet 2011; 16(7):3297-3306.. Our findings also show a higher magnitude than previous studies with representative samples of the Brazilian population1010 Ramires EKNM, Menezes RCE, Longo-Silva G, Santos TG, Marinho PM, Silveira JAC. Prevalência e Fatores Associados com a Síndrome Metabólica na População Adulta Brasileira: Pesquisa Nacional de Saúde - 2013. Arq Bras Cardiol 2018; 110(5):455-466.,1111 Sá NNB, Moura EC. Fatores associados à carga de doenças da síndrome metabólica entre adultos brasileiros. Cad Saude Publica 2010; 26(9):1853-1862.. However, our MetS estimate was close to that found by the ELSA study (44%)99 Vieira BA, Luft VC, Schmidt MI, Chambless LE, Chor D, Barreto SM, Duncan BB. Timing and type of alcohol consumption and the metabolic syndrome - ELSA-Brasil. PLoS One 2016; 11(9):1-17. and by the consensus on harmonizing MetS components (35% and 40%)99 Vieira BA, Luft VC, Schmidt MI, Chambless LE, Chor D, Barreto SM, Duncan BB. Timing and type of alcohol consumption and the metabolic syndrome - ELSA-Brasil. PLoS One 2016; 11(9):1-17..

The differences found could be justified by the different methods used to define MetS2727 Monte IP, França SL, Vasconcelos RNO, Vieira JRS. Comparação entre quatro diferentes critérios de diagnóstico de síndrome metabólica em indivíduos do Arquipélago do Marajó (Pará, Brasil). RASBRAN 2019; 10(1):96-102, but mainly by using measured and self-reported data to estimate the underpinning MetS factors. Self-reported data are knowingly subject to underestimating the prevalence of the MetS underlying biochemical factors and, consequently, of MetS itself, which could explain the proximity of our findings to those of the ELSA study, which also used biochemical data to assess the phenotype.

A relevant aspect to be highlighted in this study was the collection of biological material with national representation. We believe it is a significant advance for health assessment at the national level since many metabolic disorders have a prolonged sub-clinical phase, and delayed diagnoses can be inconvenient in preventing more severe events. For example, it is noteworthy that dyslipidemias underpinning MetS are related to a higher risk of cardiovascular diseases (CVD), including stroke2828 Lee JS, Chang PY, Zhang Y, Kizer JR, Best LG, Howard BV. Triglyceride and HDL-C Dyslipidemia and Risks of Coronary Heart Disease and Ischemic Stroke by Glycemic Dysregulation Status: The Strong Heart Study. Diabetes Care 2017; 40(4):529-537.,2929 Wang A, Li H, Yuan J, Zuo Y, Zhang Y, Chen S, Wu S, Wang Y. Visit-to-Visit Variability of Lipids Measurements and the Risk of Stroke and Stroke Types: A Prospective Cohort Study. J Stroke 2020; 22(1):119-129.. Studies with laboratory data allow estimating the prevalence of health problems in subclinical stages and populations with less access to health services, and therefore, still without diagnosis and treatment. For example, recent studies with PNS laboratory data have already shown a high prevalence of chronic renal failure3030 Malta DC, Machado ÍE, Pereira CA, Figueiredo AW, Aguiar LK, Almeida WS, Souza MFM, Rosenfeld LG, Szwarcwald CL. Avaliação da função renal na população adulta brasileira, segundo critérios laboratoriais da Pesquisa nacional de saúde. Rev Bras Epidemiol 2019; 22(Supl. 2):E190010.SUPL.2. and diabetes1515 Malta DC, Duncan BB, Schmidt MI, Machado IE, Silva AG, Bernal RTI, Pereira CA, Damacena GN, Stopa SR, Rosenfeld LG, Szwarcwald CL. Prevalência de diabetes mellitus determinada pela hemoglobina glicada na população adulta brasileira, Pesquisa Nacional de Saúde. Rev Bras Epidemiol 2019; 22(Supl. 2):E190006.SUPL.2., compared to self-reported measures.

