ORIGINAL ARTICLE http://doi.org/10.1590/S1678-9946202264069 The first year of the COVID-19 pandemic in an indigenous population in Brazil: an epidemiological study Mariana Garcia Croda 1, Marcelo dos Santos Barbosa 2, Silvana Beutinger Marchioro 3, Débora Dupas Gonçalves do Nascimento 4, Enirtes Caetano Prates Melo5, Oswaldo Gonçalves Cruz6, Alex José Leite Torres 7, Laís Albuquerque de Oliveira 8, Fabiana Ganem 9, Simone Simionatto 10 1 Universidade Federal do Mato Grosso do Sul, Escola de Medicina, Campo Grande, Mato Grosso ABSTRACT do Sul, Brazil 2 Universidade Federal da Grande Dourados, This cross-sectional observational study that describes the epidemiological data of the first Faculdade de Ciências da Saúde, Dourados, Mato year of the COVID-19 pandemic in the Mato Grosso do Sul State, aimed to demonstrate the Grosso do Sul, Brazil differences between indigenous and non-indigenous populations, characterize confirmed cases 3 Universidade Federal da Bahia, Instituto de of COVID-19 according to risk factors related to ethnicity, comorbidities and their evolution Ciências da Saúde, Laboratório de Imunologia e Biologia Molecular, Salvador, Bahia, Brazil and to verify the challenges in facing the disease in Brazil. SIVEP-Gripe and E-SUS-VE, a nationwide surveillance database in Brazil, from March 2020 to March 2021 in Mato Grosso 4 Fundação Osvaldo Cruz, Campo Grande, Mato Grosso do Sul, Brazil do Sul state, were used to compare survivors and non-survivors from indigenous and non- indigenous populations and the epidemiological incidence curves of these populations. A total of 5 Escola Nacional de Saúde Pública da Fundação Osvaldo Cruz, Rio de Janeiro, Rio de Janeiro, 176,478, including 5,299 indigenous people, were confirmed. Among the indigenous population, Brazil 52.5% (confidence interval [CI] 51.2‑53.9) were women, 38% (CI 36.7‑39.4) were 20‑39 years 6 Fundação Oswaldo Cruz, Programa de Ciências old, 56.7% were diagnosed by rapid antibody tests, 12.3% (CI 95%:11.5‑13.2) had at least one da Computação, Rio de Janeiro, Rio de Janeiro, comorbidity, and 5.3% (CI 95%:4.7–5.9) were hospitalized. In the non-indigenous patients, Brazil 56.8% were confirmed using RT-PCR, 4.4% (CI 95%:4.3‑4.5) had at least one comorbidity, and 7 Universidade Federal da Bahia, Instituto de 8.0% (CI 95%:7.9‑8.2) were hospitalized. The majority of non-survivors were ≥60 years old Ciências da Saúde, Laboratório de Imunologia e (65.1% indigenous vs. 74.1% non-indigenous). The mortality in indigenous people was more Biologia Molecular, Salvador, Bahia, Brazil than three times higher (11% vs. 2.9%). Indigenous people had a lower proportion of RT-PCR 8 Universidade Federal da Grande Dourados, diagnoses; deaths were more frequent in younger patients and were less likely to be admitted Faculdade de Ciências da Saúde, Laboratório de Pesquisas em Ciências da Saúde, Dourados, to hospital. Mass vaccination may have controlled the incidence and mortality associated with Mato Grosso do Sul, Brazil COVID-19 in this population during the period of increased viral circulation. 9 Universitat Autònoma de Barcelona, Departament de Pediatria, d’Obstetrícia I Ginecologia i de KEYWORDS: Health of indigenous peoples. Epidemiology. Coronavirus infections. Medicina Preventiva i de Salut Publica, Belaterra, COVID-19. Barcelona, Spain Universidade Federal da Grande Dourados, 10 Faculdade de Ciências Biológicas e Ambientais, Laboratório de Pesquisas em Ciências da Saúde, Dourados, Mato Grosso do Sul, Brazil INTRODUCTION Correspondence to: Simone Simionatto Universidade Federal da Grande Dourados, Indigenous populations in Brazil experience a disproportionate burden Faculdade de Ciências Biológicas e Ambientais, of disease due to geographical and socioeconomic factors and poorer social Laboratório de