Social distancing measures to control the COVID-19 pandemic: potential impacts and challenges in Brazil

Estela M. L. Aquino Ismael Henrique Silveira Julia Moreira Pescarini Rosana Aquino Jaime Almeida de Souza-Filho Aline dos Santos Rocha Andrea Ferreira Audêncio Victor Camila Teixeira Daiane Borges Machado Enny Paixão Flávia Jôse Oliveira Alves Flávia Pilecco Greice Menezes Ligia Gabrielli Luciana Leite Maria da Conceição Chagas de Almeida Naiá Ortelan Qeren Hapuk R. Ferreira Fernandes Renzo Joel Flores Ortiz Raquel Nunes Palmeira Elzo Pereira Pinto Junior Erika Aragão Luis Eugenio Portela Fernandes de Souza Manoel Barral Netto Maria Glória Teixeira Mauricio Lima Barreto Maria Yury Ichihara Raíza Tourinho dos Reis Silva Lima About the authors

Abstract

The COVID-19 pandemic has challenged researchers and policy makers to identify public safety measures forpreventing the collapse of healthcare systems and reducingdeaths. This narrative review summarizes the available evidence on the impact of social distancing measures on the epidemic and discusses the implementation of these measures in Brazil. Articles on the effect of social distancing on COVID-19 were selected from the PubMed, medRXiv and bioRvix databases. Federal and state legislation was analyzed to summarize the strategies implemented in Brazil. Social distancing measures adopted by the population appear effective, particularly when implemented in conjunction with the isolation of cases and quarantining of contacts. Therefore, social distancing measures, and social protection policies to guarantee the sustainability of these measures, should be implemented. To control COVID-19 in Brazil, it is also crucial that epidemiological monitoring is strengthened at all three levels of the Brazilian National Health System (SUS). This includes evaluating and usingsupplementary indicators to monitor the progression of the pandemic and the effect of the control measures, increasing testing capacity, and making disaggregated notificationsand testing resultstransparentand broadly available.

Key words
COVID-19; Pandemics; Social distancing; Epidemiological surveillance

Introduction

Ever since the emergence in China in December 2019 of the new coronavirus, SARS-CoV-2, the virus responsible for the COVID-19 pandemic, humanity has been facing a severe global health crisis. Numerous new cases quickly appeared in Asian countries such as Thailand, Japan, South Korea and Singapore, followed by nations in Europe and in the other continents, leading the World Health Organization (WHO) to declare a public health emergency of international concern on January 30, 202011 World Health Organization (WHO). WHO Director-General's statement on IHR Emergency Committee on Novel Coronavirus (2019-nCoV). Geneva: WHO; 2020. [cited 2020 Apr 16]. Available from: https://www.who.int/news-room/detail/23-01-2020-statement-on-the-meeting-of-the-international-health-regulations-(2005)-emergency-committee-regarding-the-outbreak-of-novel-coronavirus-(2019-ncov)
https://www.who.int/news-room/detail/23-...
and a pandemic on March 11, 202022 World Health Organization (WHO). WHO Director-General's opening remarks at the media briefing on COVID-19-11 March 2020. Geneva: WHO; 2020 [cited 2020 Apr 16]. Available from: https://www.who.int/dg/speeches/detail/who-director-general-s-opening-remarks-at-the-media-briefing-on-covid-19---11-march-2020
https://www.who.int/dg/speeches/detail/w...
. By April 16 of this same year, 210 countries and territories worldwide had reported a total of 2.1 million confirmed cases of COVID-19,with a death toll exceeding 144,00033 Worldometer. Countries where COVID-19 has spread. 2020 [cited 2020 Apr 16]. Available from: https://www.worldometers.info/coronavirus/countries-where-coronavirus-has-spread/.
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Although the lethality of the disease caused by SARS-CoV-2 is lower than that found with other coronaviruses, its high transmissibility has led to more deaths in terms of absolute numbers than the combination of the SARS-CoV and MERS-CoV epidemics44 Mahase E. Coronavirus covid-19 has killed more people than SARS and MERS combined, despite lower case fatality rate. BMJ 2020; 368:m641.. SARS-CoV-2 transmission occurs predominantly through the spread of contaminated droplets of oropharyngeal secretions from an infected individual to a disease-free person. However, the role of airborne transmission and transmission via contact with contaminated surfaces and objects, where the virus could remain active for up to 72 hours, is still unknown55 van Doremalen N, Bushmaker T, Morris DH, Holbrook MG, Gamble A, Williamson BN, Tamin A, Harcourt JL, Thornburg NJ, Gerber SI, Lloyd-Smith JO. Aerosol and Surface Stability of SARS-CoV-2 as Compared with SARS-CoV-1. N Engl J Med 2020; 382(16):1564-1567., and the role of fecal-oral transmission remains under debate66 Ong SW, Tan YK, Chia PY, Lee TH, Ng OT, Wong MS, Marimuthu K. Air, Surface Environmental, and Personal Protective Equipment Contamination by Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) From a Symptomatic Patient. JAMA Netw Open 2020. [Epub ahead of print],77 Wang W, Xu Y, Gao R, Lu R, Han K, Wu G, Tan W. Detection of SARS-CoV-2 in Different Types of Clinical Specimens. JAMA Netw Open 2020. [Epub ahead of print]. SARS-CoV-2transmission is aggravated by its protracted mean incubation period of approximately 5-6 days (min-max: 0-24 days)88 Wang Y, Wang Y, Chen Y, Qin Q. Unique epidemiological and clinical features of the emerging 2019 novel coronavirus pneumonia (COVID-19) implicate special control measures. J Med Virol 2020. [Epub ahead of print]