The most prevalent MetS components were high WC followed by low HDL cholesterol in both genders, but with higher prevalence among women and any age group. High WC measurements are associated with a higher risk for cardiovascular diseases and reliable predictors of excess visceral fat and, therefore, of general obesity2222 Shen C, Zhou Z, Lai S, Tao X, Zhao D, Dong W, Li D, Lan X, Gao J. Urban-rural-specific trend in prevalence of general and central obesity, and association with hypertension in Chinese adults, aged 18-65 years. BMC Public Health 2019; 19(1):661.. Normal HDL cholesterol levels can promote the efficient transport of excess circulating cholesterol so that its low levels increase cardiovascular risk3131 Forti N, Diament J. Lipoproteínas de alta densidade: aspectos metabólicos, clínicos, epidemiológicos e de intervenção terapêutica. Atualização para os clínicos. Arq Bras Cardiol 2006; 87(5):671-679.. Physical activity is one of the main options to increase plasma HDL3232 Silva RC, Diniz MFHS, Alvim S, Vidigal PG, Fedeli LMG, Barreto SM. Atividade Física e Perfil Lipídico no Estudo Longitudinal de Saúde do Adulto (ELSA-Brasil). Arq Bras Cardiol 2016; 107(1):10-19. levels. In women, the proportion of high WC and low HDL could be explained by the reduced estrogen levels with advancing age, which influences dyslipidemia’s appearance by reducing liver receptors and a more significant abdominal fat deposition with increased cardiovascular risk3333 Mendes KG, Theodoro H, Rodrigues AD, Olinto MTA. Prevalence of metabolic syndrome and its components in the menopausal transition: A systematic review. Cad Saude Publica 2012; 28(8):1423-1437.. Another possible explanation for low HDL is that women are less physically active than men3434 Mitáš J, Cerin E, Reis RS, Conway TL, Cain KL, Adams MA, Schofield G, Sarmiento OL, Christiansen LB, Davey R, Salvo D, Orzanco-Garralda R, Macfarlane D, Hino AAF, Bourdeaudhuij ID, Owen N, Van Dyck D, Sallis JF. Do associations of sex, age and education with transport and leisure-time physical activity differ across 17 cities in 12 countries? Int J Behav Nutr Phys Act 2019; 16(1):121..

Our study also found a higher occurrence of MetS in more advanced age groups, an expected result, since aging is an essential factor of metabolic deterioration and the accumulation of risk factors22 Neto JCGL, Xavier MA, Borges JWP, Araújo MFM, Damasceno MMC, Freitas RWJF. Prevalence of Metabolic Syndrome in individuals with Type 2 Diabetes Mellitus. Rev Bras Enferm 2017; 70(2):265-270.,66 Vidigal FC, Bressan J, Babio N, Salas-Salvadó J. Prevalence of metabolic syndrome in Brazilian adults: a systematic review. BMC Public Health 2013; 13:1198.,1010 Ramires EKNM, Menezes RCE, Longo-Silva G, Santos TG, Marinho PM, Silveira JAC. Prevalência e Fatores Associados com a Síndrome Metabólica na População Adulta Brasileira: Pesquisa Nacional de Saúde - 2013. Arq Bras Cardiol 2018; 110(5):455-466.. This study allowed observing a high prevalence of two MetS components, high WC, and low HDL levels in the younger group (18-39 years). This scenario predicts that future generations may reach a high prevalence of MetS earlier. The promotion of a healthier lifestyle such as a diet rich in fruits and vegetables and regular physical activity in young people could reduce MetS prevalence by delaying the accumulation of risk factors3232 Silva RC, Diniz MFHS, Alvim S, Vidigal PG, Fedeli LMG, Barreto SM. Atividade Física e Perfil Lipídico no Estudo Longitudinal de Saúde do Adulto (ELSA-Brasil). Arq Bras Cardiol 2016; 107(1):10-19.,3535 Fagherazzi S, Dias RL, Bortolon F. Impacto do exercício físico isolado e combinado com dieta sobre os níveis séricos de HDL, LDL, colesterol total e triglicerídeos. Rev Bras Med do Esporte 2008; 14(4):381-386.. This finding signals that public policies for the prevention of cardiovascular diseases and diabetes, when there are no established conditions yet, and among women, can achieve better results in coping with cardiovascular diseases and diabetes.

