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      Ethnic and regional variations in hospital mortality from COVID-19 in Brazil: a cross-sectional observational study

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          Summary

          Background

          Brazil ranks second worldwide in total number of COVID-19 cases and deaths. Understanding the possible socioeconomic and ethnic health inequities is particularly important given the diverse population and fragile political and economic situation. We aimed to characterise the COVID-19 pandemic in Brazil and assess variations in mortality according to region, ethnicity, comorbidities, and symptoms.

          Methods

          We conducted a cross-sectional observational study of COVID-19 hospital mortality using data from the SIVEP-Gripe ( Sistema de Informação de Vigilância Epidemiológica da Gripe) dataset to characterise the COVID-19 pandemic in Brazil. In the study, we included hospitalised patients who had a positive RT-PCR test for severe acute respiratory syndrome coronavirus 2 and who had ethnicity information in the dataset. Ethnicity of participants was classified according to the five categories used by the Brazilian Institute of Geography and Statistics: Branco (White), Preto (Black), Amarelo (East Asian), Indígeno (Indigenous), or Pardo (mixed ethnicity). We assessed regional variations in patients with COVID-19 admitted to hospital by state and by two socioeconomically grouped regions (north and central-south). We used mixed-effects Cox regression survival analysis to estimate the effects of ethnicity and comorbidity at an individual level in the context of regional variation.

          Findings

          Of 99 557 patients in the SIVEP-Gripe dataset, we included 11 321 patients in our study. 9278 (82·0%) of these patients were from the central-south region, and 2043 (18·0%) were from the north region. Compared with White Brazilians, Pardo and Black Brazilians with COVID-19 who were admitted to hospital had significantly higher risk of mortality (hazard ratio [HR] 1·45, 95% CI 1·33–1·58 for Pardo Brazilians; 1·32, 1·15–1·52 for Black Brazilians). Pardo ethnicity was the second most important risk factor (after age) for death. Comorbidities were more common in Brazilians admitted to hospital in the north region than in the central-south, with similar proportions between the various ethnic groups. States in the north had higher HRs compared with those of the central-south, except for Rio de Janeiro, which had a much higher HR than that of the other central-south states.

          Interpretation

          We found evidence of two distinct but associated effects: increased mortality in the north region (regional effect) and in the Pardo and Black populations (ethnicity effect). We speculate that the regional effect is driven by increasing comorbidity burden in regions with lower levels of socioeconomic development. The ethnicity effect might be related to differences in susceptibility to COVID-19 and access to health care (including intensive care) across ethnicities. Our analysis supports an urgent effort on the part of Brazilian authorities to consider how the national response to COVID-19 can better protect Pardo and Black Brazilians, as well as the population of poorer states, from their higher risk of dying of COVID-19.

          Funding

          None.

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          COVID-19: the gendered impacts of the outbreak

