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. 2021 Sep 17;16(9):e0257347. doi: 10.1371/journal.pone.0257347

COVID-19 in Brazilian cities: Impact of social determinants, coverage and quality of primary health care

Marcello Barbosa Otoni Gonçalves Guedes 1, Sanderson José Costa de Assis 2, Geronimo José Bouzas Sanchis 2, Diego Neves Araujo 3, Angelo Giuseppe Roncalli Da Costa Oliveira 2, Johnnatas Mikael Lopes 4,*
Editor: Bruno Pereira Nunes5
PMCID: PMC8448317  PMID: 34534235

Abstract

Background

Brazil, as many other countries, have been heavily affected by COVID-19. This study aimed to analyze the impact of Primary health care and the family health strategy (FHS) coverage, the scores of the National Program for Improving Primary Care Access and Quality (PMAQ), and socioeconomic and social indicators in the number of COVID-19 cases in Brazilian largest cities.

Methods

This is an ecological study, carried out through the analysis of secondary data on the population of all Brazilian main cities, based on the analysis of a 26-week epidemiological epidemic week series by COVID-19. Statistical analysis was performed using Generalized Linear Models with an Autoregressive work correlation matrix.

Results

It was shown that greater PHC coverage and greater FHS coverage together with an above average PMAQ score are associated with slower dissemination and lower burden of COVID-19.

Conclusion

It is evident that cities with less social inequality and restrictions of social protection combined with social development have a milder pandemic scenario. It is necessary to act quickly on these conditions for COVID-19 dissemination by timely actions with high capillarity. Expanding access to PHC and social support strategies for the vulnerable are essential.

Introduction

The world has been suffering from the persistent evolution of SARS-COV-2 contagion that leads to the manifestation of the new coronavirus disease (COVID-19), with unprecedented consequences for public health [1]. Since January 2020, WHO has given visibility to this globalized public health problem with the Declaration on Public Health Emergency of International Concern [2]. Although Brazil has had extra time to prepare, the pandemic has hit the country and has been plaguing its population with several cases and deaths in a continuous and aggressive manner [3]. COVID-19 infection presents itself, with a significant frequency of its cases, with complicated symptoms and may lead to death [4].

Brazil is part of a large group of countries in the developing world, with a considerable portion of its population in a situation of social vulnerability [5]. The Brazilian health system (Sistema Único de Saúde—SUS), is based on the principles of universal care, comprehensive care and equity of actions based on the precept of social justice. The resources for coping with COVID-19 are structured based on these pillars [6].

SUS is essentially built by primary health care (PHC), as the first level of community care, regulating and organizing other levels and services, capable of serving most people, based on the Family Health Strategy (FHS) [7]. However, a considerable percentage of the Brazilian territory does not have PHC coverage or has a deficient quality of these services [8]. In addition, an important layer of this population is under unfavorable socioeconomic conditions, with low access to social protection policies, demonstrating a high degree of inequity in the country [5].

The quality of the services offered by PHC may directly influence the resolution of COVID-19 cases. In Brazil, there is the National Program for Improving Primary Care Access and Quality (PMAQ), which measures the level of PHC quality and promotes the quality of its services with additional resources. This program serves as an indicator for PHC to the Ministry of Health and it is based on the idea that the conditions of these services are the gateway for its users, with accountability for care, the ability to provide comprehensive care and to organize the network of health services with multidisciplinary work, promoting the highest possible degree of resolution [9].

In the Brazilian COVID-19 epidemic scenario, PHC is responsible for welcoming measures, clinical screening, social support, monitoring and care in home isolation until the discharge of social restriction, as well as clinical stabilization, effective referral and transportation to referral centers or hospital services for the most serious cases [6]. A well-qualified and engaged FHS team, for example, could provide evident support to all other health services, easing the burden on more complex levels of care [10].

In this context, in which a large part of the Brazilian population is under an unfavorable socioeconomic situation and still depends exclusively on a public system that is unable to serve the entire population with quality, the epidemiological analysis of health and social protection indicators [11], as well as the coverage and quality of PHC, become essential for the assertive coping with this epidemic [12]. The implementation of effective public policies throughout the national territory, with well-defined strategies, may improve the distribution and use of the scarce available resources.

Considering all issues presented here, the effects of this epidemic can be shown to be even more devastating in countries with great social inequities and which also make wrong choices of public policies and management strategies to combat COVID-19. Therefore, the objectives of this study were to identify the socioeconomic and health system factors associated with the accumulation of cases of COVID-19 diagnosed in the capitals of the twenty-seven Brazilian federative units (FU), characterizing them in terms of disease burden and evolutionary pattern, providing information for planning public policies for Brazil and countries with a similar profile.

Method

This is an ecological time series study, with quantitative approach, carried out through the analysis of population-based secondary data. The outcome was COVID-19 cases confirmed by laboratory test, clinical, clinical-epidemiological and clinical-image per 100,000 inhabitants, in all Brazilian FU captaincies until the 26th epidemiological week. Outcome data were extracted from Painel Covid-19 (https://covid.saude.gov.br/) database, fed by the Health Surveillance Department and made available by the the SUS Informatics Department in [1]. To date, only criteria for confirmation of cases (laboratory and clinical-epidemiological) were used as a form of diagnosis of Covid-19, using immunological tests, rapid test or classical serology for the detection of antibodies.

Brazil is a federation with 26 states and a federal district. Each of the FU has an administrative capital that is characterized as the city with the greatest economic power in the FU. The capitals present different variability in socio-economic and demographic indicators, which helps us to understand their influences on the dispersion of COVID-19 in the population (Table 1) and described below.

Table 1. Description of the socioeconomic characteristics of the capitals of Brazilian federative units in 2020.