Another relevant aspect of this study was the higher prevalence of MetS among women, corroborating findings from other studies2424 Ranasinghe P, Mathangasinghe Y, Jayawardena R, Hills AP, Misra A. Prevalence and trends of metabolic syndrome among adults in the asia-pacific region: A systematic review. BMC Public Health 2017; 17(1):101.,2525 Moreira FP, Jansen K, Cardoso TA, Mondin TC, Magalhães PV, Kapczinski F, Souza LDM, Silva RA, Oses JP, Wiener CD. Metabolic syndrome and psychiatric disorders: A population-based study. Rev Bras Psiquiatr 2019; 41(1):38-43.. Women had a higher prevalence in four of the five components, except for blood pressure, considered a more prevalent condition among men3636 Malta DC, Santos NB, Perillo RD, Szwarcwald CL. Prevalence of high blood pressure measured in the Brazilian population, national health survey, 2013. Sao Paulo Med J 2016; 134(2):163-170. globally. High blood pressure becomes more frequent after menopause, which can be partially attributed to estrogen’s protective hormonal effect during the reproductive phase3636 Malta DC, Santos NB, Perillo RD, Szwarcwald CL. Prevalence of high blood pressure measured in the Brazilian population, national health survey, 2013. Sao Paulo Med J 2016; 134(2):163-170..

Besides the biological changes associated with a higher risk for NCDs, we observed a change in health behaviors among women from the results of recent studies. Incorporating unhealthy lifestyles, such as increased sedentary lifestyle3737 Guthold R, Stevens GA, Riley LM, Bull FC. Worldwide trends in insufficient physical activity from 2001 to 2016: a pooled analysis of 358 population-based surveys with 1·9 million participants. Lancet 2018; 6(10):e1077-86. and unhealthy food consumption3838 Schlindwein MM, Kassouf AL. Influência do custo de oportunidade do tempo da mulher sobre o padrão de consumo alimentar no Brasil. PPE 2007; 37(3):489-520., is increasingly frequent and is associated with a high prevalence of obesity among women3939 Araújo FG. Tendência da prevalência de sobrepeso, obesidade, diabetes e hipertensão em mulheres brasileiras em idade reprodutiva, Vigitel 2008-2015 [dissertação]. Belo Horizonte: Universidade Federal de Minas Gerais; 2018.. Also, female social roles, which accumulate domestic responsibilities, and increased working hours, can have a strong influence on the risk of becoming ill4040 Ortiz YM, Gustafsson PE, Chasco MSS, Céspedes AXA, López JML, Velarde DEI, Méndez PAM. Underpinnings of entangled ethnical and gender inequalities in obesity in Cochabamba-Bolivia: an intersectional approach. Int J Equity Health; 18(1):153., especially regarding NCDs, which may be related to the fact that women exceed the already high occurrence of MetS among men4141 Barros MBA, Francisco PMSB, Zanchetta LM, César CLG. Tendências das desigualdades sociais e demográficas na prevalência de doenças crônicas no Brasil, PNAD: 2003-2008. Cien Saude Colet 2011; 16(9):3755-3768..

This study evidenced differences in the prevalence of MetS concerning schooling, and individuals with low education had worse metabolic conditions, which could reinforce the explanation that vulnerable people have lower access to quality information and conditions to maintain healthier lifestyle habits such as a diet rich in fruits and vegetables, restricted number of ultra-processed foods, and adequate exercise4242 Kim I, Song YM, Ko H, Sung J, Lee K, Shin J, Shin S. Educational Disparities in Risk for Metabolic Syndrome. Metab Syndr Relat Disord 2018; 16(8):416-424.. The most socially vulnerable people have more frequently shown chronic conditions4343 Bernal RTI, Felisbino-Mendes MS, Carvalho QH, Pell J, Dundas R, Leyland A, Barreto ML, Malta DC. Indicators of chronic noncommunicable diseases in women of reproductive age that are beneficiaries and non-beneficiaries of bolsa família. Rev Bras Epidemiol 2019; 22(Supl. 2):E190012.SUPL.2., such as diabetes and hypertension, and their risk factors4444 Medina LPB, Barros MBA, Sousa NFS, Bastos TF, Lima MG, Szwarcwald CL. Social inequalities in the food consumption profile of the Brazilian population: National health survey, 2013. Rev Bras Epidemiol 2019; 22(Supl. 2):E190011.SUPL.2, especially in women4343 Bernal RTI, Felisbino-Mendes MS, Carvalho QH, Pell J, Dundas R, Leyland A, Barreto ML, Malta DC. Indicators of chronic noncommunicable diseases in women of reproductive age that are beneficiaries and non-beneficiaries of bolsa família. Rev Bras Epidemiol 2019; 22(Supl. 2):E190012.SUPL.2., and the MetS components included in this study and the metabolic syndrome itself4242 Kim I, Song YM, Ko H, Sung J, Lee K, Shin J, Shin S. Educational Disparities in Risk for Metabolic Syndrome. Metab Syndr Relat Disord 2018; 16(8):416-424.,4545 Blanquet M, Legrand A, Pélissier A, Mourgues C. Socio-economics status and metabolic syndrome: A meta-analysis. Diabetes and Metabolic Syndrome: Clinical Research and Reviews 2019; 13(3):1805-1812., corroborating our findings.

