Healthcare delivery, economics and global health ORIGINAL RESEARCH Heart: first published as 10.1136/heartjnl-2020-317663 on 15 October 2020. Downloaded from Excess of cardiovascular deaths during the COVID-19 pandemic in Brazilian capital cities Luisa Campos Caldeira Brant ,1,2 Bruno Ramos Nascimento ,1,2 Renato Azeredo Teixeira,3 Marcelo Antônio Cartaxo Queiroga Lopes,4,5 Deborah Carvalho Malta,6 Glaucia Maria Moraes Oliveira,7 Antonio Luiz Pinho Ribeiro 1,2 1Serviço de Cardiologia e ABSTRACT New York City.2 Of note, excess of all-cause deaths Cirurgia Cardiovascular, Hospital Introduction During the COVID-19 pandemic, excess in this period may have occurred due to identified das Clínicas da Universidade Federal de Minas Gerais, Belo mortality has been reported, while hospitalisations or non- identified COVID-19 or other causes, being Horizonte, Brazil for acute cardiovascular events reduced. Brazil is the an objective and comparable metric for evaluating 2Departamento de Clínica second country with more deaths due to COVID-19. We the true impact of the pandemic in the mortality of Médica, Universidade Federal de aimed to evaluate excess cardiovascular mortality during a location.3 Minas Gerais, Belo Horizonte, COVID-19 pandemic in 6 Brazilian capital cities. Concomitantly, there has been a decrease in Minas Gerais, Brazil 3Pós- graduação em Saúde Methods Using the Civil Registry public database, hospital admissions associated with acute cardio- Pública, Universidade Federal de we evaluated total and cardiovascular excess deaths, vascular diseases, markedly acute coronary Minas Gerais, Belo Horizonte, further stratified in specified cardiovascular deaths syndromes (ACS), in high- income countries (HIC). Minas Gerais, Brazil (acute coronary syndromes and stroke) and unspecified In Northern Italy, a significant decrease in hospital 4Sociedade Brasileira de cardiovascular deaths in the 6 Brazilian cities with daily admissions due to ACS during the pandemic Cardiologia, Rio de Janeiro, Rio 4 de Janeiro, Brazil greater number of COVID-19 deaths (São Paulo, Rio de was reported. In parallel, a 58% increase in out- 5Cardiologia Intervencionista, Janeiro, Fortaleza, Recife, Belém, Manaus). We compared of- hospital cardiac arrest, strongly associated Hospital Alberto Urquiza observed with expected deaths from epidemiological with cumulative COVID-19 incidence, was also Wanderley, João Pessoa, weeks 12–22 of 2020. We also compared the number of observed.5 In the USA, an estimated 38% reduc- Paraíba, Brazil 6Escola de Enfermagem, hospital and home deaths during the period. tion in cardiac catheterisation laboratories activa- Universidade Federal de Minas Results There were 65 449 deaths and 17 877 tions due to ST- elevation myocardial infarction was Gerais, Belo Horizonte, Minas COVID-19 deaths in the studied period and cities described,6 similar to the 40% reduction in Spain.7 Gerais, Brazil for 2020. Cardiovascular mortality increased in most This behaviour may be associated with avoidance of 7Faculdade de Medicina e Instituto do Coração Edson cities, with greater magnitude in the Northern capitals. medical care due to social distancing and concerns Saad, Universidade Federal do However, while there was a reduction in specified of contracting COVID-19, and misdiagnosis. More- http://heart.bmj.com/ Rio de Janeiro, Rio de Janeiro, cardiovascular deaths in the most cities, the Northern over, in regions where healthcare resources became Brazil capitals showed an increase of these events. For scarce during the pandemic, excess deaths may have unspecified cardiovascular deaths, there was a marked occurred due to healthcare collapse, reinforcing Correspondence to increase in all cities, which strongly correlated to the rise social disparities in the death tolls. Professor Antonio Luiz Pinho Ribeiro, Internal Medicine, in home deaths (r=0.86, p=0.01). The pandemic has been delayed in low-income Universidade Federal de Minas Conclusion Excess cardiovascular mortality was greater and middle- income countries (LMICs), and how Gerais, Belo Horizonte, Minas in the less developed cities, possibly associated with cardiovascular diseases will behave in LMIC is a on October 1, 2021 by guest. Protected copyright. Gerais, Brazil; healthcare collapse. Specified cardiovascular deaths matter of debate. Brazil, a middle-income country, tom1963br@ yahoo. com. br decreased in the most developed cities, in parallel is ranked second in the number of deaths due to 1 GMMO and ALPR contributed with an increase in unspecified cardiovascular and COVID-19. However, deaths are heterogeneously equally. home deaths, presumably as a result of misdiagnosis. distributed across the country and numbers are Conversely, specified cardiovascular deaths increased in underestimated due to the low rate of COVID-19 Received 26 June 2020 cities with a healthcare collapse. diagnostic tests performed.1 Using data from the Revised 14 