Capitals GDP DD Gini HDI RSP %PHC %FHS N° COVID-19 COVID-19 Incidence
Aracaju 25185,55 3140,65 0,57 0,770 3,40 75,54 70,36 31777 1746,69
Belém 21.191,47 1315,26 0,61 0,746 4,70 40,79 22,65 29115 1177,76
Belo Horizonte 36.759,66 7167,00 0,55 0,810 1,40 100,00 80,62 28462 176,27
Boa Vista 26.752,67 49,99 0,56 0,752 6,50 76,84 50,99 29570 1501,45
Campo Grande 32.942,46 97,22 0,51 0,784 1,60 70,15 56,99 15953 135,27
Cuiabá 39.043,32 157,66 0,53 0,785 2,80 56,29 44,49 15345 429,19
Curitiba 45.458,29 4027,04 0,53 0,823 1,30 54,26 32,84 24170 137,91
Florianópolis 42.719,16 623,68 0,48 0,847 ,10 100,00 88,84 4999 223,96
Fortaleza 23436,66 7786,44 0,57 0,754 3,20 61,36 49,89 44971 1238,96
Goiânia 33.004,01 1776,74 0,48 0,799 1,60 54,78 43,24 25853 338,37
João Pessoa 24319,82 3421,28 0,59 0,763 2,30 96,34 86,57 24597 1307,89
Macapá 22.181,72 512.902 0,45 0,733 9,00 82,17 53,46 16229 2368,24
Maceió 22.126,34 1854,10 0,54 0,721 6,00 44,60 26,95 24909 1273,67
Manaus 36.445,75 158,06 0,52 0,737 6,80 56,60 40,78 39563 1152,35
Natal 26497,08 4805,24 0,53 0,763 4,50 54,93 37,42 22041 863,91
Palmas 32.293,89 102,90 0,56 0,788 4,50 100,00 95,73 9173 441,28
Porto Alegre 52.149,66 2837,53 0,55 0,805 1,30 76,56 55,58 10753 114,17
Porto Velho 32.042,66 12,57 0,51 0,736 5,10 60,75 49,51 25006 1871,04
Recife 31743,72 7039,64 0,61 0,772 4,30 64,87 56,39 29718 1195,95
Rio Branco 22.287,70 38,03 0,52 0,727 4,40 75,63 49,97 9662 1485,81
Rio de Janeiro 54.426,08 5.265,82 0,48 0,799 2,60 47,29 40,96 80899 757,89
Salvador 21231,48 3859,44 0,55 0,759 3,40 47,53 36,39 68099 823,82
São Luís 27226,41 1215,69 0,53 0,768 7,00 45,43 37,26 17658 1140,50
São Paulo 58.691,90 7398,26 0,58 0,805 2,10 66,53 40,84 236163 879,29
Teresina 22481,67 584,94 0,51 0,751 3,50 100,00 100,00 21803 677,12
Vitória 73.632,55 3338,30 0,57 0,845 1,20 100,00 78,94 12897 1657,84
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GDP: per capto gross domestic product; DD: demographic density; Gini: Gini coefficient; HDI: Human Development Index; RSP: restriction on social protection; RE: restriction on education; RH: restriction on housing; RS: restriction on sanitation; %PHC: proportion of the population covered by primary health care; %FHS: proportion of the population covered by Family Health Strategy.

In this study, time in epidemiological weeks, indicators of coverage and quality of PHC and FHS, demographic and socio-economic indicators were admitted as independent variables. PHC and FHS coverage were collected in DATASUS (https://sisaps.saude.gov.br/painelsaps/). These variables correspond to the percentage of the population covered by primary care; in this study, they were categorized as less than 50%, from 50 to 74% and 75% or higher, as recommended by the World Health Organization [5, 13].

PMAQ is a program with the objective of stimulating the evaluation process in PH C in Brazil, developed by the federal government and carried out by federal educational institutions in the country [7]. The PMAQ consists of an assessment of the conditions of infrastructure, materials, supplies and medicines in primary care services, as well as the team work process, user satisfaction and care organization, which reveal the patterns of access and quality of care. The program is divided into cycles and, in this study, data were extracted from the third cycle of the PMAQ in 2019, which cover information regarding family health teams. Teams are classified as unsatisfactory, poor, regular, good, very good, excellent [9]. However, in this study a recategorization was performed in 3 categories: low quality—with categories unsatisfactory and poor put together; medium quality—regular and good put together; and high quality—with very good and excellent teams. For access to data and more details on the calculation of this composite indicator, see: http://aps.saude.gov.br/ape/pmaq/ciclo3/.

Demographic density (DD) was collected to control bias related to the probability of human contacts in the public environment. Socioeconomic conditions were measured using per capto gross domestic product (GDP), the Human Development Index (HDI) and Gini coefficient. HDI was extracted from UNDP and Gini from PNAD 2018. HDI is an important tool to assess the development of certain locations and it is measured by the geometric mean of the sum of life expectancy at birth, education index and income index. The Gini coefficient was used as an instrument to measure the degree of income concentration in the cities, as a measure of social inequality, ranging from 0 to 1, and the closer to 1, the greater the inequality in that location. The calculation of this coefficient is given by the ratio of the areas of the Lorenz curve diagram to the accumulated income of the population. These data were collected in the National Household Sample Survey [5].

In addition to these social indicators, data was also collected on the restriction on social protection (RSP). The indicator estimate the proportion of people in situations of vulnerability. It was considered as a restriction: people who simultaneously meet the following two conditions: residents in households where there was no resident aged 14 or older who contributed to the social security institute or retired/pensioner; households with real effective household income per capita of less than ½ minimum wage, and with no members receiving income from other sources, which includes social programs. Minimum wage used as reference: R$ 954.00 per month, in this study, ratio was calculated and stratified less than 2.60% or higher than 2.60% [5] These data were linked to the database of the Brazilian Institute of Geography and Statistics (IBGE), whose data were compiled by the Brazilian agency of the United Nations Development Program (UNDP) [5].

Statistical analysis was performed using Generalized Linear Models with an autoregressive work correlation matrix, in which the log ligand function with Gamma distribution was used. Association tests, such as Wald’s chi-square test, were performed between the outcome variable and the independent variables, selecting those with “p” values equal to or less than 0.20 to be included in the adjusted model. A significance level of 5% (α <0.05) was adopted. The interaction variable between FHS coverage and PMAQ score was included in the analysis. In the adjusted model, the analysis was stratified by the PHC coverage strata. Data were processed using the statistical program SPSS®, version 22.0

Results

A total of 857,741 cases were recorded in the Brazilian cities in the analyzed period, with an average of 15,884.09 (±21,604.43), revealing a heterogeneity in the dissemination of cases (Fig 1).

Fig 1. Distribution of the incidence of COVID-19 cases in Brazilian cities up to the 26th epidemiological week.

Fig 1

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Circles are the observed cases and line is the general trend of progression of the cases.

When observing the social and health system characteristics of the Brazilian cities, it is identified that the cities in strata of the FHS coverage, HDI and Gini presented discrepancies regarding the incidence of diagnosed cases of COVID-19, being homogeneous in the strata of PHC coverage. Cities with FHS coverage above 75% showed a lower incidence rate as well as those with HDI above 0.800 and Gini less than 0.50 (Fig 2).

Fig 2. Evolution of the incidence of COVID-19 cases per 100 thousand inhabitants in Brazilian cities until the 26th epidemiological week.

Fig 2

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A-Stratified incidence by the coverage of Primary Health Care (PHC); B-Incidence stratified by the coverage of FHS; C-Stratified incidence by the HDI; D-Stratified incidence by the Gini Index.

When segmenting the PMAQ assessment strata according to PHC coverage, it is observed that in situations that PHC coverage is less than 50%, there are no services with a score higher than 2.99 and a similar distribution of the incidence of COVID-19. In cities with PHC coverage between 50–74%, there is a gradient of COVID-19 cases, where those with an average PMAQ score above 3 points show less load and slope. Similarly, it occurs in cities with PHC coverage above 75%, which do not have PMAQ scores below 2 points (Fig 3).

Fig 3.

Fig 3

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Evolution of the incidence of COVID-19 cases per 100 thousand inhabitants in Brazilian cities until the 26th epidemiological week stratified by PMAQ score when the PHC coverage is less than 50% (A), 50–70% PHC coverage (B) and&gt;70% PHC coverage (C).