Also, the socially vulnerable environment is an essential determinant of these habits and conditions4646 Pessoa MC, Mendes LL, Caiaffa WT, Malta DC, Velásquez-Meléndez G. Availability of food stores and consumption of fruit, legumes and vegetables in a Brazilian urban area. Nutr Hosp 2014; 31(3):1438-1443.. These findings reinforce the importance of considering these inequalities when promoting health care through public policies since unhealthy behaviors mainly influence the lipid profile and blood glucose of individuals4747 Ferraz IAR, Pereira IG, Monteiro ML, Silva ML, Ladeia AM, Guimaraes A. Comparison of the energy and metabolic nutritional profile of women with central obesity of socioeconomic classes a/b vs c/d/e. Nutr Hosp 2019; 36(4):819-825..

Our findings may contribute to the consolidation of public policies to address NCDs and their risk factors in providing public health services, which implies meeting social vulnerability and strengthening the SUS and its dearest principles. It also shows the importance of PNS in the monitoring and surveillance of NCDs and their risk factors.

Limitations

A potential limitation of this study refers to using cutoff points for high WC that may not be suitable for Latin American4848 Cardinal TR, Vigo A, Duncan BB, Matos SMA, Fonseca MJM, Barreto SM, Schmidt MI. Optimal cut-off points for waist circumference in the definition of metabolic syndrome in Brazilian adults: Baseline analyses of the Longitudinal Study of Adult Health (ELSA-Brasil). Diabetol Metab Syndr 2018; 10:49. populations, even with its recommendation for international comparability33 Alberti K, Eckel R, Grundy S, Zimmet P, Cleeman J, Donato K, Fruchart JC, James WPT, Loria CM, Smith Junior SC, International Diabetes Federation Task Force on Epidemiology and Prevention; Hational Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; International Association for the Study of Obesity. Harmonizing the metabolic syndrome: A joint interim statement of the international diabetes federation task force on epidemiology and prevention; National heart, lung, and blood institute; American heart association; World heart federation; International. Circulation 2009; 120(16):1640-1645.. In a sensitivity analysis, when comparing the prevalence of high WC and MetS using the cutoff points proposed by NCEP44 Executive Summary of the Third Report of the National Cholesterol Education Program (NCEP). Expert Panel on Detection, Evaluation, and Treat-ment of High Blood Cholesterol in Adults (Adult Treatment Panel III). JAMA 2001; 285(19):2486-2497. with the cutoff points of the consensus used in this study, we observed, with the use of consensus, an increase of 21.8 % in the prevalence of abdominal obesity among women and 33.4% among men, with a total increase of 27.3%, leading to an increase of about 5% in the final prevalence of MetS. In other words, the use of consensus significantly increases the prevalence of high WC but does not impact the prevalence of MetS as much.