Pesquisas em Ciências da Saúde, Rodovia Dourados - Itahum, km 12, Cidade determinants of health than non-indigenous people1. The coronavirus disease Universitária, CEP 79804970, Dourados, MS, 2019 (COVID-19) pandemic has raised great concerns about the increased risk of Brazil mortality in indigenous people. The spread of the severe acute respiratory syndrome Tel: +55 67 3410 2339 coronavirus-2 (SARS‑CoV-2) in indigenous communities has exposed a failing Fax: +55 67 3410 2256 health system, involving challenges with access to health services, social distancing, E-mail: simonesimionatto@ufgd.edu.br effective communication, and social support2-4. Data on the conduct and effects Received: 1 June 2022 of pandemics on indigenous people are scarce. Thus, assessing the impact of this Accepted: 22 September 2022 disease on this population is urgently needed. Rev Inst Med Trop São Paulo. 2022;64:e69 This is an open-access article distributed under the Page 1 of 8 terms of the Creative Commons Attribution License. Croda et al. The Mato Grosso do Sul State, located in the south of people. It has the second largest indigenous population in the Central-West region of Brazil, is home to the second Brazil, consisting of 80,841 people. The main ethnicities largest indigenous population in the country. Bordering of this population include Guarani-Kaiowa, Terena, and Paraguay and Bolivia, with a population of approximately Guarani-Nhandeva, representing 96% of the indigenous 2.8 million inhabitants and great ethnic diversity, the population of the state11. state presents major challenges for health surveillance. We did a retrospective analysis between March 1, 2020, Indigenous villages are located close to urban areas, where and March 31, 2021, of all COVID-19 cases registered in social and commercial relations with non-indigenous the Influenza Epidemiological Surveillance Information people can expedite the spread of COVID-19 in indigenous System, SIVEP-Gripe (Sistema de Informacao de Vigilancia territories. Therefore, it is expected that the epidemiology Epidemiologica da Gripe), and E-SUS Epidemiological of the disease in indigenous and non-indigenous people Surveillance (E-SUS Vigilancia Epidemiologica - will follow similar patterns owing to their geographical E-SUS‑VE), a nationwide surveillance databases used to proximity and unrestricted contact4. monitor COVID-19 infections in Brazil. We accessed the Brazil has one of the worst responses to the COVID-19 data through the Health Department of the Mato Grosso pandemic worldwide5-7. Non-pharmaceutical interventions, do Sul State, which checks notifications daily, excludes such as testing all suspected cases, physical distancing incomplete and duplicate data, and provides anonymized measures, income support for households affected by organized data. COVID-19, and associated interventions (especially for All cases who had their ethnicity recorded in the more vulnerable populations as indigenous), have not dataset were included in this study. Cases confirmed by been widely adopted8-10. In the period up to March 2021, laboratory or clinical criteria, as defined by the Ministry the cumulative incidence rate of COVID-19 in Brazil was of Health, were selected12. This study was approved by the 6,117.2 cases per 100,000 inhabitants, and the cumulative National Research Ethics Commission and the National mortality rate was 155.9 deaths per 100,000 inhabitants. Research Ethics Commission of the affiliated institution In the same period, the incidence rate in the indigenous (Nº 4.311.712). Patients with laboratory confirmation for population was 515.9 per 100,000 inhabitants, and the SARS-CoV-2 screening (reverse transcriptase-polymerase mortality rate was 11.1 per 100,000 inhabitants. chain reaction [RT-PCR] or antigen