September 2020 Accepted 18 September 2020 civil registry database, we aimed to evaluate excess cardiovascular mortality during the COVID-19 pandemic in six Brazilian capital cities from 15 INTRODUCTION March to 22 May 2020. The COVID-19 pandemic was decreed by WHO on © Author(s) (or their 11 March 2020. Since the first case was notified employer(s)) 2020. No in Brazil in 26 February, the epidemic has evolved METHODS commercial re- use. See rights and permissions. Published rapidly, and in 23 June, >1 136 470 cases have been Data sources 1 by BMJ. reported in the country, with almost 51 271 deaths. Data analytic methods and study materials will be Beyond deaths due to confirmed COVID-19, made available to other researchers for purposes To cite: Brant LCC, previous reports have also emphasised an increase of reproducing the results or replicating the proce- Nascimento BR, Teixeira RA, et al. Heart Epub ahead of in the number of total deaths during the pandemic dure, from the corresponding author on reasonable print: [please include Day compared with the same period of previous years: request. Month Year]. doi:10.1136/ the excess mortality. From March to May 2020, the We conducted an observational retrospective heartjnl-2020-317663 excess of deaths in Italy was 49%, reaching 277% in study using the Civil Registry public database Brant LCC, et al. Heart 2020;0:1–8. doi:10.1136/heartjnl-2020-317663 1 Healthcare delivery, economics and global health Table 1 Sociodemographic characteristics and total deaths in six selected Brazilian capital cities during epidemiological weeks 12–22, in 2019 and Heart: first published as 10.1136/heartjnl-2020-317663 on 15 October 2020. Downloaded from 2020 Capital São Paulo Rio de Janeiro Fortaleza Recife Belém Manaus Region Southeast Southeast Northeast Northeast North North Population, 2019 12 097 289 6 587 583 2 639 652 1 604 920 1 370 685 2 180 647 Population, 2020 12 142 621 6 592 228 2 651 800 1 607 059 1 359 971 2 216 197 HDI 0.805 0.799 0.754 0.772 0.746 0.737 ICU beds per 100 000 28.6 38.5 21.9 60.3 30.2 13.3 Physicians per 100 000 353 329 251 407 234 167 Nurses per 100 000 192 192 171 268 114 117 Total deaths, 2019 18 046 13 055 4239 3165 2077 2334 Total deaths rates, 2019 149 198 161 197 152 107 Total deaths, 2020 23 738 18 115 7992 5440 4657 5507 Total deaths rates, 2020 195 275 301 339 342 248 Excess deaths 5624 5051 3733 2271 2596 3135 Excess deaths (%) 31.1 (28.5 to 33.6) 38.7 (35.6 to 41.8) 87.7 (80.8 to 94.8) 71.7 (64.3 to 79.3) 126 (114.6 to 138) 132.2 (121.2 to 143.7) COVID-19 deaths 5343 5277 3623 1119 1399 1116 Excess deaths—COVID-19 deaths 281 −226 110 1152 1197 2019 Excess deaths—COVID-19 deaths (%) 1.6 (−0.5 to 3.6) −1.7 (-4.1 to 0.7) 2.6 (−1.7 to 7) 36.3 (30.2 to 42.7) 58.1 (49.6 to 67) 85.1 (76 to 94.6) HDI, human development index; ICU, intensive care unit.; (Transparency Portal)8 from ARPEN- Brasil for mortality data. and city declared in the DC) and c) place of death (hospital or ARPEN (Associação dos Registradores de Pessoas Naturais, home). SARS was the second condition, because SARS is usually National Association of Natural Persons Registrars) represents reported in DC when COVID-19 was not confirmed by testing. the class of Civil Registry Officers in the country, and performs The Transparency Portal8 is frequently updated by the Civil the certifications of civil life of all Brazilian citizens, including Registry Offices following legal deadlines: the family has 24 death certificates (DC). We used registers from the six Brazilian hours to register the death in the notary, which has 5 days to capitals with more COVID-19 deaths: São Paulo, Rio de Janeiro, perform the official registration, and 10 days to send the act to Fortaleza, Recife, Belém and Manaus, from the epidemiological week of the first documented death due to COVID-19 in Brazil (17 March) to 22 May 2020 (12–22 epidemiological weeks), and Table 2 Hierarchical data mining procedure to assess natural causes compared observed with expected deaths. of death in the death certificate to define one cause per death, and Data were not compared with the Brazilian Mortality Infor- other related conditions http://heart.bmj.com/ mation System (SIM), which is officially used by the govern- Condition Hierarchical definition ment, because it is only publicly available in the following year. 1 Mention of COVID-19, coronavirus: considered as ‘COVID-19’ (suspected Table 1 shows the region of Brazil, population, health or confirmed). resources and human development index (HDI) for the six 1.1 Mention of ACS/infarction, associated with COVID-19, coronavirus: capital cities. The HDI for each city was extracted from Atlas considered as ‘ACS with COVID-19’. de Desenvolvimento Humano no Brasil (Atlas of Human Devel- 1.2 Mention of stroke (ischaemic or haemorrhagic), associated with opment in Brazil),9 being a summary measure of socioeconomic COVID-19: considered as ‘stroke with COVID-19’.