          Policies and public health efforts have not addressed the gendered impacts of disease outbreaks. 1 The response to coronavirus disease 2019 (COVID-19) appears no different. We are not aware of any gender analysis of the outbreak by global health institutions or governments in affected countries or in preparedness phases. Recognising the extent to which disease outbreaks affect women and men differently is a fundamental step to understanding the primary and secondary effects of a health emergency on different individuals and communities, and for creating effective, equitable policies and interventions. Although sex-disaggregated data for COVID-19 show equal numbers of cases between men and women so far, there seem to be sex differences in mortality and vulnerability to the disease. 2 Emerging evidence suggests that more men than women are dying, potentially due to sex-based immunological 3 or gendered differences, such as patterns and prevalence of smoking. 4 However, current sex-disaggregated data are incomplete, cautioning against early assumptions. Simultaneously, data from the State Council Information Office in China suggest that more than 90% of health-care workers in Hubei province are women, emphasising the gendered nature of the health workforce and the risk that predominantly female health workers incur. 5 The closure of schools to control COVID-19 transmission in China, Hong Kong, Italy, South Korea, and beyond might have a differential effect on women, who provide most of the informal care within families, with the consequence of limiting their work and economic opportunities. Travel restrictions cause financial challenges and uncertainty for mostly female foreign domestic workers, many of whom travel in southeast Asia between the Philippines, Indonesia, Hong Kong, and Singapore. 6 Consideration is further needed of the gendered implications of quarantine, such as whether women and men's different physical, cultural, security, and sanitary needs are recognised. Experience from past outbreaks shows the importance of incorporating a gender analysis into preparedness and response efforts to improve the effectiveness of health interventions and promote gender and health equity goals. During the 2014–16 west African outbreak of Ebola virus disease, gendered norms meant that women were more likely to be infected by the virus, given their predominant roles as caregivers within families and as front-line health-care workers. 7 Women were less likely than men to have power in decision making around the outbreak, and their needs were largely unmet. 8 For example, resources for reproductive and sexual health were diverted to the emergency response, contributing to a rise in maternal mortality in a region with one of the highest rates in the world. 9 During the Zika virus outbreak, differences in power between men and women meant that women did not have autonomy over their sexual and reproductive lives, 10 which was compounded by their inadequate access to health care and insufficient financial resources to travel to hospitals for check-ups for their children, despite women doing most of the community vector control activities. 11 Given their front-line interaction with communities, it is concerning that women have not been fully incorporated into global health security surveillance, detection, and prevention mechanisms. Women's socially prescribed care roles typically place them in a prime position to identify trends at the local level that might signal the start of an outbreak and thus improve global health security. Although women should not be further burdened, particularly considering much of their labour during health crises goes underpaid or unpaid, incorporating women's voices and knowledge could be empowering and improve outbreak preparedness and response. Despite the WHO Executive Board recognising the need to include women in decision making for outbreak preparedness and response, 12 there is inadequate women's representation in national and global COVID-19 policy spaces, such as in the White House Coronavirus Task Force. 13 © 2020 Miguel Medina/Contributor/Getty Images 2020 Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active. If the response to disease outbreaks such as COVID-19 is to be effective and not reproduce or perpetuate gender and health inequities, it is important that gender norms, roles, and relations that influence women's and men's differential vulnerability to infection, exposure to pathogens, and treatment received, as well as how these may differ among different groups of women and men, are considered and addressed. We call on governments and global health institutions to consider the sex and gender effects of the COVID-19 outbreak, both direct and indirect, and conduct an analysis of the gendered impacts of the multiple outbreaks, incorporating the voices of women on the front line of the response to COVID-19 and of those most affected by the disease within preparedness and response policies or practices going forward.
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            The Epidemiological Characteristics of an Outbreak of 2019 Novel Coronavirus Diseases (COVID-19) — China, 2020

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              Evidence mounts on the disproportionate effect of COVID-19 on ethnic minorities