screening) or Owing to a shortage of vaccines, the immunization immunological testing through antibody screening (before plan proposed by the Ministry of Health of Brazil consists the vaccination period) were considered confirmed cases. of four phases based on priority groups, with indigenous people living in villages included in phase one (indigenous Data collection and study variables people living in cities were not included). At this phase, two doses of the CoronaVac vaccine (Sinovac Life Sciences, COVID-19 incidence by municipality was calculated Beijing, China) have been offered to all indigenous adults as the ratio between the absolute number of cases and over 18 years of age since January 2021. the resident population in the municipality multiplied by This cross-sectional observational study that describes 100,000. Data on the resident population by municipality the epidemiological data of the first year of the COVID-19 correspond to the estimates by the Federal Accounts Court pandemic in the Mato Grosso do Sul State, aimed to (TCU) for 2020, based on census data from the Brazilian demonstrate the differences between indigenous and Institute of Geography and Statistics in 2010 13. The non‑indigenous populations, characterize confirmed indigenous population estimated by municipality was based cases of COVID-19 according to risk factors related to on the Special Secretary of Indigenous Health population ethnicity, comorbidities and their evolution and to verify data11. the challenges in facing the disease in Brazil Demographic data (ethnicity, sex, age, and city of residence), laboratory test results (RT-PCR and rapid tests), MATERIALS AND METHODS comorbidities, patient hospitalization, and clinical outcomes were evaluated. Data from indigenous and non-indigenous Study setting and population populations were evaluated separately. We performed a cross-sectional observational study Statistical analysis of COVID-19 in indigenous and non-indigenous patients from Mato Grosso do Sul State in the Central-West Region Descriptive analysis included frequency analysis (%) of Brazil, with a population of approximately 2.8 million and 95% confidence intervals for categorical variables, and Page 2 of 8 Rev Inst Med Trop São Paulo. 2022;64:e69 The first year of the COVID-19 pandemic in an indigenous population in Brazil the chi-square test was used to compare differences between The global incidence per 100,000 inhabitants was groups where appropriate. The R Statistic (version 4.0, similar between the indigenous and non-indigenous Windows, Microsoft, USA) was used for all the calculation. populations (6617 and 6543, respectively) (Figure 2A). Spatial distribution was analyzed and processed in the GIS However, in the north central regions of the state, the environment (QGIS version 3.8 Open Source, Geospatial incidence in some cities was up to seven times higher Foundation Project), with meshes and vector points that among indigenous people, such as Anastacio (18,290 vs. considered municipalities with confirmed cases and 4,884), Aquidauana (17,085 vs. 5,731), Dois Irmao do incidence higher than 5,000 cases per 100,000 inhabitants Buriti (23,261 vs. 3,322), and Sidrolandia (25,897 vs. in the indigenous population. The epidemic curve of 5,832) (Figure 2). COVID-19 cases was obtained based on the absolute daily variation of the new cases, 7-day moving average, and Profile of COVID-19 cases cumulative cases during the period. The digital mesh of the 79 municipalities was obtained from the Brazilian Institute In the indigenous population, 52.5% (CI 95%:51.2‑53.9) of Geography and Statistics14. of COVID-19-confirmed cases were women, and 38% (CI 95%:36.7‑39.4) were aged between 20 and 39 years, RESULTS with an average age of 32 years. Regarding diagnostic tests, 