Risk factors for death due to COVID-19, in the state of Acre, Brazil, 2020: a retrospective cohort study

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Original
 article      Risk factors for death due to COVID-19, in the state of Acre,
              Brazil, 2020: a retrospective cohort study
              doi: 10.1590/S1679-49742021000300018

           Patrícia Rezende do Prado¹ - orcid.org/0000-0002-3563-6602
           Fernanda Raphael Escobar Gimenes² - orcid.org/0000-0002-5174-112X
           Marcos Venicius Malveira de Lima³ - orcid.org/0000-0002-0332-2721
           Virgilio Batista do Prado4 - orcid.org/0000-0003-0394-2143
           Carolina Pontes Soares1 - orcid.org/0000-0002-9897-5863
           Thatiana Lameira Maciel Amaral1 - orcid.org/0000-0002-9197-5633

           ¹Universidade Federal do Acre, Centro de Ciências da Saúde e do Desporto, Rio Branco, AC, Brazil
           ²Universidade de São Paulo, Escola de Enfermagem de Ribeirão Preto, Ribeirão Preto, SP, Brazil
           ³Secretaria de Estado de Saúde do Acre, Departamento de Vigilância Epidemiológica, Rio Branco, AC, Brazil
           4
            Secretaria de Estado de Saúde do Acre, Rio Branco, AC, Brazil

           Abstract
               Objective: To analyze risk factors for death in individuals with severe acute respiratory syndrome due to COVID-19.
           Methods: This was a retrospective cohort study, comprised of adult individuals with COVID-19, from March to September 2020,
           notified by the Epidemiological Surveillance System in the state of Acre, Brazil. Cox regression was used. Results: Among 57,700
           individuals analyzed, the incidence was 2,765.4/100,000 inhabitants, and mortality was, 61.8/100,000 inhabitants. The risk
           factors for death were: being male (HR=1.48 -95% CI 1.25;1.76), age ≥60 years (HR=10.64 -95% CI 8.84;12.81), symptom
           of dyspnea (HR=4.20 -95% CI 3.44;5.12) and multimorbidity (HR=2.23 -95% CI 1.77;2.81), with emphasis on heart disease
           and diabetes mellitus. 'Sore throat' and 'headache' were symptoms present in mild cases of COVID-19. Conclusion: Being
           male, elderly, having heart disease, diabetes mellitus and dyspnea were characteristics associated with death due to COVID-19.
               Keywords: Severe Acute Respiratory Syndrome; Coronavirus infections; Longitudinal studies; Risk Factors; Mortality.

           Correspondence:
           Thatiana Lameira Maciel Amaral - Universidade Federal do Acre, Centro de Ciências da Saúde e do Desporto, Campus
           Universitário, BR 364, Km 4, Distrito Industrial, Rio Branco, AC, Brazil. CEP: 69920-900
           Postcode: 500
           E-mail: thatianalameira27@gmail.com

                                                Epidemiol. Serv. Saude, Brasília, 30(3):e2020676, 2021                                   1
Risk factors for death due to COVID-19