In order to estimate the effect of the independent variables and to control the effect of their interactions, an adjusted model presented in Table 2 was created, stratified by PHC coverage. In situations of PHC coverage below 50%, PMAQ score low demonstrated nine times more cases per 100,000 inhabitants COVID-19 cases than those with a score medium or high (B = 9.08; p<0.001). Positive associations were also found for RSP (B = 2.45; p<0.001), Gini (B = 7.54; p<0.001) and HDI (B = 16.19; p<0.001) with the outcome incidence rate. For the interpretation of Gini and HDI, it is more appropriate to observe the interaction of these factors and not the main effect. The Gini-HDI interaction shows a negative relationship (B = -72.46; p<0.001), which may suggest a mitigating effect in cities with high HDI and low Gini.

Table 2. Adjusted model for association with the incidence of Covid-19 in the largest cities of all federal units in Brazil stratified by the coverage of primary health care.

Independent Variables Badj Standard Error CI 95% Wald Hypothesis test
Lower Upper x2 Wald df p
PHC <50% Model
Interception 17.38 0.197 16.99 17.77 7786.51 1 <0.001
RSP 2.45 0.021 2.41 2.49 13543.65 1 <0.001
Gini 7.54 0.02 7.49 7.50 70924.88 1 <0.001
HDI 16.19 0.11 15.96 16.42 18704.31 1 <0.001
Gini-HDI -72.46 0.713 -73.85 -71.06 10304.16 1 <0.001
Epidemiológical Week 0.05 0.002 0.04 0.05 361.80 1 <0.001
Stratum FHS-PMAQ
 Cov. FHS <50%- PMAQ<low 9.08 0.082 8.92 9.24 12067.74 1 <0.001
 Cov. FHS <50%- PMAQ<medium 0
Scale 0.62
PHC 50–74% Model
Interception 7.06 1.77 3.58 10.55 15.81 1 <0.001
RSP 0.33 0.05 0.23 0.44 39.88 1 <0.001
Gini -8.47 3.36 -15.07 -1.88 6.34 1 0.01
HDI -15.49 6.77 -28.76 -2.22 5.23 1 0.02
Gini-HDI -13.89 4.38 -22.47 -5.30 10.05 1 0.002
Epidemiológical Week 0.07 0.004 0.06 0.08 306.83 1 <0.001
Stratum FHS-PMAQ
 Cov. FHS <50%*PMAQlow 2.36 0.17 2.01 2.71 177.60 1 <0.001
 Cov. FHS <50%*PMAQmedium 0.85 0.11 0.62 1.08 52.29 1 <0.001
 Cov. FHS <50%*PMAQhigh 2.87 0.31 2.25 3.49 81.63 1 <0.001
 Cov. FHS50-75%*PMAQlow 2.63 0.36 1.92 3.35 52.43 1 <0.001
 Cov. FHS50-75% *PMAQhigh 0
Scale 0.56
PHC> 75% Model
Interception -3.15 1.98 -7.05 0.74 2.51 1 0.11
RSP 0.26 0.07 0.12 0.41 12.63 1 <0.001
Gini 17.06 5.44 6.40 27.73 9.83 1 0.002
HDI -2.41 4.89 -12.00 7.18 0.24 1 0.62
Gini * HDI 15.20 4.76 5.86 24.53 10.17 1 0.001
Week 0.06 0.003 0.06 0.07 442.16 1 <0.001
Stratum FHS-PMAQ
 Cov. FHS <50% * PMAQmedium 0.76 0.35 0.07 1.45 4.71 1 0.03
 Cov. FHS50-75% * PMAQmedium -0.22 0.53 -1.26 0.81 0.17 1 0.67
 Cov. FHS>75% * PMAQmedium -0.22 0.51 -1.24 0.79 0.19 1 0.66
 Cov. FHS>75% * PMAQhigh 0
Scale 0.83
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B–Regression Coefficient; CI–Confidence Interval; x2 –Chi-square; df–degrees of freedom; p–probability; PHC–Primary Health Care; RSP–Restriction to Social Protection; HDI–Human Development Index; Cov. FHS–Health Strategy Family Coverage; PMAQ–National Program for Improving Primary Care Access and Quality.

In the PHC 50–74% stratum, cities with intermediate FHS coverage and PMAQ scores high showed almost twice less (B = 2,36) COVID-19 incidence rates than cities with lower ratings. It is still possible to verify a positive association of RSP (B = 0.33; p <0.001) with the outcome. In this PHC context, the Gini-HDI interaction shows a negative association with the outcome (B = -13.89; p<0.001), similar to cities with PHC coverage below 50% (Table 2), In other words, with each increase in the Gini-HDI interaction unit, there is a decline of more than 13 covid-19 cases per 100,000 inhabitants in the average growth rate (B = -13,89).

In cities with PHC above 75%, it was estimated that only cities with FHS coverage below 50% and PMAQ score medium have sligthly higher incidence of COVID-19 than those with higher strata of FHS and PMAQ scores (B = 0,76). Positive associations were also found for RSP (B = 0.26; p<0.001), Gini (B = 17.06; p<0.001) and Gini-HDI interaction (B = 15.20; p<0.001). However, the HDI establishes a negative relationship with the outcome (B = -2.41) (Table 2).

In both scenarios of primary health care coverage, social indicators in the adjusted model, with emphasis on the Gini and the HDI, which present the highest coefficients in the model. On the other hand, the pure weekly evolution, without the effects of other factors, has a low influence on the evolution of cases (B<0.10). This reflects the effect of contextual factors on the spread of covid-19 in the sample.

Discussion

This study sought to analyze the impact of PHC and FHS coverage, PMAQ scores obtained by health units, socioeconomic indicators, and social restrictions on the incidence of COVID-19 in Brazilian largest cities. We highlight that strata of better FHS coverage and PMAQ scores obtained correlation with slower progression and lower load of COVID-19, controlling the effects of socioeconomic indicators. This pandemic is also influenced by social indicators, revealing that inequality and social restrictions modulate the dispersion of cases. These factors must be considered by health managers to develop better strategies to combat the pandemic and to improve management of health resources.

Our findings pointed out that, by stratifying FHS coverage, cities with the highest coverage had their population less affected by COVID-19 cases, especially those that were better evaluated in PMAQ. These data reinforce the hypothesis that the prevention actions developed in areas better assisted by PHC services is a strategy of extreme relevance to minimize the impact of this pandemic, thus being able to assist the other levels and services of health care [14].

Adequate coverage leads to greater access to essential services, being an essential factor for a favorable scenario of health conditions within a community, either due to its high level of capillarity, or by encouraging actions of promotion and prevention for the individuals in this context [15]. These factors may directly impact prevalence and incidence of cases both in chronic non-communicable diseases and in communicable diseases, as it is the case with COVID-19 [16]. It is noteworthy that, although SUS is based on universality, not all Brazilian territory is served by PHC services [8].

In Brazil, the predominant PHC strategy is based on the community and centered on the family and the individual. Although other modalities of service organization in PHC are possible, 75% of public managers choose FHS as a structural model of their services in the primary care network [8, 17]. Thus, FHS presents itself as an important organizational model within PHC, becoming effective as a source of access to health promotion and prevention actions, as well as for the use of different health services, which can directly influence behavioral positive adjustments for the assisted population, as well as in the rationalization of health costs [17, 18].

