NOGUEIRA Et Al (2022) - COVID-19's Intra-Urban Inequalities and Social Vulnerability in A Medium-Sized City
NOGUEIRA Et Al (2022) - COVID-19's Intra-Urban Inequalities and Social Vulnerability in A Medium-Sized City
Major Article
[1]. Universidade Federal de Juiz de Fora, Faculdade de Medicina, Departamento de Saúde Coletiva, Juiz de Fora, MG, Brasil.
[2]. Universidade Federal de Juiz de Fora, Instituto de Ciências Exatas, Departamento de Estatística, Juiz de Fora, MG, Brasil.
[3]. Universidade Federal de Juiz de Fora, Faculdade de Medicina, Departamento de Internato, Juiz de Fora, MG, Brasil.
ABSTRACT
Background: Social conditions are related to the impact of epidemics on human populations. This study aimed to investigate the spatial
distribution of cases, hospitalizations, and deaths from COVID-19 and its association with social vulnerability.
Methods: An ecological study was conducted in 81 urban regions (UR) of Juiz de Fora from March to November 2020. Exposure was
measured using the Health Vulnerability Index (HVI), a synthetic indicator that combines socioeconomic and environmental variables from
the Demographic Census 2010. Regression models were estimated for counting data with overdispersion (negative binomial generalized
linear model) using Bayesian methods, with observed frequencies as the outcome, expected frequencies as the offset variable, and HVI as the
explanatory variable. Unstructured random-effects (to capture the effect of unmeasured factors) and spatially structured effects (to capture
the spatial correlation between observations) were included in the models. The models were estimated for the entire period and quarter.
Results: There were 30,071 suspected cases, 8,063 confirmed cases, 1,186 hospitalizations, and 376 COVID-19 deaths. In the second
quarter of the epidemic, compared to the low vulnerability URs, the high vulnerability URs had a lower risk of confirmed cases (RR=0.61;
CI95% 0.49–0.76) and a higher risk of hospitalizations (RR=1.65; CI95% 1.23–2.22) and deaths (RR=1.73; CI95% 1.08–2.75).
Conclusions: The lower risk of confirmed cases in the most vulnerable UR probably reflected lower access to confirmatory tests, while
the higher risk of hospitalizations and deaths must have been related to the greater severity of the epidemic in the city’s poorest regions.
Keywords: COVID-19. Spatial analysis. Social inequality. Urban health.
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Nogueira MC et al. | Intra-urban inequalities of COVID-19
entry and dissemination of COVID-19. After the first confirmed case new world standard population8. In addition, the relative risks (RRi)
on March 9, 2020, the epidemic expanded in the following months were also estimated as the ratio between the observed (Yi) and
to most municipalities in the state6. Juiz de Fora is the pricipal city expected (Ei) cases in each UR:
of the southeastern health macro-region of the state and the fourth
most populous city in the Zona da Mata region, with almost 600
thousand inhabitants. With an Human Development Index (HDI) of
0.778, it has almost 30% of the population with a nominal monthly
To consider the differences in age structure between the
income per capita of up to 1/2 minimum wage, according to the
different URs, the expected cases of each UR (Ei) were estimated
last demographic census (https://cidades.ibge.gov.br/brasil/mg/ as the sum of the expected values in each age group obtained by
juiz-de-fora/panorama). The city had its first confirmed case on multiplying the specific rates per age group of the city (rj(s)) by the
March 10, 20207, and according to the web platform “JF Salvando specific population of the age group in each UR (nj):
Todos” (http://jfsalvandotodos.ufjf.br/), on June 6, 2021, it had
34,296 cases and 1,657 confirmed by COVID-19 deaths.
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−21.60 −21.60
AR
−21.65 Central −21.65
East Vulnerability
Northeast Low
−21.70 North −21.70 Medium
West High
Southest
−21.75 South −21.75
−21.80 −21.80
Suspected Confirmed
−21.55 −21.55
−21.60 −21.60
−21.80 −21.80
Hospitalizations Deaths
−21.55 −21.55
−21.60 −21.60
−21.80 −21.80
FIGURE 1: Urban Regions (UR) of Juiz de Fora by Administrative Regions (AR) and by Health Vulnerability Index (HVI) categories, and standardized rates of
suspected, confirmed, hospitalizations and deaths by COVID-19 in Juiz de Fora, March to November 2021.