56.7% of indigenous individuals were confirmed During the study period, 671,616 records were by rapid antibody tests, whereas in non-indigenous registered in the SIVEP-Gripe and e-SUS-VE datasets. individuals, 56.8% were confirmed by RT-PCR. Among Of these, 198,109 were COVID-19-confirmed cases and indigenous people, 12.3% (CI 95%:11.5‑13.2) had at least 176,478 had their ethnicity recorded, including 5,299 one comorbidity, whereas 4.4% (CI 95%:4.3‑4.5) of non- indigenous people (Figure 1). indigenous people had at least one comorbidity. In the Figure 1 - Flowchart of SIVEP-GRIPE/ e-SUS-VE data used in this study. SIVEP Gripe = Sistema de Informacao de Vigilancia Epidemiologica da Gripe; e-SUS-VE = E-SUS Vigilancia Epidemiologica. Rev Inst Med Trop São Paulo. 2022;64:e69 Page 3 of 8 Croda et al. Figure 2 - Distribution of COVID-19 cases: A) Proportional spatial distribution of incidence due to COVID-19 in the indigenous and non-indigenous populations; B) Distribution of the incidence of COVID-19-confirmed cases in the indigenous population by municipality. indigenous population, 5.3% (CI 95%:4.7‑5.9) of the cases 2% (CI 95%:1.7‑2.5) and 2.2% (CI 95%:2.1‑2.3) in the were hospitalized, while it was 8.0% (CI 95%:7.9‑8.2) in indigenous and non-indigenous populations, respectively the non-indigenous population. The case fatality rates were (Table 1). Table 1 - Demographics, baseline characteristics, and clinical outcomes of the indigenous and non-indigenous patients with COVID-19 March 2020 to March 2021 in Mato Grosso do Sul State. Indigenous Non-Indigenous % CI % CI (N=5.299) (N=171.179) Sex Male 2.515 47.5 46.1 – 48.8 79.587 46.5 46.3 – 46.3 Female 2.784 52.5 51.2 – 53.9 91.592 53.5 53.3 – 53.7 Age 0–19 1.328 25.1 23.1 – 26.3 17.198 10.0 9.9 – 10.2 20–39 2.015 38.0 36.7 – 39.4 74.052 43.3 43.0 – 43.5 40–59 1.312 24.8 23.6 – 25.9 56.676 33.1 32.9 – 33.3 >=60 644 12.2 11.3 – 13.1 23.253 13.6 13.4 – 13.7 Laboratorial testing IgM/IgG rapid tests 3.003 56.7 55.3 – 58.0 68.399 40.0 39.7 – 40.2 RT-PCR 2.272 42.9 41.5 – 44.2 97.226 56.8 56.6 – 57.1 Not informed 24 0.5 0.3 – 0.7 5.534 3.2 3.2 - 3.3 Comorbidities Only one 653 12.3 11.5 – 13.2 7.502 4.4 4.3 – 4.5 Two 132 2.5 2.1 – 3.0 1.855 1.1 1.0 – 1.2 More than two 65 1.2 1.0 – 1.6 1.098 0.64 0.60 – 0.68 Not informed 4.447 84 83.0 – 85.0 160.676 93.9 93.7 – 94.0 Hospital admission 281 5.3 4.7 – 5.9 13.786 8.0 7.9 – 8.2 Died 109 2.0 1.7– 2.5 3.752 2.2 2.1 -2.3 RT-PCR = reverse-transcriptase polymerase chain reaction. Page 4 of 8 Rev Inst Med Trop São Paulo. 2022;64:e69 The first year of the COVID-19 pandemic in an indigenous population in Brazil Profile of non-survivors for COVID-19 incidence in indigenous people occurred from July to September 2020, with no further increase in incidence Regarding indigenous non-survivors, 56.9% of the during that period. The acceleration (highest period) of the deaths occurred among men, 65.1% were ≥60 years old, curve in non-indigenous people was from November 2020 and 14.7% had at least one comorbidity. Furthermore, to March 2021, and was not accompanied by any increase indigenous people had a higher prevalence of diabetes in the incidence, making it relatively stable (Figure 3). mellitus (31.8% vs. 24.6%) and chronic kidney disease (6.8% vs. 3.5%). In the non-indigenous population, DISCUSSION 54.1% were men, 74.1% were aged ≥60 years, and 30% had at least one comorbidity (Table 2). The most The COVID-19 pandemic has highlighted social prevalent comorbidities were cardiovascular diseases vulnerability and inadequate healthcare services in (29.4%), diabetes mellitus (24.1%), and obesity (8%). Brazilian indigenous communities, with high incidence Non-indigenous people had a higher prevalence of and mortality rates in these populations, and we evaluated cardiovascular