9 Huang R, Xia J, Chen Y, Shan C, Wu C. A family cluster of SARS-CoV-2 infection involving 11 patients in Nanjing, China. Lancet Infect Dis 2020.
-1010 Kraemer MU, Yang CH, Gutierrez B, Wu CH, Klein B, Pigott DM, du Plessis L, Faria NR, Li R, Hanage WP, Brownstein JS. The effect of human mobility and control measures on the COVID-19 epidemic in China. Science 2020; pii:eabb4218., and by the fact that individuals who are asymptomatic, pre-symptomatic or with only mild symptoms are able to transmit the disease1111 Bai Y, Yao L, Wei T, Tian F, Jin DY, Chen L, Wang M. Presumed Asymptomatic Carrier Transmission of COVID-19. JAMA Netw Open 2020. [Epub ahead of print].

12 Tong ZD, Tang A, Li KF, Li P, Wang HL, Yi JP, Zhang YL, Yan JB. Potential Presymptomatic Transmission of SARS-CoV-2, Zhejiang Province, China, 2020. Emerg Infect Dis 2020; 26:5.
-1313 Kimball A, Hatfield KM, Arons M. Asymptomatic and Presymptomatic SARS-CoV-2 Infections in Residents of a Long-Term Care Skilled Nursing Facility - King County, Washington, March 2020. MMWR Morb Mortal Wkly Rep 2020; 69(13):377-381.. Although 80% of cases present as milder respiratory infections and pneumonias, the severe forms of the disease tend to affect the elderly and those with underlying chronic diseases1414 Eurosurveillance Editorial Team. Updated rapid risk assessment from ECDC on coronavirus disease 2019 (COVID-19) pandemic: increased transmission in the EU/EEA and the UK. Euro Surveill 2020; 25:12., requiring hospitalization, intensive care and mechanical ventilation.

The still sparse information on the modes of transmission and the role of asymptomatic carriers in spreading SARS-CoV-2, together with the inexistence of vaccines and specific treatment options, represents a challenge to researchers, healthcare managers and governments. Non-pharmaceutical public health interventions aimed at reducing the spread of the virus and avoiding the collapse of healthcare systems, have been used to allow timely treatment of severe complications and avoid deaths.

Several countries have implemented a series of interventions to reduce transmission of the virus and decelerate progression of the pandemic1515 Kupferschmidt K, Cohen J. Can China's COVID-19 strategy work elsewhere? Science 2020; 367(6482): 1061-1062.. These include isolation of cases, encouraging hand hygiene, respiratory etiquette and the use of homemade facemasks, and implementing social distancing measures such as closing schools and universities, banning large events and mass gatherings, restricting travel and public transportation, making the public aware of the need to stay at home, and even implementing total lockdown in which individuals are only allowed out to buy food or medicines or to seek healthcare. These measures have been introduced gradually and in differing ways, to a greater or lesser extent, in the different countries, and their results probably depend on socioeconomic and cultural aspects, on the characteristics of their political and healthcare systems, and on the operational procedures used in their implementation.

The sustainability and effectiveness of these measures depend on establishing social protection and support policies for vulnerable populations, guaranteeing the survival of individuals and their families while restrictions to economic activities remain in effect. In Brazil, there are vast social and regional inequalities, with 66 million individuals living in poverty or extreme poverty and only 40% of the population in formal employment1616 Instituto Brasileiro de Geografia, Estatística (IBGE). Síntese de indicadores sociais: uma análise das condições de vida da população brasileira. Rio de Janeiro: IBGE; 2018.. Such conditions require urgent economic measures to be implemented to guarantee a minimum income for the most vulnerable segment of the population and employment protection for salaried workers so as to ensure that a relevant proportion of the population will comply with social distancing measures.