PMAQ evaluation generates a score for each health team that is part of PHC and has joined the program [9]. In addition to the aspects related to coverage and organization of services, team quality indicators have important consequences on the population’s health results. PMAQ stimulates the culture of evaluation within PHC services, in order to encourage good practices within the health units, providing the quality and innovation in its management and provision of its services with resources [10]. Our results indicated that strata with higher PMAQ scores in all PHC and FHS coverage scenarios had lower incidence of COVID-19 in Brazilian cities in the evaluated period.

PMAQ scores related findings indicate that adequate quality of PHC services can also positively impact the habits and behaviors of the registered population, which may, in general, attenuate the dissemination of the new coronavirus in Brazilian cities. Higher PMAQ scores may imply reinforcement of actions with strategic characteristics in the FHS, for example, and in adverse situations such as this current pandemic, they become even more important. Comprehensive PHC quality assessment programs prove to be important promotion tools to increase the resolution capacity of these services [19].

Stratified and nested analyses were also carried out and some considerations are as follows. As PHC coverage strata rise, the difference in the incidence of COVID-19 between FHS-PMAQ nests becomes smaller. This organization is very favorable to support the control of this pandemic, as it is a situation of good supply of PHC services, facilitating user access to care and quality health education actions [20, 21].

PHC qualities can make a difference in coping with this pandemic. Knowledge of the territory, access, the bond between the user and the health team, comprehensive care, monitoring vulnerable families and monitoring suspicious and mild cases are fundamental strategies for containing the pandemic [6, 22]. As an example, primary care services is able to mitigate problems related to the precariousness of social and economic life, domestic violence, alcoholism and mental health problems, which also come from prolonged social isolation [22]. These roles developed by the FHS and other PHC services may stimulate popular health education and a culture of healthy habits and preventive actions to combat COVID-19.

Regarding socioeconomic indicators, cities with greater social inequality or less development had a higher number of diagnosed COVID-19 cases. It is known that high social inequality is accompanied by worse socio-demographic and health conditions for the most vulnerable social classes [23]. Often, populations under considerable social vulnerability do not have several resources or appropriate living conditions, such as access to piped water in their homes, an adequate number of people per household and economic stability. This scenario makes it difficult to carry out the prevention strategies for COVID-19, due to the population’s lack of information, or even due to the lack of conditions needed for these actions to happen or to be effectively applied [24].

Another relevant issue for the analysis related to social inequities is that the prevalence of chronic diseases such as diabetes, hypertension and obesity, as well as the difficulty of its management, is higher in the poorest populations of the Brazilian society [25], and these cardiovascular conditions are one of the main risk factors for worse outcomes and mortality due to COVID-19. Even though our study did not control cardiovascular variables, a large part of the studied population is at high social risk and, therefore, preventive measures should have a special focus on these groups.

Important evidence from the results is the effect of RSP on the spread of COVID-19 in Brazilian cities. The RSP indicator portrays the absence of the State to protect citizens who are not inserted in the means of production, which increases their vulnerability. Thus, cities with a higher proportion of these individuals had more cases of COVID-19. However, these effects are minimized when PHC coverage is expanded. Based on these inferences, some social protection measures should be developed by the government in the current situation, such as 1) the provision of free and comprehensive tests, prioritizing communities that present a greater risk for the worsening and contagion of the disease, also the collection of sociodemographic data from individuals [26], 2) government officials, community leaders and the local media should consult and collaborate with specialists in medicine and public health to offer public health messages directed at low-income and high-risk populations [26]; 3) government officials must provide a minimum income for informal or unemployed workers to be able to achieve social isolation in an appropriate manner and in a timely manner; 4) alternative options for providing creative, flexible, and accessible health services to populations with difficult access to health services [27, 28]. These measures must be taken by Government officials to reduce health inequities, which makes PHC and its teams essential for the effectiveness of social protection measures, as they are inserted in vulnerable communities, and have knowledge of the territory and the resident population and their risk factors.

Unfortunately, what we observe is a denial of the pandemic, reflecting the lack of interest by the Ministry of Health in proposing guidelines based on available scientific evidence. This reflected in the timely organization of PHC community services, which could be leveraged with appropriate investments as presented above until obtaining effective and effective vaccines for the population [28, 29].

Despite the findings that impact public health in Brazil, it is reasonable to mention some limitations that should be analyzed. The first is that COVID-19 is underdiagnosed in Brazil as well as elsewhere in the world, which leads to underreporting of events. However, this influences the disease burden in general and not on stratifications. A second limitation is the outdated ecological measure of the HDI, however we believe that its modification since the last results and the current date has been minimal. Important additional COVID-19 prevention strategies were not measured in this research and are relevant tools that should be considered in further studies.

Finally, the results of this investigation address the importance of a well-structured PHC with the FHS as a priority structural model in this fight against the coronavirus, especially in areas with considerable social inequity. Preventive actions and formal social support to the population can be decisive factors for a positive outcome in this battle. This pandemic brings unprecedented elements and specific characteristics that affect each region of the world in an unprecedented way, imposing a great challenge for the reorganization of health services across the planet.

Although each Brazilian larger city experiences specific contextual conditions and distinct moments in the development of the epidemic by COVID-19, our results allow us to make relevant generalizable and timeless analyses that will support the decision-making process of public managers. These findings are in line with the important attributions of PHC, especially those that promote a more efficient fight against the epidemic. Other countries with characteristics of social vulnerability and organization of health services similar to Brazil, can make use of these results as an aid for more effective referrals in public policies in this pandemic context.

Data Availability

All 3 covid-19 files are available from the DATASUS database (https://covid.saude.gov.br/).

Funding Statement

The authors received no specific funding for this work.