disease (24.6% vs. 18.5%) and obesity (8% these vulnerabilities within the second largest indigenous vs. 6.5%). The number of deaths in a non-hospital setting population in Brazil. Our data demonstrated the evolution of was more than three times higher among indigenous the COVID-19 pandemic in its first year among ethnically people (11% vs. 2.9%) (Table 2), with the most prevalent distinct populations in Mato Grosso do Sul State, Brazil, comorbidities being cardiovascular disease (29.4%), which is home to the second largest indigenous population diabetes mellitus (24.1%), and obesity (8%). Indigenous in the country. Although the global incidence of the disease individuals had a higher proportion of diabetes mellitus per 100,000 inhabitants was similar, we found significant (31.8% vs. 24.6%) and chronic kidney disease (6.8% vs. regional variations in the incidence and epidemiological 3.5%). Cardiovascular disease (24.6% vs. 18.5%) and curves between the indigenous and non-indigenous obesity (8% vs. 6.5%) were more prevalent among non- populations. indigenous populations. Our data showed a heterogeneous distribution of incidence and mortality among indigenous people in the Cumulative cases state. We hypothesized that the healthcare characteristics differ for each region. Furthermore, there may be differences The curves for indigenous and non-indigenous in the characteristics of indigenous populations in the populations exhibited heterogeneous behavior. The highest northern and southern regions. Indigenous people have more Table 2 - Characteristics of the COVID-19-confirmed 2019 cases reported in the SIVEP-Gripe database who died by March 2020 to March 2021 in Mato Grosso do Sul State. Indigenous Non-Indigenous % CI % CI (N=109) (N=3,752) Sex Male 62 56.9 47.5 – 65.8 2.030 54.1 52.51 - 55.69 Female 47 43.1 34.2 – 52.6 1.722 45.9 44.31 – 47.49 Age 0-19 0 0 5 0.2 0.10 – 0.31 20-39 9 8.3 4.4 – 14.9 140 3.7 3.17 – 4.39 40-59 29 26.6 19.2 – 35.6 826 22.0 20.72 – 23.37 >=60 71 65.1 55.8 – 73.4 2.781 74.1 72.69 – 75.50 Comorbidities Only one 16 14.7 9.2 – 22.5 1.127 30.0 28.6 – 31.5 Two 1 0.9 0.2 – 5.0 350 9.3 8.4 – 10.3 More than two 1 0.9 0.2 – 5.0 211 5.7 4.9 – 6.4 Not informed 91 83.5 75.4 – 89.3 2.064 55.0 53.4 – 56.6 Hospital admission Yes 96 88.1 80.7 – 92.90 3.621 96.5 95.87 – 97.05 No 12 11.0 6.4 – 18.3 107 2.9 2.37 – 3.43 Not informed 1 0.9 0.16 – 5.0 19 0.6 0.32 – 0.79 SIVEP Gripe = Sistema de Informacao de Vigilancia Epidemiologica da Gripe. Rev Inst Med Trop São Paulo. 2022;64:e69 Page 5 of 8 Croda et al. Figure 3 - Total number of daily recordings of confirmed new COVID-19 cases for one-year, cumulative cases, and moving average of 7 days in the non-indigenous (A), and indigenous (B) population from the Mato Grosso do Sul State. individuals under 15 years old and fewer elderly individuals died from the disease in both populations studied. The than the overall population11. This may partially explain case fatality rate of COVID-19 was 2.05 and 2.19 per why a greater number of younger indigenous patients 100,000 people for the indigenous and non-indigenous tested positive. populations, respectively. Previous data have shown the The pandemic may disproportionately affect people worst disease lethality in indigenous people3,25,26, though from minority ethnic communities including indigenous this may have changed due to the decrease in the number populations15-17. Indigenous people had more missing data of cases and deaths after vaccination. In addition, our regarding comorbidities and hospitalizations. Therefore, assessment covered indigenous peoples from remote and improving the quality and completeness of the data across urban areas, failing to differentiate indicators related to health and administrative datasets is essential for building spatial