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Three mixed generalized linear models were fitted, with a log link Ethical considerations
function and negative binomial family: a) model only considering
all factors as fixed effects; b) the previous model with the inclusion This project was approved by the Research Ethics Committee
of an unstructured random effect, which can capture the effect of the Federal University of Juiz de Fora on 09/02/2020 (CAAE No.
of unmeasured factors; and c) model with the inclusion of both 36855920.0.0000.5133).
the unstructured random effect and a structured spatial effect, RESULTS
which can capture the spatial correlation between observations.
The criterion for choosing the best model was the lowest value There were 30,071 notifications of FS from March to November
of DIC (deviance information criterion). The Bayesian estimation 2020, of which 8,063 had positive laboratory test results for
method used was the integrated nested Laplace approximation COVID-19. In the same period, 1,186 hospital admissions were
(INLA), using the INLA library (http://www.r-inla.org/) of the R confirmed for COVID-19, of which 376 progressed to death. There
program (https://cran.r-project.org /). Relative risk posteriors are was a higher proportion of women for suspected and confirmed
summarized as the mean for point estimates and their respective cases and a higher proportion of men for admissions and deaths.
95% credibility intervals (CI95%). Cases predominated in the age groups of 20 to 39 years and 40
to 59 years, while hospitalizations and deaths predominated in
The three models are described below. those over 60 years. Owing to the large proportion of missing
data regarding race/color, it is not possible to determine its
Model A:
actual distribution. There were 283 notifications of FS in pregnant
women, of which 41 had a laboratory confirmation, but only three
hospitalizations and no deaths. The proportion of people at high risk
of unfavorable prognosis due comorbidities increased from 22.71%
of FS notifications to 90.69% of deaths. Regarding the categories of
social vulnerability of the place of residence, a greater proportion
of patients in the UR had medium vulnerability. In relation to AR,
although the central region had the highest proportion of cases, the
Model B: east region had the highest proportion of deaths. Most notifications
of suspected cases were made in hospital shifts (45.90%) or basic
health units (20.85%), whereas confirmed cases were notified in
other places, such as clinical analysis laboratories (Table 1).
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TABLE 1: Characteristics of suspected and confirmed cases, hospitalizations, and deaths due to COVID-19 of residents in the urban area of Juiz de Fora from March
to November 2020.
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Nogueira MC et al. | Intra-urban inequalities of COVID-19
Suspected Confirmed
High−High High−High
Low−Low Low−Low
High−Low High−Low
Low−High Low−High
N. Sig. N. Sig.
Hospitalizations Deaths
High−High High−High
Low−Low Low−Low
High−Low High−Low
Low−High Low−High
N. Sig. N. Sig.
FIGURE 2: Local spatial autocorrelation (LISA) maps for standardized rates of suspected, confirmed, hospitalizations and deaths by
COVID-19 from March to November 2020 in Juiz de Fora / MG. N. Sig.: not significant.
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TABLE 2: Distribution of indicators in urban regions (UR) of the municipality and Moran's coefficient I (spatial autocorrelation measure), by period, March to November
2020, Juiz de Fora/MG.
*I: Moran's coefficient, significant at the 5% level; HVI: Health vulnerability index; Rate: Standardized rates per 100,000 people; SD: standard deviation; Min: minimum;
Q1: first quartile; Q2: median; Q3: third quartile; Max: maximum; Period 1: March to May; Period 2: June to August; Period 3: September–November.
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total ● ● ● ●
period3 ● ● ● ●
HVI_high
period2 ● ● ● ●
period1 ● ● ● ●
Period
total ● ● ● ●
period3 ● ● ● ●
HVI_medium
period2 ● ● ● ●
period1 ● ● ● ●
1 2 1 2 1 2 1 2
RR (CI95%)
FIGURE 3: Results of the regression models (relative risk – RR and 95% credible interval – CI95%) between the Health Vulnerability
Index (HVI) and the risk of suspected cases, confirmed cases, hospitalizations, and deaths from COVID- 19 in residents of the urban
area of Juiz de Fora from March to November 2020.
vulnerability URs had a lower risk of confirmed cases in all the spreading to the periphery. Thus, in the initial period (March to
periods. The risk of hospitalization had the opposite behavior, May 2020), there was no difference in the risk of hospitalization
with a greater risk in the UR of medium vulnerability in the second or death according to the vulnerability of the urban regions. In
period (June to August) and in the UR of high vulnerability in the period 2 (June to August 2020), there was an increased risk of
second and third period (September to November), while hospital hospitalizations and deaths in the most vulnerable regions. In
deaths also presented an increased risk in the medium and high the final period (September to November 2020), the increase in
vulnerability URs, but only in the second period (Figure 3). hospitalizations and deaths was more widespread, especially in
November, when the second wave started in the city.