References

  • 1.He F, Deng Y, Li W. Coronavirus disease 2019: What we know? Journal of Medicine Virology. 2020, 1–7. 10.1002/jmv.25766 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.World Health Organization (WHO). Covid 19. Public Health Emergency of International Concern (PHEIC). Feb 2020.
  • 3.Department of Informatics of the Unified Health System (DATASUS). Ministry of Health, Brazil. Coronavírus Brazil. [accessed 03 Jul 2020]. Available in: https://covid.saude.gov.br/
  • 4.Huang X, Wei F, Hu L, Wen L, Chen K. Epidemiology and Clinical Characteristics of COVID-19. Archive Iran Medicine. 2020; 23(4):268–71. doi: 10.34172/aim.2020.09 [DOI] [PubMed] [Google Scholar]
  • 5.PNUD. Relatório do Desenvolvimento Humano 2019. Além do rendimento, além das médias, além do presente: Desigualdades no desenvolvimento humano no século XXI. Programa das Nações Unidas para o Desenvolvimento, 2019.
  • 6.Ministry of Health, Brazil. Coronavirus clinical management protocol (COVID-19) in Primary Helth Care. 2020. [accessed 28 jun 2020].
  • 7.Ministry of Health, Brazil. Política Nacional de Atenção Básica. Portaria 2.436, 21 setembro, 2017. [accessed 28 jun 2020]. [Google Scholar]
  • 8.Gomes CBS, Guiérrez AC, Soranz D. National Primary Care Policy 2017: analysis of team’s composition and national coverage of Family Health. Ciência & Saúde Coletiva, 2020; 25(4):1327–1337. doi: 10.1590/1413-81232020254.31512019 [DOI] [PubMed] [Google Scholar]
  • 9.Ministry of Health, Brazil. Programa Nacional da Melhoria do Acesso e da Qualidade. Manual Instrutivo para Equipes de Saúde da Família e NASF. 2017. [accessed 28 jun 2020].
  • 10.Pinto et al. The National Program for Access and Quality Improvement in Primary Care: faces of an innovative policy. Saúde Debate. Rio de Janeiro, out, 2014; 38: 358–72. doi: 10.5935/0103-1104.2014S027 [DOI] [Google Scholar]
  • 11.Zhai P, Ding Y, Wu X, Long J, Zhong Y, Li Y. The epidemiology, diagnosis, and treatment of COVID-19. Int J Antimicrob Agents. 2020: 105955. doi: 10.1016/j.ijantimicag.2020.105955 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Pan A, Liu L, Wang C, et al. Association of Public Health Interventions with the Epidemiology of the COVID-19 Outbreak in Wuhan, China. JAMA. 2020; 323(19): 1915–1923. doi: 10.1001/jama.2020.6130 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Pinto LF, Giovanella L. The Family Health Strategy: expanding access and reducing hospitalizations due to ambulatory care sensitive conditions (ACSC). Ciência & Saúde Coletiva. 2018; 23(6):1903–1913. 10.1590/1413-81232018236.05592018 [DOI] [PubMed] [Google Scholar]
  • 14.Jenq GY, Mills JP, Malani PN. Preventing COVID-19 in Assisted Living Facilities—A Balancing Act. JAMA Intern Med. Published online May 21, 2020. doi: 10.1001/jamainternmed.2020.2224 [DOI] [PubMed] [Google Scholar]
  • 15.Lopes JM, Guedes MBOG. Fisioterapia na atenção primária: manual de prática profissional baseado em evidência. 1. ed. Rio de Janeiro: Atheneu, 2019. [Google Scholar]
  • 16.Heymann DL, Shindo N. COVID-19: what is next for public health? The Lancet. Feb22, 2020; 395: 542–45. doi: 10.1016/S0140-6736(20)30374-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Neves RG et al. Time trend of Family Health Strategy coverage in Brazil, its Regions and Federative Units, 2006–2016. Epidemiologia e Serviços de Saúde [online]. 2018, 27(3). 10.5123/S1679-49742018000300008. [DOI] [PubMed] [Google Scholar]
  • 18.Bastos ML et al. The impact of the Brazilian family health on selected primary care sensitive conditions: a systematic review. Plos One. 2017; 12(12): e0189557. 10.1371/journal.pone.0182336 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Barbazza E et al. Creating performance intelligence for primary health care strengthening in Europe. BMC Health Services Research. 2019; (19), 1006. 10.1186/s12913-019-4853-z [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Facchini LA, TomasI E, Dilélio AS. Quality of Primary Health Care in Brazil: advances, challenges, and perspectives. Saúde Debate. Rio de Janeiro, 2018; 4,(1): 208–22. doi: 10.1590/0103-11042018S114 [DOI] [Google Scholar]
  • 21.Moreira KS, Vieira MA, Costa SM. Quality of Primary Care: assessment of the Family Health Teams. Saúde Debate Rio de Janeiro, 2016; 40(111):117–27. doi: 10.1590/0103-1104201611109 [DOI] [Google Scholar]
  • 22.Sarti TD et al. What is the role of Primary Health Care in COVID-19 pandemic? Epidemiol. Serv. Saude, Brasília, 2020; 29(2):e2020166. 10.5123/s1679-49742020000200024 [DOI] [PubMed] [Google Scholar]
  • 23.Oliveira BLCA, LUIZ RR. Racial density and the socioeconomic, demographic and health context in Brazilian cities in 2000 and 2010. Revista Brasileira de Epidemiologia, 2019; 22: 1–12. 10.1590/1980-549720190036 [DOI] [PubMed] [Google Scholar]
  • 24.Pirtle LWN. Racial Capitalism: A Fundamental Cause of Novel Coronavirus (COVID-19) Pandemic Inequities in the United States. Health Education and Behavior, 2020. doi: 10.1177/1090198120922942 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Ribeiro ALP. et al. Cardiovascular Health in Brazil. Circulation, 2016; 133 (4): 422–33, 26. doi: 10.1161/CIRCULATIONAHA.114.008727 [DOI] [PubMed] [Google Scholar]
  • 26.Wang, et al. Addressing inequities in COVID-19 morbidity and mortality: research and policy recommendations. TBM. 2020. doi: 10.1093/tbm/ibaa055 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.de Peralta AM, Gillispie M, Mobley C, Gibson LM. It’s all about trust and respect: cultural competence and cultural humility in mobile health clinic services for underserved minority populations. J Health Care Poor Underserved. 2019;30(3):1103–1118 doi: 10.1353/hpu.2019.0076 [DOI] [PubMed] [Google Scholar]
  • 28.Costa de Assis SJ, Lopes JM, Guedes MBOG, Sanchis GJB, Araujo DN, et al. (2021) Primary health care and social isolation against COVID-19 in Northeastern Brazil: Ecological time-series study. PLOS ONE 16(5): e0250493. 10.1371/journal.pone.0250493 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Sarti Thiago Dias, azarini Welington L Serra, Fontenelle Leonardo Ferreira, Almeida Ana Paula Santana Coelho. What is the role of Primary Health Care in the COVID-19 pandemic?. Epidemiol. Serv. Saúde [Internet]. 2020; 29(2): e2020166. Disponível em: http://scielo.iec.gov.br/scielo.php?script=sci_arttext&pid=S1679-49742020000200043&lng=pt. doi: 10.5123/s1679-49742020000200024 [DOI] [PubMed] [Google Scholar]

Decision Letter 0

Bruno Pereira Nunes

6 May 2021

PONE-D-21-10779

COVID-19 IN BRAZILIAN CITIES: IMPACT OF SOCIAL DETERMINANTS, COVERAGE AND QUALITY OF PRIMARY HEALTH CARE

PLOS ONE

Dear Dr. LOPES,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

The manuscript has been assessed by five reviewers. Their comments are appended below. The reviewers have raised some of major concerns about the manuscript, and in particular they feel that important methodological issues exist that affect the technical soundness of your study, and the conclusions of the paper.

Please submit your revised manuscript by Jun 20 2021 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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We look forward to receiving your revised manuscript.

Kind regards,

Bruno Pereira Nunes, Ph.D.

Academic Editor

PLOS ONE

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Please complete your Competing Interests on the online submission form to state any Competing Interests. If you have no competing interests, please state "The authors have declared that no competing interests exist.", as detailed online in our guide for authors at http://journals.plos.org/plosone/s/submit-now

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: No

Reviewer #2: Yes

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: I Don't Know

Reviewer #2: Yes

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The original idea to assess the role of PHC in COVID-19 incidence is good but the adopted methodological approach is very confuse and unclear.