Introduction                                                        The aim of this research was to analyze the
                                                                 epidemiological characteristics and risk factors for
   Severe acute respiratory syndrome (SARS) due to               death in individuals with SARS due to COVID-19 in the
COVID-19 (SARS due to COVID-19) is a viral respiratory           state of Acre, Brazil, in 2020.
disease caused by a newly discovered coronavirus. It was
identified in Wuhan, Hubei Province, China, in December          Methods
2019.1 The novel coronavirus has high transmissibility
and can cause severe acute respiratory syndrome and                 This was a retrospective longitudinal cohort study.
deaths. At the end of September, 2020, more than 32.7            Acre is located in the northern region of the country,
million COVID-19 cases and more than 1 million deaths            in the Western Brazilian Amazon, borders Peru and
had been confirmed worldwide. The American Continent             Bolivia, and had an estimated population of 881,935
was the hardest hit, with a number of cases exceeding            people on July 1, 2019.5 The state has 380 health
16.2 million. Brazil was the second worst affected               facilities, including centers and hospitals, distributed
country by COVID-19 in the Americas, with 4.8 million            among 22 municipalities.6
confirmed cases and more than 143 million deaths.2                  The study included all COVID-19 cases reported
                                                                 in Acre by September 1, 2020. The first COVID-19
                                                                 notification, in the state, occurred on March 15, 2020,
    A lot of research is being conducted                         with the reported symptoms having started the day
    in the search for practices based on                         before; the last case included in the study presented
    scientific evidence. It is fundamental to                    the first symptoms four days before notification, on
    contribute with epidemiological studies                      September 1, 2020. The time-zero of the cohort was
    aimed at health promotion, disease                           defined by the date of onset of symptoms, and delta-
                                                                 time (∆T) corresponded to the time between the date
    prevention and hospital care planning,                       of symptom onset and outcome (cure or death) for
    with identification of individuals                           cases with diagnostic confirmation of SARS due to
    subject to risk factors for mortality.                       COVID-19. The follow-up time was 60 days, started
                                                                 from the date of the first symptoms.
   The pandemic has dramatically affected health                    Every case of SARS is compulsorily notified and typed
services. Many studies have been conducted in the                individually on the Influenza Surveillance Information
quest for practices based on scientific evidence. It is          System (SIVEP-Gripe), whose data were used on this
essential to contribute to epidemiological studies aimed         notification system. On January 30, 2020, SARS due to
at health promotion, disease prevention and health               COVID-19 was declared as a public health emergency of
care planning, with the identification of individuals            international concern, by WHO, therefore the Ministry
subjected to risk factors for mortality.3                        of Health, through Technical Note No. 20/2020-SAPS/
   In this scenario, some risk factors for mortality             GAB/MS, made it compulsory to notify cases in order
associated with SARS due to COVID-19 have been                   to enable longitudinal epidemiological investigation
suggested, such as severe lymphopenia, high levels of            and formulation of health policies and strategies. This
C-reactive protein (correlated with severe hypoxemia),           was the objective of this research.7
older age(≥60 years), male gender, race/skin color                  The diagnosis of COVID-19 was performed through
(non-white), lower socioeconomic level, presence of              laboratory tests such as, molecular test (RT-PCR) or
comorbidities (e.g., diabetes mellitus, cardiovascular           immunological test.
diseases, hypertension and cancer, presence of fever,               SARS was defined by the concomitant presence
dyspnea, cough and immunocompromised status), as                 of four criteria: (i) fever, even if self-reported, (ii)
well as obesity and unhealthy lifestyle.4 However, such          cough or sore throat, (iii) dyspnea or O2 saturation
factors may change depending on the characteristics
Patrícia Rezende do Prado et al.

the public or private sector, throughout the national        was used to analyze the continuous variables; and
territory and according to the current legislation,          categorical variables were described using absolute
issued within 24 hours.                                      (n) and relative (%) frequency. Pearson's chi-square
   The notification form of the e-SUS Epidemiological        test and/or Fisher's exact test were used to compare
Surveillance (e-SUS VE) contains the following               independent variables with less than five occurrences.
information related to individuals: notification number;         Risk factors for death were analyzed using Cox
Federative Unit and notifying municipality; Individual       regression to estimate hazard ratio (HR) and their
Taxpayer Registration Number (CPF); whether the              respective 95% confidence intervals (95%CI).
individual who was notified is a foreigner, health           Multivariate analysis was performed using the variables
professional or public security professional; date of        that presented p
Risk factors for death due to COVID-19

Table 1 – Characterization of the individuals who got tested for COVID-19 (N=57,700) according to test results,
          notified, Acre, Brazil 2020
                                                                                                              Total          Positive             Negative
 Variable                                                                                                                                                              p-valuea
                                                                                                                 N       N               %       N               %
 Sexb                                                                 Male                                    26,296   11,342           46.5   14,954           45.0
Patrícia Rezende do Prado et al.

Continuation

Table 2 – Distribution of COVID-19 cases (n=24,389) according to municipality of residence, signs and
          symptoms, and presence of multimorbidity, Acre, Brazil, 2020
 Variable                                                                                                                                                                 N          %
 Multimorbidity                                                                                     Yes                                                               1,492          5.9
                                                                                                    Heart disease                                                        834         3.3
                                                                                                    Diabetes mellitus                                                    443         1.7
                                                                                                    Chronic respiratory disease                                          186         0.7
 Reported Morbidities                                                                               Chronic kidney disease                                               103         0.7
                                                                                                    Immunosuppression                                                    173         0.7
                                                                                                    Chromosomal disorder                                                  61         0.2
                                                                                                    High-risk pregnancy                                                   63         0.2

Table 3 – Distribution of SARSa cases due to COVID-19 (n=18,987) according to epidemiological, clinical and
          occurrence of death outcome due to the disease, Acre, Brazil, 2020
                                                                                                                                Total                       Death
 Variable                                                                                                                                                                       p-valueb
                                                                                                                                  N                    N             %
 Sexc                                                                        Male                                               8,905                 333           3.7
Risk factors for death due to COVID-19

Table 4 – Risk factors for death due to COVID-19a, Acre, Brazil, 2020
                                                                                                                                                Adjustede
 Variable                                                                     Crude HRb               95%ICc               p-valued                                    95%ICc               p-valued
                                                                                                                                                   HRb
 Sex                                                    Male                      1.78              1.49;2.11
Patrícia Rezende do Prado et al.