DISCUSSION
This study showed spatial heterogeneity in the risk of In a study that analyzed data from Brazil by states and
notifications, confirmations, hospitalizations, and deaths due municipalities between February and October 2020, inequalities
to COVID-19 in the urban area of Juiz de Fora, a medium-sized during the epidemic associated with social vulnerability were
city in Minas Gerais. It also highlighted that this heterogeneity also identified. The epidemic initially had a greater burden in
was associated with socio-environmental vulnerability in the city more vulnerable states and municipalities; however, due to more
districts, with the lowest vulnerability presenting a greater risk intense social distancing measures in these states, there was better
of notifying confirmed cases, while the most vulnerable districts evolution, with lower mortality rates in the final period of the study12.
presented a greater risk of hospitalizations and deaths.
Some studies in Brazilian municipalities have found results
During the study period, access to services, reflected in similar to those presented here. A study carried out in the city
notifications of suspects, did not differ between areas with of Santa Maria/RS found that at the beginning of the epidemic,
different levels of vulnerability, while the risk of confirmed cases there was a greater concentration of confirmed cases of COVID-19
was lower for the most vulnerable regions, suggesting difficulty in in more central neighborhoods, and during the epidemic, there
accessing the tests generating underreporting of confirmed cases, was a peripheralization of the epidemic to neighborhoods with
especially on the outskirts of the city. The risk of hospitalizations greater social deprivation13. A study conducted in the districts
and deaths due to COVID-19, on the other hand, was higher in of São Paulo municipality found that the incidence of COVID-19
the most vulnerable regions, which does not seem to be related was concentrated in clusters of districts with a higher proportion
to underreporting since these cases had priority for testing. The of slums and lower salaries14. Rio de Janeiro, the second-most
epidemic began in the wealthiest regions of the city, before populous city in Brazil with great social inequality, also showed
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spatial heterogeneity in vulnerability to severe cases of COVID-19, inequality and ethnic-racial composition24. In New York and other
identifying the most vulnerable areas as those with the highest urban centers, some vulnerable groups were most affected by
density of residents per household, the highest density of older the COVID-19 epidemic, such as African Americans, Latinos,
people, and a higher incidence of tuberculosis15. immigrants, and native peoples. Some of the structural causes of
these inequalities create barriers for these social groups to practice
Less access to diagnostic tests in socially more vulnerable areas social distancing, such as residential segregation and structural
was also verified in a study carried out in the metropolitan region
racism25. In another study conducted in Chicago, spatial clusters of
of São Paulo, in which confirmation of the disease was positively
social vulnerability and risk factors for death from COVID-1926 were
associated with higher per capita income in the census sector
found. An ecological study showed an association between areas
of residence1. Vulnerable populations in Brazil have poor access
with greater income inequality, as measured by the Gini index, and
to essential health services in the case of COVID-19, especially
higher incidence and mortality rates of COVID-19 in the USA27.
low-income communities with a predominance of people of black
race/color in the urban peripheries of large cities16. In a study In European countries, social inequalities related to the
carried out with data on hospitalizations for COVID-19 in Brazil COVID-19 pandemic have been identified. A study conducted in
between the beginning of the epidemic and mid-May, regional
Sweden showed that the infection rate was 3–4 times higher in
and ethnic-racial inequalities in mortality were evidenced. It was
socioeconomically vulnerable areas28. In a survey representative
hypothesized that regional inequalities, with higher mortality in the
of the UK population, social groups with households of more than
North and Northeast of the country, would be related to a greater
five people had the greatest impact on their well-being during the
burden of comorbidities in regions with lower socioeconomic
epidemic and lockdown measures29.
development, while ethnic-racial inequalities, with higher mortality
of black and brown people , would be related to less access to There was an expectation that Brazil could do well in controlling
health services17. In another study carried out with adults admitted the epidemic, as it has a universal health system centered on a
for COVID-19 until the beginning of October 2020, a higher risk of primary care strategy with community agents in the most socially
death was also identified in black and brown people, in addition
vulnerable areas; in the recent past, it has shown effectiveness in
to indigenous people18.
controlling various diseases and in reducing health inequalities2.