Methods - please cite the original source of data: hospitalizations (SIH), severe cases (SIVEP-Gripe); DATASUS is the "SUS IT department); it is not a dataset.

Please expain how the score that assess the Primary Care Teams is calculated. What is evaluated?

What is "social Gini"? Please explain.

COVID-19 incidence rates were adjusted for age?

Please describe the cities included. Please describe the number of cases and the rates for each city.

Figures are not informative and hard to follow.

Where are the results of the univariate analysis?

Why authors have decided to include in the multiple model only variables with p<0.10? (too scrict criterium)

It is not clear to me if the authors intend to evaluate the influence of socioeconomic and PHC variables in the cumulative incidence of COVID-19 until the 26th week in those cities or if the authors wanted to evaluate the influence of socioeconomic and PHC variables in time-trends in incidence of COVID-19 until the 26th week in those cities.

Please clarify.

Reviewer #2: Introduction

The world has been suffering from a persistent contagion evolution by the new coronavirus (COVID-19 ),

Review: The new virus is SARS-COV-2 and COVID-19 is the disease caused of the virus.

Therefore, the objectives of this study were to identify the socioeconomic and health system factors associated with the diagnosis of COVID-19 in the main cities of each twenty-seven Brazilian federative units, characterizing them in terms of disease burden and evolutionary pattern, providing information for planning public policies for Brazil and countries with a similar profile.

Review: It does not seem to me that the aim of the study was to assess which socioeconomic factors were associated with the diagnosis of COVID-19. Associated factors could be access to health services for symptomatic cases and the number of tests offered.

Methodology

This is an ecological time series study, with quantitative approach, carried out through the analysis of population-based secondary data. The outcome was COVID-19 cases per 100,000 inhabitants, in all Brazilian main largest cities until the 26th epidemiological week.

Review: It was not clear the size of the selected cities.

It was not described in the methodology which COVID-19 case definition and database were used. In Brazil, notification of suspected cases of COVID-19 is mandatory in cases of flu like illness-ILI syndrome or severe acute respiratory syndrome-SARS. After notification, cases are investigated for confirmation of COVID-19 using the following criteria: laboratory, clinical, clinical-epidemiological and clinical-image. The databases are e-sus-VE (ILI) and Sivep-Gripe (SARS).

In the assessment of the Primary Care Teams Certification Score, teams are classified as unsatisfactory - those who have not fulfilled the commitments assumed in the adhesion;

Review. It is necessary to describe the items that were used in the assessment of the PMAQ, the Methodological Teams of Primary Care Certification Score.

In addition to these social indicators, data was also collected on the restriction on education (RE), restriction on housing (RH), restriction on sanitation (RS) and restriction on social protection (RSP).

Review: It would be important to describe which database was used to build the RH, RS and RSP indicator.

It could standardize the incidence coefficients of COVID-19, considering the different age structures in cities, we know that COVID-19 is more severe in the elderly population, with an increase in hospitalizations and deaths.

Results

A total of 857,741 cases were recorded in the Brazilian cities in the analyzed period, with an average of 15,884.09 (±21,604.43), revealing a heterogeneity in the dissemination of cases, seen in figure 1.

Review: Are the cases confirmed or suspected of COVID-19 in Brazil? SARS, flu-like illness both? What is the study period?

Figure 1. Distribution of the incidence of COVID-19 cases in Brazilian cities up to the 26th epidemiological week. Circles are the observed cases and line is the general trend of progression of the cases

Review:I didn't find figure 1.

In order to estimate the effect of the independent variables and to control the effect of their interactions, an adjusted model presented in Table 1

Review: Describe better results of the model, and how to interpret the results of beta in the incidence of the disease, when the values are greater than 1 or less. It was not clear the description of these results.

Discussion:

Review:It would be interesting to include in the discussion articles that corroborate the results. There is talk in Brazil that the Ministry of Health and governments in general

they have not trained and extensively prepared the single health system, especially primary care to track contacts and other policies that could impact the curve of the epidemic.

**********

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Reviewer #1: No

Reviewer #2: No

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PLoS One. 2021 Sep 17;16(9):e0257347. doi: 10.1371/journal.pone.0257347.r002

Author response to Decision Letter 0

28 Jun 2021

Firstly, we would like to thank the reviewers for their suggestions that would greatly improve the manuscript.

The document was extensively revised and readjusted on several points, as listed in the comments associated with the study specifically below.

Review Comments to the Author

Reviewer #1: The original idea to assess the role of PHC in COVID-19 incidence is good but the adopted methodological approach is very confuse and unclear.

“1. Methods - please cite the original source of data: hospitalizations (SIH), severe cases (SIVEP-Gripe); DATASUS is the "SUS IT department); it is not a dataset.”

Answer: Text was adequate as suggested.

“Please expain how the score that assess the Primary Care Teams is calculated. What is evaluated?”

Answer: Teams are classified as unsatisfactory, poor, regular, good, very good, excellent(9). However, in this study a recategorization was performed in 3 categories: low quality - with categories unsatisfactory and poor put together; medium quality - regular and good put together; and high quality - with very good and excellent teams. The database was access in PMAQ site (http://aps.saude.gov.br/ape/pmaq/ciclo3/).

Text was adequate as suggested.

“2. What is "social Gini"? Please explain.”

Answer: The Gini coefficient was used as an instrument to measure the degree of income concentration in the cities, as a measure of social inequality, ranging from 0 to 1, and the closer to 1, the greater the inequality in that location. The calculation of this coefficient is given by the ratio of the areas of the Lorenz curve diagram to the accumulated income of the population. Theses data were collected in the National Household Sample Survey.

Text was adequate as suggested.

“3. COVID-19 incidence rates were adjusted for age?”

Answer: We agree that age groups have an influence on the occurrence of cases sensitive to the need for health services. However, for the purposes of this study, standardization by age has no implication as the age structures of Brazilian capitals are similar. For example, in all capitals the proportion of people aged 60-64 varies from 1.3% to 2.0% and this pattern will be repeated in other age groups https://censo2010.ibge.gov.br/sinopse/index.php?uf=42&dados=26). However, it is to state that the age pattern of contagion is similar among the 27 capitals analyzed according to age.

Furthermore, our objective is to identify the effects of ecological, social, economic and health system conditions and not to compare individual conditions that might be affected by a possible distribution discrepancy between age groups.

“4. Please describe the cities included.

Answer: The description of the capitals of the federative units (states) of brazil were placed in a tableua in the method: non-changing social characteristics in the time series and variables that changed over time.

“5. Please describe the number of cases and the rates for each city.”

Answer: Text was adequate as suggested.

“6. Figures are not informative and hard to follow.”

Answer: Text was adequate as suggested. The four graphics in Figure 1 were submitted separately to facilitate the editorial process. They are arranged from A-D.

“7. Where are the results of the univariate analysis?”

Answer: They were included in tableau 1 as they are not results directly produced in our research. This information exists in the Brazilian information system. Furthermore, our objective is to evidence the effects of the independent variables described in our method.

“8. Why authors have decided to include in the multiple model only variables with p<0.10? (too scrict criterium).”

Answer: Sorry, it was a typo. In fact, the p-value criterion to enter the model was <0.20. Text was adequate as suggested.