The present study aimed to analyze the impact of social distancing policies on the COVID-19 pandemic and the challenges to implementing these policies in Brazil with a view to increasing understanding in the population and to provide a basis capable of supporting managers in their decision-making.

Methods

A total of 2,771 articles on COVID-19, published up to April 6, 2020 and listed in the PubMed databases, were screened for inclusion in this narrative review. In addition, manuscripts in the prepublication phase and available in the medRXiv and bioRvix databases or in the grey literature were also reviewed. Due to the speed of publication at the present time, articles published after the cut-off date but of the utmost relevance for Brazil were included in this review a posteriori. Twenty-one original or review articles focusing on control strategies and measures, particularly those on social distancing measures in different countries, were selected for inclusion. In addition to the scientific papers, federal and state legislation implemented throughout the country, specifically decrees and judicial decisions regarding social distancing, were analyzed up to the cut-off date of April 16, 2020 to summarize social distancing strategies in Brazil.

Since a great number of new papers are being produced every day, the recommendations presented here are subject to change as new evidence emerges.

What are social distancing measures and what is known regarding their effect on the progression of the epidemic?

The recent discovery of SARS-CoV-2 has resulted in a colossal effort by doctors, epidemiologists and other healthcare professionals to classify individuals with symptoms such as fever, cough, breathing difficulties and loss of smell and taste as being suspected of having the disease or not. Defining a case is relevant in monitoring the progression of an epidemic and studying the effect of disease control strategies in the population. In view of the high transmissibility of individuals infected by SARS-CoV-2 (symptomatic, pre-symptomatic and asymptomatic individuals), ideally, health surveillance authorities should adopt the definition most capable of detecting the universe of cases within a population. Since this is a new disease, the definitions need to be reviewed as more detailed information on the cases investigated comes to light1717 Brasil. Ministério da Saúde (MS). [informar o título da publicação]. Brasilia: MS; 2018.. In Brazil, a large proportion of symptomatic SARS-CoV-2 infections fail to be diagnosed in a timely fashion; therefore, to monitor the progression of the epidemic it has been suggested that broader definitions of cases should be included in the figures, also taking into consideration additional admissions to hospital and excess deaths due to acute respiratory diseases.

Some terms have been used to refer to the control actions used in the COVID-19 epidemic. These terms are not new and refer to the non-pharmaceutical public health interventions historically adopted for the control of epidemics, particularly in the absence of vaccines and antivirals. These include, principally, isolation, quarantining, social distancing and community containment strategies1818 Wilder-Smith A, Freedman DO. Isolation, quarantine, social distancing and community containment: pivotal role for old-style public health measures in the novel coronavirus (2019-nCoV) outbreak. J Travel Med 2020; 27:2..

Isolation consists of separating people who are ill from uninfected individuals to reduce the risk of transmission of the disease. To be effective, the isolation of sick individuals requires cases to be detected at an early stage and viral transmissibility of asymptomatic carriers to be very low. In the case of COVID-19, in which the incubation period is longer than that of other viruses, the high transmissibility of the disease by asymptomatic carriers limits effectiveness whenever case isolation constitutes the single or main measure1818 Wilder-Smith A, Freedman DO. Isolation, quarantine, social distancing and community containment: pivotal role for old-style public health measures in the novel coronavirus (2019-nCoV) outbreak. J Travel Med 2020; 27:2.. In fact, there is evidence that in asymptomatic SARS-CoV-2 carriers the viral load is similar to that of symptomatic patients1919 Zou L, Ruan F, Huang M, Liang L, Huang H, Hong Z, Yu J, Kang M, Song Y, Xia J, Guo Q. SARS-CoV-2 Viral Load in Upper Respiratory Specimens of Infected Patients. N Engl J Med 2020; 382(12):1177-1179., a finding that is corroborated by reports of disease transmission involving both asymptomatic carriers and individuals with only mild symptoms2020 Ling Z, Xu X, Gan Q, Zhang L, Luo L, Tang X, Liu J. Asymptomatic SARS-CoV-2 infected patients with persistent negative CT findings. Eur J Radiol 2020; 126:108956.. Therefore, the mass use of diagnostic tests, allowing infected individuals to be identified, as adopted in Germany and South Korea, is essential for isolation to be effective.