male, 60 years of age or older, dyspnea, presence of            ICU and may progress to acute respiratory distress
multimorbidity, especially diabetes mellitus and heart          syndrome (ARDS), with high mortality.4 In Rio Branco,
diseases; among the symptoms and signs related to better        the prevalence of body mass index (BMI) above 25 kg/
prognosis, the presence of sore throat and headache, as         m² is 48.4% among individuals aged 18 to 39 years, and
well as being a health professional stood out.                  62.1% in the age group 40 to 59 years,15 which also
    The pandemic began in Acre in mid-March 2020. At            puts the younger population at risk, given that adipose
that moment, the emergence of COVID-19 in the state,            tissue serves as a reservoir for the virus.16
represented an advantage for Acre by allowing more time             It has been shown that health professionals,
to plan a regional Public Health response. In addition,         especially nursing technicians, physicians and nurses
the city of Rio Branco has a specialized infectious disease     are at greater risk of contracting COVID-19 because
laboratory, which allowed the identification of cases at        they are at the forefront of health actions in the face
the beginning of the pandemic. Isolation measures, such         of the pandemic. These professionals in their daily
as suspension of classes and restriction on non-essential       work, risk their lives to save patients with SARS due
activities, were also implemented early, in order to            to COVID-19, despite physical and mental exhaustion,
reduce the impact on the health system. However, these          the concern and agony of having to make difficult
advantages and measures taken did not fully stop the            decisions about patient screening process in health
spread of the disease, and deaths were inevitable.              care services, the grief of losing patients, colleagues,
    In this study, the profile of infected individuals shows    friends, and also, the fear of transmitting the infection
that those at productive age are at higher risk of infection.   to their families. The lack of personal protective
However, the higher mortality observed in individuals           equipment (PPE) is also a concern17 and, despite the
aged 60 years or older corroborates the data obtained           high infection rate, this study did not find an increased
in a study with 1,808 COVID 19 cases in the city of Rio de      risk of mortality among health professionals. As if this
Janeiro, state capital of Rio de Janeiro, where, according      were not enough, the high viral load in the most severe
to the researchers involved, people aged 30 to 59 years         cases, puts the professionals responsible for their
were more frequent among the cases, while individuals           care, among the groups at higher risk of infection,4
aged 60 to 89 years had a higher mortality rate.8               in addition to the asymptomatic and presymptomatic
    Data from SouthKorea9 and Germany,10 in turn,               transmission that accounted for, respectively, 51.7%18
showed a high incidence in the second decade of                 and 44.0%19 of the new infections.
life, an aspect to be considered equally, given that the            Regarding symptomatic people, the main symptoms
German study suggested that this age group has played           observed were: fever and cough; sore throat and
an important role in the spread of the epidemic, even           dyspnea were also present among them. These findings
after the implementation of social distancing measures.         corroborate a review of 65 articles, according to
In Italy, among Intensive Care Unit (ICU) cases, a mean         which, other symptoms such as headache, diarrhea,
age of 63 years was observed, and only 13.0% were               hemoptysis and runny nose, although less frequent,
less than 51 years old.11                                       were also identified; 20 and the most important
    Elderly patients with COVID-19 are more likely to           predictors of COVID-19 infection, loss of smell and
progress to severe disease,12 although recent studies           loss of taste, were also identified in another study.21
point out that young people are not free of this                    Hyposmia is a prevalent symptom in individuals with
condition when they are obese. A study conducted in             COVID-19, being more frequent in this disease than in
the United States showed that the prevalence of obesity         other respiratory tract infections. It has been described
was nearly 40%, while in China, this condition was              as a symptom with a high positive predictive value of
6.2%.13 In France, a significant association was found          coronavirus infection (88.8%) and, also, as the initial
between prevalence of obesity and SARS due to severe            symptom in up to 35% of the cases of the disease. It
COVID-19, suggesting that obesity might be a risk factor        has been associated with less severe cases,3 as revealed
for severe disease progression and, consequently, a             in the cohort of this study.
higher risk of ICU admission.14                                     Among the symptoms reported, regarding
    Severe disease involves bilateral interstitial              the presence of dyspnea, there was a statistical
pneumonia, which requires ventilatory support in the            difference between those who died and those who