localization. a complete picture of ethnic disparities. Brazilian states, including Mato Grosso do Sul, saw In our study, the indigenous cases had a lower a further significant increase in cases of COVID-19 as of proportion of diagnostic tests by RT-PCR, and the non- December 2020, which was termed the “second wave.” The survivors were less likely to be admitted to a hospital new Brazilian SARS-CoV-2 variant, “Gamma,” has quickly compared to the non-indigenous population. We also become predominant in the country and was thought to identified three times more deaths in a non-hospital be a large factor behind a massive second wave that has setting among indigenous people (11% vs. 2.9%). These brought the country’s death toll to the second highest in the disparities may also be reflected in other determinants, world27. It was hypothesized that the SARS-CoV-2 variants such as access to healthcare. Socioeconomic determinants circulating in the second wave might have higher inherent are directly related to access to COVID-19 tests, which transmissibility than the pre-existing variants28,29. may explain the difference in testing between indigenous Surprisingly, in our analyses, the indigenous population and non-indigenous people18,19. did not experience a significant increase in the number The Brazilian COVID-19 epidemic highlights the non- of cases and deaths when the non-indigenous population equitable access to COVID-19 diagnostics as a factor that experienced the worst point of the pandemic. We potentially contributes to the sustained spread of the virus. hypothesized that mass vaccination of indigenous adults The lack of investment in RT-PCR, geographical barriers, protected the population in time to face the second wave, and ease of access using point-of-care tests can justify the given that no new non-pharmacological measures were use of rapid antibody tests, even though the gold standard implemented during that period. for diagnosing COVID-19 is RT-PCR18. Although antibody- In terms of vaccination rate, 70% of indigenous people based tests are appropriate for surveillance studies, they received the first dose, and almost 53% had received the cannot be used to identify acute cases (transmitters)20. second dose (4 weeks between doses), as of March 2021. Some studies have shown that COVID-19-associated A recent study has shown that the CoronaVac vaccine is hospitalization rates have been higher among men than effective against the gamma variant30. Our study reinforces among women21,22, with the former having higher mortality that the number of new infections can be controlled in a rates23,24. Similar to our findings, although the number of population with a vaccine coverage rate, even in a scenario women diagnosed with COVID-19 was higher, more men of high circulation of a new variant of concern, gamma. Page 6 of 8 Rev Inst Med Trop São Paulo. 2022;64:e69 The first year of the COVID-19 pandemic in an indigenous population in Brazil CONCLUSION 3. Cupertino GA, Cupertino MC, Gomes AP, Braga LM, Siqueira- Batista R. COVID-19 and Brazilian indigenous populations. Despite the limitations intrinsic to the descriptive studies Am J Trop Med Hyg. 2020;103:609-12. of secondary data, which may not reflect the reality in its 4. Simionatto S, Barbosa M, Marchioro SB. COVID-19 in Brazilian entirety, we believe that this work fulfilled its purpose of indigenous people: a new threat to old problems. Rev Soc Bras generating hypotheses that should be confirmed with other Med Trop. 2020;53:e20200476. methodological designs. In addition, the data included all 5. Ferigato S, Fernandez M, Amorim M, Ambrogi I, Fernandes LM, patients who declared themselves to be indigenous, and not Pacheco R. The Brazilian government’s mistakes in responding just those who resided in indigenous territories. to the COVID-19 pandemic. Lancet. 