“9. It is not clear to me if the authors intend to evaluate the influence of socioeconomic and PHC variables in the cumulative incidence of COVID-19 until the 26th week in those cities or if the authors wanted to evaluate the influence of socioeconomic and PHC variables in time-trends in incidence of COVID-19 until the 26th week in those cities.

Please clarify.”

Answer: Data were analyzed using a matrix of autoregressive correlations in the GEE method. This approach allows us to verify the effects of independent factors on the outcome trend. As the trend of cases in the analyzed period is increasing (week factor), factors that influence the trend have implications for the increase in accumulated cases.

Reviewer #2

“Introduction

1. The world has been suffering from a persistent contagion evolution by the new coronavirus (COVID-19 ),

Review: The new virus is SARS-COV-2 and COVID-19 is the disease caused of the virus.”

Answer: Text was adequate as suggested.

“2. Therefore, the objectives of this study were to identify the socioeconomic and health system factors associated with the diagnosis of COVID-19 in the main cities of each twenty-seven Brazilian federative units, characterizing them in terms of disease burden and evolutionary pattern, providing information for planning public policies for Brazil and countries with a similar profile.

Review: It does not seem to me that the aim of the study was to assess which socioeconomic factors were associated with the diagnosis of COVID-19. Associated factors could be access to health services for symptomatic cases and the number of tests offered.”

Answer: After the analysis, we adjusted the objective. Therefore, the objectives of this study were to identify the socioeconomic and health system factors associated with the accumulation of cases of COVID-19 diagnosed in the capitals of the twenty-seven Brazilian federative units (FU).

“Methodology

1.This is an ecological time series study, with quantitative approach, carried out through the analysis of population-based secondary data. The outcome was COVID-19 cases per 100,000 inhabitants, in all Brazilian main largest cities until the 26th epidemiological week. Review: It was not clear the size of the selected cities.”

Answer: The selected cities are the capitals of the 27 federated states of Brazil. Text was adequated.

“2. It was not described in the methodology which COVID-19 case definition and database were used. In Brazil, notification of suspected cases of COVID-19 is mandatory in cases of flu like illness-ILI syndrome or severe acute respiratory syndrome-SARS. After notification, cases are investigated for confirmation of COVID-19 using the following criteria: laboratory, clinical, clinical-epidemiological and clinical-image. The databases are e-sus-VE (ILI) and Sivep-Gripe (SARS).”

Answer: Text was adequate to meet the suggestions.

“In the assessment of the Primary Care Teams Certification Score, teams are classified as unsatisfactory - those who have not fulfilled the commitments assumed in the adhesion;

Review. It is necessary to describe the items that were used in the assessment of the PMAQ, the Methodological Teams of Primary Care Certification Score.”

Answer: Text was adequate to meet the suggestions.

“In addition to these social indicators, data was also collected on the restriction on education (RE), restriction on housing (RH), restriction on sanitation (RS) and restriction on social protection (RSP).

Review: It would be important to describe which database was used to build the RH, RS and RSP indicator.”

Answer: Text was adequate to meet the suggestions.

“It could standardize the incidence coefficients of COVID-19, considering the different age structures in cities, we know that COVID-19 is more severe in the elderly population, with an increase in hospitalizations and deaths.”

Answer: We agree that age groups have an influence on the occurrence of cases sensitive to the need for health services. However, for the purposes of this study, standardization by age has no implication as the age structures of Brazilian capitals are similar. For example, in all capitals the proportion of people aged 60-64 varies from 1.3% to 2.0% and this pattern will be repeated in other age groups https://censo2010.ibge.gov.br/sinopse/index.php?uf=42&dados=26). However, it is to state that the age pattern of contagion is similar among the 27 capitals analyzed according to age.

Furthermore, our objective is to identify the effects of ecological, social, economic and health system conditions and not to compare individual conditions that might be affected by a possible distribution discrepancy between age groups.

“Results

1. A total of 857,741 cases were recorded in the Brazilian cities in the analyzed period, with an average of 15,884.09 (±21,604.43), revealing a heterogeneity in the dissemination of cases, seen in figure 1.

Review: Are the cases confirmed or suspected of COVID-19 in Brazil? SARS, flu-like illness both? What is the study period?”

Answer: These are all confirmed cases. The period refers to the 13th and 26th epidemiological weeks.

“2. Figure 1. Distribution of the incidence of COVID-19 cases in Brazilian cities up to the 26th epidemiological week. Circles are the observed cases and line is the general trend of progression of the cases

Review:I didn't find figure 1.”

Answer: It was probably an error in the submission system. It is found at the end of the manuscript.

“3. In order to estimate the effect of the independent variables and to control the effect of their interactions, an adjusted model presented in Table 1

Review: Describe better results of the model, and how to interpret the results of beta in the incidence of the disease, when the values are greater than 1 or less. It was not clear the description of these results.”

Answer: Text was adequate to meet the suggestions.

Discussion:

1. “Review:It would be interesting to include in the discussion articles that corroborate the results. There is talk in Brazil that the Ministry of Health and governments in general

they have not trained and extensively prepared the single health system, especially primary care to track contacts and other policies that could impact the curve of the epidemic.”

Answer: Text was adequate to meet the suggestions.

Attachment

Submitted filename: Resposta_Revisores 19.06.21.docx

Click here for additional data file. (22.5KB, docx)

Decision Letter 1

Bruno Pereira Nunes

13 Aug 2021

PONE-D-21-10779R1

COVID-19 IN BRAZILIAN CITIES: IMPACT OF SOCIAL DETERMINANTS, COVERAGE AND QUALITY OF PRIMARY HEALTH CARE

PLOS ONE

Dear Dr. LOPES,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

The reviewer has raised some of minor concerns about the manuscript, and there are some methodological issues that affect the technical soundness of your study.

Please submit your revised manuscript by Sep 27 2021 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

  • A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.

  • A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.

  • An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols.

We look forward to receiving your revised manuscript.

Kind regards,

Bruno Pereira Nunes, Ph.D.

Academic Editor

PLOS ONE

Journal Requirements:

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

Additional Editor Comments (if provided):

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #2: (No Response)

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #2: (No Response)

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #2: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #2: Methods - 1. The COVID-19 reporting systems where data were collected were not detailed. Are they mild and serious cases? Were the systems used e sus ve (mild) and sivepripe (severe)?

2. The standardization of the incidence coefficient would be important, due to the difference in the impact of the disease in the elderly. The proportion of elderly people (> = 60 years) varies from 6.9% in Boa Vista to 20.4% in Porto Alegre, according to data from DATASUS in 2020.

3. As the study was carried out until week 26 of 2020, there were only criteria for confirmation of cases (laboratory and clinical-epidemiological). (Source: file:///C:/Users/AnaRibeiro/Downloads/GuiaDeVigiEp-final.pdf). After 8/5/2020 (SE 31), the new clinical and clinical-image criteria were included (https://portalarquivos.saude.gov.br/images/af_gvs_coronavirus_6ago20_adjustments-finalis-2.pdf).

Results.