                                 Epidemiol. Serv. Saude, Brasília, 30(3):e2020676, 2021                                  7
Risk factors for death due to COVID-19

survived. Dyspnea is reported in severe cases, given             underreported cases. However, the use of this database
that COVID-19 uses the angiotensin-converting                    allows to trace the profile of severe cases of SARS due to
enzyme 2 (ACE2) as a receptor, which is widely                   COVID-19, fundamental in times of pandemic.
found in lung, intestinal, kidney and blood vessel                   Another point to be considered is the self-report of
tissues. Moreover, this process results in the release           multimorbidity, which may result in underreporting
of cytokines and consequent damage to pulmonary,                 and underestimation of the strength of association
renal and cardiac tissues.21                                     with adverse outcomes. It should be remembered
    Regarding the presence of multimorbidity, it                 that self-report of chronic diseases is widely used,
was higher among individuals who died due to                     and that such information was obtained by health
COVID-19 in Acre. In New York, United States, a                  professionals. Further studies are needed to explore
study conducted with 5,700 hospitalized individuals              the theme, using primary data sources and having a
showed that 88.0% had more than one morbidity, the               longer follow-up time. Finally, the reduced number
most prevalent were: hypertension (56.6%), obesity               of deaths resulted in wide confidence intervals,
(41.7%) and diabetes mellitus (33.8%).23 In China,               requiring caution in the analysis of the data.
a study conducted with 1,590 hospitalized people                     The long-term follow-up stands out as the strong
showed that the most prevalent morbidities were                  point of this study, with assessment of 'cure' and
hypertension and diabetes, the hazard ratio (95%CI)              'death' outcomes. In addition, the study was conducted
was 1.79 (1.16;2.77) among individuals with at least             in a state in the Northern region of Brazil, with a
one morbidity, and 2.59 (1.61;4.17) among those with             population whose laboratory diagnosis for COVID
two or more morbidities.24 According to a Brazilian              19 and notification of the disease were performed
study conducted in the pandemic period up to the                 via the e-SUS VE/SIVEP-Gripe, being followed up for
21st Epidemiological Week of 2020, diabetes was also             case closure and identification of health outcomes.
more prevalent in individuals hospitalized with SARS             The choice of the type of study and the sample size, in
due to COVID-19, compared to the general population              times of pandemic, reinforces its importance, insofar
of the country.25 The possible explanation for severe            as work subsidizes knowledge about the reality of states
conditions in people with diabetes mellitus is due to            that are far from the large urban centers in the country,
constant glucose recognition by C type lectin receptors,         enabling the identification of regional risk factors for
generating greater inflammatory response.22                      death due to COVID-19.
    In a study with 1,139 cases and 11,390 controls                  Taking these results, it can be concluded that the
conducted in Madrid, Spain, researchers observed that            study analyzed the epidemiological characteristics and
renin-angiotensin-aldosterone system inhibitors did              risk factors for death in individuals diagnosed with
not increase the risk of SARS due to severe COVID-19,            SARS due to COVID-19 in the state of Acre. Risk groups
and the discontinuity of treatment by patients was               need special attention, especially the elderly, patients
discouraged. Furthermore, continuous monitoring                  with dyspnea and those with diabetes mellitus. Some
of these individuals was recommended because the                 symptoms were more frequent in mild cases of COVID-19
presence of cardiovascular diseases can aggravate                and should be better elucidated in future studies.
pneumonia and may result in unfavorable outcomes.26
    Among the limitations of this study, it is worth             Authors’ contributions
mentioning the use of secondary data obtained from
the state epidemiological surveillance, which limited               Prado PR, Gimenes FRE, Lima MVM and Soares
information detailing, especially about the presence or          CP collaborated with the conception and design of
not of hypertension. It is suggested the inclusion of the        the manuscript, data analysis and interpretation and
following variables: 'arterial hypertension', 'anosmia/          drafting the first version of the manuscript. Prado
hyposmia/dysgeusia/ageusia', 'myalgia', 'sore throat',           VB and Amaral TLM collaborated with data analysis
'headache', 'runny nose' and 'diarrhea', in the e-SUS VE         and interpretation, and critical reviewing of the
questionnaire, in order to better support future studies.        manuscript. All authors have approved the final version
Other possible limitations of the study are (i) information      of the manuscript and have declared themselves to
quality, dependent on the complete and correct                   be responsible for all aspects of the work, including
completion of the e-SUS VE notification form, and (ii)           ensuring its accuracy and integrity.

8                                  Epidemiol. Serv. Saude, Brasília, 30(3):e2020676, 2021
Patrícia Rezende do Prado et al.

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                                                                       Received on 26/08/2020
                                                                       Approved on 09/03/2021

                                                      Associate Editor: Bruno Pereira Nunes -      orcid.org/0000-0002-4496-4122
                                                         Scientific Editor: Taís Freire Galvão -   orcid.org/0000-0003-2072-4834
                                                       Editor-in-chief: Leila Posenato Garcia -    orcid.org/0000-0003-1146-2641

10                                Epidemiol. Serv. Saude, Brasília, 30(3):e2020676, 2021
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