Spatial inequalities in health are present in territories marked At the beginning of the pandemic, several measures were
by vulnerabilities with historical origins updated by new economic, implemented, including the declaration of a national public health
social, and political dynamics. They are manifested by inequalities emergency in January 2020, activation of an emergency health
in the risks of exposure, illness, and aggravation as well as by operation center, and recommendation of health surveillance
differentiated access to health actions and services. The current measures and social distancing30. However, this expectation did
economic moment of globalization accentuates social and health not materialize, since Brazil has become one of the countries
inequalities for several reasons, including the generation of more with the highest incidence and mortality from COVID-19. A
frequent and intense economic crises and increased structural characteristic of the Brazilian response to the pandemic was the
poverty, resulting from greater competition and selectivity of lack of coordination by the federal government during its course,
economic processes. In Brazil, these inequalities are especially which still promoted ineffective interventions. The epidemic rapidly
important, as Brazil is one of the most unequal countries globally, spread to the country’s interior, with some differences between
which has been increasing. Inequality is also manifested in the states. Some factors that could be related would be large disparities
indicators of the COVID-19 pandemic, whether in incidence, in economic and health resources; the great communication
mortality, lethality rates, or access to health services19. between municipalities and regions in terms of transport, services,
and trade; the alignment of some state and municipal government
Studies carried out in Juiz de Fora on other health outcomes,
officials with the conduct of the federal government in denying the
such as mortality from acute myocardial infarction20 and incidence
importance of social distancing measures; the circulation of the
of tuberculosis9, also showed a similar pattern of lower rates in the
virus was not detected early due to the difficulties of well-equipped
city’s central area and higher rates in more peripheral regions. This
health surveillance and the lack of coordination, coherence, and
is due not only to a compositional effect, as in the central area,
criteria in state and municipal decisions about the closing and
there is a greater proportion of people with higher income and
opening moments of non-essential activities2.
education, but also to a contextual effect, as the more peripheral
regions are marked by more precarious infrastructure with less This study showed that, in medium-sized cities, various aspects
access to services in general. of the behavior of the COVID-19 epidemic are closely related to
In the US, there are regional inequalities in access to health the life context of population groups. Although the public health
services, specifically to COVID-19 confirmation tests, which can services network has guaranteed equity in access to first care,
compromise the control of the epidemic by being related to the reflected in the notification of suspected cases, it has not brought
undetected spread of the disease21. In New York City, a study the same guarantee for access to examinations needed to confirm
identified an association between areas with a higher proportion the disease. More importantly, social vulnerability was associated
of blacks, Hispanics, and poor people with a higher proportion with a higher risk of severe disease progression, thus unveiling the
of positive tests for COVID-1922. In the state of Georgia, a set social inequality of the impact of this pandemic on the population.
of socioeconomic indicators, which included the percentage of The planning of disease prevention and control actions, not only
children in poverty and the percentage of adults without health COVID-19 but also other communicable or noncommunicable
insurance, was associated with the incidence rate of COVID-1923. diseases, should consider territorial-based epidemiological
In the first 200 days of the epidemic in US counties, the incidence surveillance so that public policy interventions can reduce social
and mortality rates of COVID-19 were associated with income inequalities in health.
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Nogueira MC et al. | Intra-urban inequalities of COVID-19
ACKNOWLEDGMENTS 15. Santos JPC, Siqueira ASP, Praça HLF, Albuquerque HG. Vulnerabilidade
a formas graves de COVID-19: uma análise intramunicipal na cidade
We offer our thanks to the Subsecretaries of Health Surveillance do Rio de Janeiro, Brasil. Cad Saude Publica. 2020;36(5):e00075720.
of the Health Department of the City of Juiz de Fora for providing 16. Pereira RHM, Braga CKV, Servo LM, Serra B, Amaral P, Gouveia N, et al.
the data used in the analysis. Geographic access to COVID-19 healthcare in Brazil using a balanced
float catchment area approach. Soc Sci Med. 2021;273:113773.
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