2020;396:1636. Regarding clinical data, comorbidities in cases of SARS- 6. Santos VS, Souza Araújo AA, Oliveira JR, Quintans-Júnior LJ, CoV-2 do not specify the type or degree of disease, as in Martins-Filho PR. COVID-19 mortality among indigenous cases of cardiovascular disease or kidney disease. In addition, people in Brazil: a nationwide register-based study. J Public we highlighted the disparities between ethnic minorities in Health (Oxf.). 2021;43:e250-1 their access to healthcare and the heterogeneous distribution 7. Ventura D, Aith F, Reis R. The catastrophic Brazilian response between different municipalities. The indigenous population to covid-19 may amount to a crime against humanity. had a lower average age and fewer comorbidities, but a similar Thebmjopinion. Weblog. [cited 2022 Sep 22]. Available mortality rate as the non-indigenous population. The possible from: https://blogs.bmj.com/bmj/2021/04/05/the-catastrophic- protective effect of the vaccine maintained a stable incidence brazilian-response-to-covid-19-may-amount-to-a-crime- rate during the worst moments of the pandemic in the state. against-humanity/ The control of the disease in a region with ethnic 8. Boschiero MN, Palamim CV, Ortega MM, Mauch RM, Marson diversity and different access to healthcare services, FA. One year of coronavirus disease 2019 (COVID-19) in with areas bordering two countries with different coping Brazil: a political and social overview. Ann Glob Health. strategies, as well as the lack of coordination of the 2021;87:44. federal government for COVID-19 control, demonstrates 9. Candido DS, Claro IM, De Jesus JG, Souza WM, Moreira FR, the challenges that Brazilian states face. Our findings Dellicour S, et al. Evolution and epidemic spread of SARS- can be extrapolated to other regions and help to improve CoV-2 in Brazil. Science. 2020;369:1255-60. institutional health policies. 10. Ortega F, Orsini M. Governing COVID-19 without government in Brazil: ignorance, neoliberal authoritarianism, and the collapse CONFLICT OF INTERESTS of public health leadership. Glob Public Health. 2020;15:1257- 77. The authors declare no conflict of interests. 11. Brasil. Ministério da Saúde. Secretaria Especial de Saúde Indígena. Distrito Sanitário Especial Indígena do Mato Grosso FUNDING do Sul. Plano de contingência COVID-19/DSEI-MS. Campo Grande: Ministério da Saúde; 2020. [cited 2022 Sep 22]. This work was funded by Conselho Nacional de Available from: http://ds.saudeindigena.icict.fiocruz.br/handle/ Desenvolvimento Cientifico e Tecnologico (CNPq grant bvs/1820 Nº 401727/2020-3), Secretaria do Estado de Saude do 12. Brasil. Ministério da Saúde. Guia de vigilância epidemiológica: Mato Grosso do Sul and Universidade Federal da Grande emergência de saúde pública de importância nacional pela Dourados. LAO and SS received a research grant from doença pelo coronavírus 2019: COVID-19. Brasília: Ministério CNPq. Sponsors didn’t take part in data collection, analysis da Saúde; 2021. [cited 2022 Sep 22]. Available from: https:// and interpretation nor in manuscript writing. www.gov.br/saude/pt-br/centrais-de-conteudo/publicacoes/ guias-e-manuais/2021/guia-de-vigilancia-epidemiologica- REFERENCES covid-19-3.pdf/view 13. Instituto Brasileiro de Geografia e Estatística. Brasil: Mato Grosso 1. Santos AP, Mazzeti CM, Franco MC, Santos NL, Conde WL, do Sul: panorama. [cited 2022 Sep 22]. Available from: https:// Leite MS, et al. Estado nutricional e condições ambientais e cidades.ibge.gov.br/brasil/ms/panorama de saúde de crianças Pataxó, Minas Gerais, Brasil. Cad Saude 14. Instituto Brasileiro de Geografia e Estatística. Mapas. [cited 2022 Publica. 