Figure 1 shows the image per city per 100,000 inhabitants per city. What is considered each circle. Which cities are shown.

table 1: I do not understand some results. In situations of PHC coverage below 50%, PMAQ score low demonstrated "nine times more cases" per 100,000 inhabitants COVID-19 cases than those with a score medium or high (B=9.08; p<0.001). In the PHC 50-74% stratum, cities with intermediate FHS coverage and PMAQ scores high showed almost "twice less" (B=2,36) COVID-19 incidence rates than cities with lower ratings.

For the interpretation of Gini and HDI, it is more appropriate to observe the interaction of these factors and not the main effect. The Gini-HDI interaction shows a negative relationship (B=-72.46; p<0.001), which may suggest a mitigating effect in cities with high HDI and low Gini.

**********

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Reviewer #2: No

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PLoS One. 2021 Sep 17;16(9):e0257347. doi: 10.1371/journal.pone.0257347.r004

Author response to Decision Letter 1

20 Aug 2021

EDITOR

Editor-in-Chief

Plos One

Aug 20, 2021.

Dear Editor,

Thank you for your email with the reviewers’ comments. We have reviewed the comments and edited the manuscript accordingly. Please, find attached our point-by-point response to the reviewers. All authors have read this protocol and agreed with Plos One policy. We hope the revised manuscript is now suitable for publication.

Sincerely. Johnnatas Mikael Lopes.

Reviewer Comments:

Comments to the Author:

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #2: (No Response)

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #2: Yes

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #2: Yes

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #2: (No Response)

Response: All data used for this manuscript is in the public domain. In the Methods section you will find all this information, as well as links to access the full material.

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #2: Yes

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #2:

Methods –

1. The COVID-19 reporting systems where data were collected were not detailed. Are they mild and serious cases? Were the systems used e sus ve (mild) and sivepripe (severe)?

Response: Thank you for your comments. In the present study, no differentiation was made between severe and mild cases. Cases diagnosed by COVID-19 were used, according to data extracted from the Covid-19 Panel (https://covid.saude.gov.br/) database, fed by the Health Surveillance Department and made available by the SUS Informatics Department. This information can be found in the methods section of the manuscript.

2. The standardization of the incidence coefficient would be important, due to the difference in the impact of the disease in the elderly. The proportion of elderly people (> = 60 years) varies from 6.9% in Boa Vista to 20.4% in Porto Alegre, according to data from DATASUS in 2020.

Response: We agree with the reviewer that the higher proportion of elderly people in the capitals of the southern region of the country make them more likely to have COVID-19 cases. However, this difference in reported proportion does not match official data from the Brazilian Institute of Geography and Statistics, the official body for this information (https://censo2010.ibge.gov.br/sinopse/index.php?uf=43&dados=26#topo_piramide).

In any case, the objective of the research is not to estimate the differences in the load of COVID-19 between the capitals, where standardization would be of great importance, as the age composition would impact the compared estimates.

The objective was to estimate the effects of socioeconomic conditions and health system organization prior to the pandemic on the occurrence of COVID-19 cases. In this facet, the effect of age composition is reduced in the inferences, as the comparison is made with levels of independent variables, such as coverage of the PHC and FHS, which do not suffer a direct effect from the age composition. Furthermore, they assume that the primary health care system must be organized according to the local population profile.

Thus, the inferential analysis does not compare the Brazilian capitals, but analyzes them as a single group, being stratified by factors such as healthcare coverage.

3. Como o estudo foi realizado até a semana 26 de 2020, havia apenas critérios para confirmação dos casos (laboratoriais e clínico-epidemiológicos). (Fonte: arquivo: /// C: /Users/AnaRibeiro/Downloads/GuiaDeVigiEp-final.pdf). Após 05/08/2020 (SE 31), os novos critérios clínicos e de imagem clínica foram incluídos (https://portalarquivos.saude.gov.br/images/af_gvs_coronavirus_6ago20_adjustments-finalis-2.pdf).

Response: Thank you for your comments. The following sentences were added:

To date, only criteria for confirmation of cases (laboratory and clinical-epidemiological) were used as a form of diagnosis of Covid-19, using immunological tests, rapid test or classical serology for the detection of antibodies.

Results.

4. Figure 1 shows the image per city per 100,000 inhabitants per city. What is considered each circle. Which cities are shown.

Response: Figure 1 shows a general graph of the incidence in each city analyzed (circles) in order to show the exponential evolutionary profile in all of them.

5. table 1: I do not understand some results. In situations of PHC coverage below 50%, PMAQ score low demonstrated "nine times more cases" per 100,000 inhabitants COVID-19 cases than those with a score medium or high (B=9.08; p<0.001). In the PHC 50-74% stratum, cities with intermediate FHS coverage and PMAQ scores high showed almost "twice less" (B=2,36) COVID-19 incidence rates than cities with lower ratings.

Response: The first interpretation is correct. This is equivalent to stating that in situations of low PHC coverage, having better quality of care had an impact on the dissemination of COVID-19. On the other hand, the second statement is based on the inverse interpretation of the model's coefficient relative to the worst-case coverage and quality of care. This inversion of interpretation may have led to confusion.

6. For the interpretation of Gini and HDI, it is more appropriate to observe the interaction of these factors and not the main effect. The Gini-HDI interaction shows a negative relationship (B=-72.46; p<0.001), which may suggest a mitigating effect in cities with high HDI and low Gini.

Response: In multivariate analyses, when there is an interaction between factors, their interpretation prevails over that of isolated factors, which may contain measurement biases.

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

Response: Yes, the authors choose to publish the peer review history of this article

All changes made are highlighted in the manuscript.

Thank you for your comment. The manuscript has been revised accordingly.

Sincerely,

Johnnatas Mikael Lopes

Attachment

Submitted filename: Response to Reviewers_Covid_Brazil 20.08.pdf

Click here for additional data file. (204.9KB, pdf)

Decision Letter 2

Bruno Pereira Nunes

31 Aug 2021

COVID-19 IN BRAZILIAN CITIES: IMPACT OF SOCIAL DETERMINANTS, COVERAGE AND QUALITY OF PRIMARY HEALTH CARE

PONE-D-21-10779R2

Dear Dr. LOPES,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org.

If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

Kind regards,

Bruno Pereira Nunes, Ph.D.

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Acceptance letter

Bruno Pereira Nunes

9 Sep 2021

PONE-D-21-10779R2

COVID-19 IN BRAZILIAN CITIES: IMPACT OF SOCIAL DETERMINANTS, COVERAGE AND QUALITY OF PRIMARY HEALTH CARE

Dear Dr. LOPES:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

If we can help with anything else, please email us at plosone@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Bruno Pereira Nunes

Academic Editor

PLOS ONE

Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    Attachment

    Submitted filename: Resposta_Revisores 19.06.21.docx

    Click here for additional data file. (22.5KB, docx)
    Attachment

    Submitted filename: Response to Reviewers_Covid_Brazil 20.08.pdf

    Click here for additional data file. (204.9KB, pdf)

    Data Availability Statement

    All 3 covid-19 files are available from the DATASUS database (https://covid.saude.gov.br/).

    Articles from PLoS ONE are provided here courtesy of PLOS

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