              Tony Kirby (2020)
              As the cases of coronavirus disease 2019 (COVID-19) continue to increase across the world, evidence is continuing to emerge that the pandemic could be disproportionately affecting people from black, Asian, and minority ethnic (BAME) communities. In the UK, this trend first came to public attention during media reports that showed the first 11 doctors who sadly lost their lives to COVID-19, were all from BAME communities. Following this, various analyses have been published, with one showing that of 106 COVID-19 fatalities in health workers some two thirds (63%) were in BAME people (up to April 22, 2020). The figure was 94% for doctors and 71% for nurses, with the average reduced with the inclusion of other health-care workers (55%). The UK's Intensive Care National Audit and Research Centre data, up to April 30, shows that of 6574 patients with COVID-19 in intensive care, one third were from non-white ethnic groups; ethnic minorities make up only 13% of the population as a whole. However, data released by NHS England on April 19 showed that of 13 918 patients in hospitals in England who had tested positive for COVID-19 at time of death, 73·6% were white and 16·2% were of BAME ethnicity—more representative of the proportion of BAME people in the general population. “The problem is that data on deaths and serious illness from COVID-19 among the health-care workforce and their ethnicity is not being routinely published by the government”, explains Dr Chaand Nagpaul, the British Medical Association (BMA) council chair and a general practitioner (GP) in north London, UK. “However, it is a clear and consistent theme from the reports and what we know about those who have died so far, that a disproportionate number of those health-care workers who have tragically lost their lives are from BAME communities.” The UK Health Secretary Matt Hancock has announced that there will be a review into the impact of COVID-19 on BAME communities, led by NHS England and Public Health England (PHE). The UK Government subsequently confirmed that the review will also analyse the effect of gender and obesity, as well as ethnicity. “While the review speaks of looking at existing health data, the BMA believes it is also vital to collect detailed data around occupation for all health-care workers who contract the infection, given that more than 150 are reported to have died, including at least 16 doctors, of whom 94% are from BAME origin”, says Nagpaul. “It is important to ascertain whether there are any occupational factors that have played a part in these health-care workers contracting the virus so that we can learn how to put in place measures to protect all health-care workers.” He adds that many factors affecting the wider ethnic minority community apply to ethnic minority doctors, such as the greater prevalence of hypertension, diabetes, and coronary heart disease, which are thought to increase the severity of COVID-19 infection. “We also know that a large proportion of BAME doctors work in staff grade, specialist, and associate specialist roles, which are crucial, patient-facing roles that are invaluable for the running of the NHS”, adds Nagpaul. “Workplace factors could have a part to play too; for example, a recent BMA survey has found that BAME doctors were twice as likely as white doctors to feel pressured to see patients in high-risk settings without adequate personal protective equipment (PPE). Other BMA research revealed that BAME doctors are twice as likely not to feel confident to raise concerns about safety in the workplace compared with their white colleagues.” Nagpaul raised all these concerns in a letter to Simon Stevens, the chief executive of NHS England, and days later, on April 29, 2020, NHS England wrote to all hospital trusts across England—as well as ambulance services, mental health trusts, and organisations providing community health—asking them to risk assess their BAME workers and where necessary reassign them to duties that leave them less at risk of contracting COVID-19. On May 1, 2020, the UK's Institute for Fiscal Studies (IFS) published its report, which found that people from ethnic minorities are more likely to live in areas badly affected by COVID-19 infection. However, despite people from ethnic minorities being younger on average than the white British population, and therefore theoretically less susceptible to infection, they were found to have higher death rates. After adjusting for age, sex, and geography, the authors of the IFS report found that the death rate for people of black African descent was 3·5 times higher than for white British people, while for those of black Caribbean and Pakistani descent, death rates were 1·7 times and 2·7 times higher, respectively. In the USA, early data suggest that African Americans are disproportionately affected by COVID-19. In a preliminary study of data compiled from hospitals in 14 US states, African Americans represented 33% of COVID-19 hospitalisations, despite only making up 18% of the total population studied. In another analysis, among COVID-19 deaths for which race and ethnicity data were available, death rates from COVID-19 in New York City (NY, USA) among black or African American people (92·3 deaths per 100 000 population) and Hispanic or Latino people (74·3) were substantially higher than that of white (45·2) or Asian (34·5) people. “Studies are underway to confirm these data and understand and potentially reduce the impact of COVID-19 on the health of racial and ethnic minorities”, a spokesperson from the Centers for Disease Control and Prevention (CDC) confirmed to The Lancet Respiratory Medicine. Chronic conditions, such as diabetes, asthma, hypertension, kidney disease, and obesity, are all more common in African American than white populations; all of these conditions have been associated with worse outcomes in COVID-19. However, the CDC states many other factors could be involved, such as people from ethnic minorities being more likely to live in more densely populated areas and housing, to use public transport more, and to work in lower paid service jobs without sick pay, meaning they would be more likely to go to work under all circumstances, increasing the risk of exposure. “I do not think that the pattern we are seeing in COVID-19 deaths for African Americans is solely due to pre-existing health conditions”, says Thomas A LaVeist, Dean of the School of Public Health and Tropical Medicine at Tulane University, New Orleans, LA, USA. “Race disparities in those diseases are not large enough to fully explain the COVID-19 death disparity. For example, there are no racial differences in obesity among men. Also, especially in the southern US states, white people also have extremely high rates of obesity, diabetes, hypertension, and the other chronic diseases.” LaVeist says it is difficult to have definitive views on the cause of ethnic disparities in COVID-19 mortality until the overall infection rate has been established in different racial groups. “Are African Americans more likely to have been exposed to the virus? They seem to be more likely than others to work in jobs that place them at risk, such as check-out clerks and delivery drivers, and less likely to have jobs that allow them to work from home.” He adds that most southern states with larger ethnic minority populations have declined to expand Medicaid, which has reduced the number of poorer residents with regular access to primary health care. “Each of these factors, many of them the result of policy decisions, play a role in producing disproportionate death rates among African Americans”, he says. In Australia, steps have been taken to protect Indigenous Australians living in remote and rural locations, mainly through the introduction of extremely strict limitations on travel in or out of these communities. “It's important to stress that the majority of Indigenous Australians live in urban or regional areas—large and small cities mainly on the coast of Australia. While a lot of focus is on remote communities, a high proportion of Indigenous Australians in urban and regional areas have the same elevated risk of serious COVID-19 illness due to multiple chronic conditions and are at risk of rapid spread due to a high prevalence of overcrowding”, explains Jason Agostino, medical advisor to the National Aboriginal Community Controlled Health Organisation and Lecturer in General Practice at the Australian National University, Canberra, ACT, Australia. At the time of writing, Australia's latest COVID-19 epidemiology report (including data up to April 26, 2020) showed there were only 52 cases of COVID-19 among Indigenous Australians, representing less than 1% of Australia's cases despite Indigenous Australians being 3·3% of the population. “So far there have not been any cases in Indigenous Australians in remote or very remote regions”, explains Agostino. “Through the Aboriginal and Torres Strait Islander COVID-19 Advisory Group and other forums we are able to identify strategies to address community priorities. An early and positive step to prevent spread was the additional travel restrictions put in place for many remote communities at the request of community leaders.” However, institutional problems remain, in particular some communities have overcrowded housing and have no facilities to safely isolate and quarantine infected or suspected cases. “There has also been insufficient support to enable health-care staff to quarantine before entering remote communities. If a health service wants to enforce the 14-day quarantine for locum staff, they have to bear that cost”, says Agostino. Should an outbreak occur, protocols have been developed for early transfer of cases and their close contacts out of communities and into regional centres, and the Australian Federal Government recently announced additional funding for retrieval services. The risks of COVID-19 to Indigenous communities could not be clearer. More than 1 in 3 Indigenous Australian adults report having either cardiovascular disease, diabetes, or renal disease, and onset of these diseases often occurs 20 years earlier than the non-Indigenous population. Smoking rates are also much higher, with approximately 40% of adults smoking, more than double that seen in the non-Indigenous population. “The 2009 H1N1 influenza epidemic showed what can happen to Indigenous Australians”, says Agostino. “During that outbreak, rates of admission to the intensive care unit and mortality were some 4-times higher in Indigenous Australians compared with the non-Indigenous population.” He concludes that “while Australia's Federal and State and Territory Governments have put in place some good measures, the success so far is due to Aboriginal and Torres Strait Islander people taking the lead and protecting their communities. Indigenous Australians began a network of community-controlled health organisations in the 1970s and this so-called whole of community, whole of person approach to health care is what is helping protect them in this early stage of the pandemic.” © 2020 Jim West/Science Photo Library 2020 Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.
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                Author and article information