In this study, two MetS components were employed to replace the absence of glucose and triglyceride levels, namely, glycated hemoglobin and cholesterol, respectively. Regarding the option for total cholesterol, a sensitivity analysis, measuring MetS without this factor, showed a prevalence slightly lower than that found, of 32.4% (95% CI 31.2-33.7), and another using LDL cholesterol as a substitute for triglycerides showed a MetS prevalence of 38.0% (95% CI 36.7-39.4), very similar to that found. Thus, there were no significant differences in having used either cholesterol. Moreover, studies show that changing lifestyle habits would improve the three fractions (total cholesterol, LDL cholesterol, and triglycerides)3535 Fagherazzi S, Dias RL, Bortolon F. Impacto do exercício físico isolado e combinado com dieta sobre os níveis séricos de HDL, LDL, colesterol total e triglicerídeos. Rev Bras Med do Esporte 2008; 14(4):381-386.. On the other hand, glycated hemoglobin has the advantage of estimating the mean blood glucose concentration in the last 60 to 90 days, unlike fasting glucose or the glucose tolerance test, which are measured at specific times1515 Malta DC, Duncan BB, Schmidt MI, Machado IE, Silva AG, Bernal RTI, Pereira CA, Damacena GN, Stopa SR, Rosenfeld LG, Szwarcwald CL. Prevalência de diabetes mellitus determinada pela hemoglobina glicada na população adulta brasileira, Pesquisa Nacional de Saúde. Rev Bras Epidemiol 2019; 22(Supl. 2):E190006.SUPL.2.,4949 World Health Organization (WHO). Use of Glycated Haemoglobin (HbA1c) in the Diagnosis of Diabetes Mellitus: Abbreviated Report of a WHO Consultation. Geneva: WHO; 2011.. The advantage is the simplicity of the collection and the accuracy of the diagnosis. Both the World Health Organization and the American Diabetes Association (ADA) use this measure to diagnose and monitor MetS1515 Malta DC, Duncan BB, Schmidt MI, Machado IE, Silva AG, Bernal RTI, Pereira CA, Damacena GN, Stopa SR, Rosenfeld LG, Szwarcwald CL. Prevalência de diabetes mellitus determinada pela hemoglobina glicada na população adulta brasileira, Pesquisa Nacional de Saúde. Rev Bras Epidemiol 2019; 22(Supl. 2):E190006.SUPL.2.,4949 World Health Organization (WHO). Use of Glycated Haemoglobin (HbA1c) in the Diagnosis of Diabetes Mellitus: Abbreviated Report of a WHO Consultation. Geneva: WHO; 2011.. Also, the non-fasting collection option prevents losses and facilitates collection on any day and time1717 Szwarcwald CL, Malta DC, Souza Júnior PRB, Almeida WS, Damacena GN, Pereira CA, Rosenfeld LG. Exames laboratoriais da Pesquisa Nacional de Saúde: metodologia de amostragem, coleta e análise dos dados. Rev Bras Epidemiol 2019; 22(Supl. 2): E190004.SUPL.2.,1919 Instituto Brasileiro de Geografia e Estatística (IBGE). Pesquisa Nacional de Saúde 2013: Manual de Antropometria. Rio de Janeiro: IBGE; 2013..

Conclusion

In this study, MetS was a very prevalent condition in the Brazilian population, and high WC and low HDL cholesterol were the most prevalent component factors, with the aggravation of high property in young adults. Women, individuals with low schooling, and older individuals had an even higher prevalence of MetS. These findings reveal the need to consider laboratory data to obtain more reliable results from this condition, which can be a challenge at the national level. Consolidating and strengthening public policies that promote healthy lifestyles and combat risk factors is essential to address this challenge. It is also noteworthy that this is the first national study using laboratory data representative of the Brazilian population to estimate the prevalence of MetS as a basis for supporting prevention and health promotion programs.

Acknowledgments

BNSS is grateful to PIBIC/CNPq/UFMG for the scientific initiation scholarship. GVM is grateful to the Fundação de Amparo à Pesquisa de Minas Gerais (FAPEMIG) for its support.

Ministério da Saúde (Laboratório da Pesquisa Nacional de Saúde).

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Publication Dates

  • Publication in this collection
    06 Nov 2020
  • Date of issue
    Nov 2020

History

  • Received
    15 Aug 2020
  • Accepted
    17 Aug 2020
  • Published
    19 Aug 2020
ABRASCO - Associação Brasileira de Saúde Coletiva Rio de Janeiro - RJ - Brazil
E-mail: revscol@fiocruz.br