2018;34:e00165817. Sep 22]. Available from: https://portaldemapas.ibge.gov.br/ 2. Santos RV, Pontes AL, Coimbra Jr CE. A “total social fact”: portal.php#homepage COVID-19 and indigenous peoples in Brazil. Cad Saude 15. Baqui P, Bica I, Marra V, Ercole A, van Der Schaar M. Ethnic Publica. 2020;36:e00268220. and regional variations in hospital mortality from COVID-19 Rev Inst Med Trop São Paulo. 2022;64:e69 Page 7 of 8 Croda et al. in Brazil: a cross-sectional observational study. Lancet Glob 22. Garg S, Kim L, Whitaker M, O’Halloran A, Cummings C, Holstein Health. 2020;8:e1018-26. R, et al. Hospitalization rates and characteristics of patients 16. Mathur R, Rentsch CT, Morton CE, Hulme WJ, Schultze A, hospitalized with laboratory-confirmed Coronavirus Disease MacKenna B, et al. Ethnic differences in SARS-CoV-2 2019 - COVID-NET, 14 States, March 1-30, 2020. MMWR infection and COVID-19-related hospitalisation, intensive care Morb Mortal Wkly Rep. 2020;69:458-64. unit admission, and death in 17 million adults in England: an 23. Du Y, Tu L, Zhu P, Mu M, Wang R, Yang P, et al. Clinical observational cohort study using the OpenSAFELY platform. features of 85 fatal cases of COVID-19 from Wuhan: a Lancet. 2021;397:1711-24. retrospective observational study. Am J Respir Crit Care Med. 17. Polidoro M, Mendonça FA, Meneghel SN, Alves-Brito A, 2020;201:1372-9. Gonçalves M, Bairros F, et al. Territories under siege: risks of 24. Chen T, Wu D, Chen H, Yan W, Yang D, Chen G, et al. Clinical the decimation of indigenous and Quilombolas peoples in the characteristics of 113 deceased patients with coronavirus context of COVID-19 in South Brazil. J Racial Ethn Health disease 2019: retrospective study. BMJ. 2020;368:m1091. Disparities. 2021;8:1119-29. 25. Fellows M, Paye V, Alencar A, Nicácio M, Castro I, Coelho ME, 18. Wiersinga WJ, Rhodes A, Cheng AC, Peacock SJ, Prescott HC. et al. Under-reporting of COVID-19 cases among indigenous Pathophysiology, transmission, diagnosis, and treatment of peoples in Brazil: a new expression of old inequalities. Front coronavirus disease 2019 (COVID-19): a review. JAMA. Psychiatry. 2021;12:638359. 2020;324:782-93. 26. Jardim TD, Dias IM, Grande AJ, O’Keeffe M, Dazzan P, Harding 19. Cobre AF, Böger B, Fachi MM, Vilhena RO, Domingos EL, Tonin S. COVID-19 experience among Brasil’s indigenous people. FS, et al. Risk factors associated with delay in diagnosis and Rev Assoc Med Bras. 2020;66:861-3. mortality in patients with COVID-19 in the city of Rio de 27. World Health Organization. Coronavirus (COVID-19) dashboard. Janeiro, Brazil. Cien Saude Colet. 2020;25 Suppl 2:4131-40. [cited 2022 Sep 22]. Available from: https://covid19.who.int 20. Kameda K, Barbeitas MM, Caetano R, Löwy I, Oliveira AC, 28. Sabino EC, Buss LF, Carvalho MP, Prete Jr. CA, Crispim MA, Corrêa MC, et al. Testing COVID-19 in Brazil: fragmented Fraiji NA, et al. Resurgence of COVID-19 in Manaus, Brazil, efforts and challenges to expand diagnostic capacity at the despite high seroprevalence. Lancet. 2021;397:452-5. Brazilian Unified National Health System. Cad Saude Publica. 29. Faria NR, Mellan TA, Whittaker C, Claro IM, Candido DS, Mishra 2021;37:e00277420. S, et al. Genomics and epidemiology of the P.1 SARS-CoV-2 21. Petrilli CM, Jones SA, Yang J, Rajagopalan H, O’Donnell L, lineage in Manaus, Brazil. Science. 2021;372:815-21. Chernyak Y, et al. Factors associated with hospital admission 30. Hitchings MD, Ranzani OT, Torres MS, Oliveira SB, Almiron M, and critical illness among 5279 people with coronavirus Said R, et al. Effectiveness of CoronaVac among healthcare disease 2019 in New York City: prospective cohort study. BMJ. workers in the setting of high SARS-CoV-2 Gamma variant 2020;369:m1966. transmission in Manaus, Brazil: a test-negative case-control study. Lancet Reg Health Am. 2021;1:100025. Page 8 of 8 Rev Inst Med Trop São Paulo. 2022;64:e69