                Contributors
                Journal
                Lancet Glob Health
                Lancet Glob Health
                The Lancet. Global Health
                The Author(s). Published by Elsevier Ltd.
                2214-109X
                2 July 2020
                2 July 2020
                Affiliations
                [a ]Núcleo de Astrofísica e Cosmologia, Universidade Federal do Espírito Santo, Vitória, ES, Brazil
                [b ]Departamento de Física, Universidade Federal do Espírito Santo, Vitória, ES, Brazil
                [c ]Department of Engineering Science, University of Oxford, Oxford, UK
                [d ]The Alan Turing Institute, London, UK
                [e ]Department of Medicine, University of Cambridge, Cambridge, UK
                [f ]Cambridge Centre for Artificial Intelligence in Medicine, Cambridge, UK
                [g ]Department of Applied Mathematics and Theoretical Physics and Department of Population Health, University of Cambridge, Cambridge, UK
                [h ]Department of Electrical and Computer Engineering, University of California Los Angeles, Los Angeles, CA, USA
                Author notes
                [* ]Correspondence to: Dr Valerio Marra, Departamento de Física, Universidade Federal do Espírito Santo, 29075–910, Vitória, ES, Brazil marra@ 123456cosmo-ufes.org
                [†]

                Contributed equally

                Article
                S2214-109X(20)30285-0
                10.1016/S2214-109X(20)30285-0
                7332269
                32622400
                23784237-0d82-47fd-bfe7-4baaa7625d1f
                © 2020 The Author(s). Published by Elsevier Ltd. This is an Open Access article under the CC BY 4.0 license

                Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.

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