Quarantining consists of restricting the movement of individuals who are presumed to have been exposed to a contagious disease but who are not ill, either because they were not infected or because they are still in the incubation period of the disease or even because in the case of COVID-19 they will remain asymptomatic and will fail to be identified. This can be applied at individual or group level, ensuring that exposed individuals remain in their own homes, in institutions or in other specifically designated places. Quarantine can be voluntary or obligatory. During quarantine, all individuals must be monitored for the occurrence of symptoms. If symptoms develop, the individuals must be immediately isolated and treated. Quarantining is more successful in situations in which cases are detected rapidly and their contacts can be identified and screened within a short space of time1818 Wilder-Smith A, Freedman DO. Isolation, quarantine, social distancing and community containment: pivotal role for old-style public health measures in the novel coronavirus (2019-nCoV) outbreak. J Travel Med 2020; 27:2..

Social distancing refers to measures aimed at reducing interactions within a community, which can include infected individuals as yet unidentified, hence not in isolation. Since diseases transmitted through respiratory droplets require a certain physical proximity for contagion to occur, social distancing allows transmission to be reduced. Examples of social distancing measures that have been adopted include: the closure of schools and workplaces, closure of certain businesses, and cancellation of events to avoid mass gatherings. Social distancing is particularly useful in settings where there is community transmission of the virus, where the restriction measures imposed exclusively on known cases or on the most vulnerable segments of the population are considered insufficient to prevent new transmissions. The most extreme case of social distancing is total lockdown in which a rigorous intervention is applied to an entire community, city or region by forbidding people to leave their homes except to purchase basic supplies or to access emergency services. Lockdown enables social contact to be drastically reduced1818 Wilder-Smith A, Freedman DO. Isolation, quarantine, social distancing and community containment: pivotal role for old-style public health measures in the novel coronavirus (2019-nCoV) outbreak. J Travel Med 2020; 27:2..

What measures have been adopted in different countries and under what circumstances?

The first cases of this new disease began to appear in December 2019 in the Chinese city of Wuhan. There was one common source of exposure, a seafood market that also sold live animals2121 Singhal T. A Review of Coronavirus Disease-2019 (COVID-19). Indian J Pediatr 2020; 87(4):281-286.. The health surveillance authorities were alerted and several measures began to be taken to identify the causative agent of the disease. On December 31 of that same year, China notified the WHO of the outbreak and on the following day the market where the cases had originated was closed2222 World Health Organization (WHO). Novel Coronavirus (2019-nCoV) Situation report-5, 25 January 2020. Geneva: WHO; 2020.. From then onwards, an exponential increase occurred in the number of cases and community transmission was confirmed. Within a short period of time, measures were implemented to restrict travel and the circulation of people, including screening travellers for symptoms, until on January 23, 2020 total lockdown was declared in Wuhan, with no one being allowed to enter or leave the region2323 Chinazzi M, Davis JT, Ajelli M, Gioannini C, Litvinova M, Merler S, Piontti AP, Mu K, Rossi L, Sun K, Viboud C. The effect of travel restrictions on the spread of the 2019 novel coronavirus (COVID-19) outbreak. Science 2020; pii:eaba9757..

These localized measures were followed by the implementation of similar actions in other Chinese provinces affected by the virus, in several other Asian countries, and in other countries around the world. The initial measures focused to a major extent on controlling travel at a time when the majority of cases were imported; however, the measures were progressively ramped up as community transmission was confirmed.

The first three cases of COVID-19 in Europe were recorded in France on January 24, 2020 and the first death in that continent was reported in that same country on February 152424 Spiteri G, Fielding J, Diercke M, Campese C, Enouf V, Gaymard A, Bella A, Sognamiglio P, Moros MJ, Riutort AN, Demina YV. First cases of coronavirus disease 2019 (COVID-19) in the WHO European Region, 24 January to 21 February 2020. Euro Surveill 2020; 25:9.. A week later, cases were registered in another eight countries. The epidemic expanded dramatically in Italy, Spain and France, where it rapidly developed into a severe health crisis with many critical cases and deaths, consequently overwhelming healthcare system resources. This accelerated the adoption of control measures, which did not occur simultaneously and varied greatly between countries and between different regions of the same country. However, over time these measures had to be ramped up and strengthened in all countries as the health crisis deteriorated.

Chart 1 summarizes the main interventions adopted by selected European countries based on a study by Imperial College London. Despite some similarities, implementation of the different measures varied, even in relation to the time period between the first initiative and the announcement of total lockdown.

Chart 1
Measures to contain COVID-19 implemented in a selection of European countries affected by the disease.

In some countries, the first initiative was to ban mass gatherings of more than 1,000 people; however, this number was subsequently reduced to 500 and then to 50. In other countries, cinemas, restaurants, gyms and places of worship were closed. Germany determined the closure of most non-essential shops and extended the opening times of supermarkets to reduce the number of customers in the stores at the same time. In some countries, stores reserved the first hours of trading for elderly clients at a high risk of severe disease2525 Cohen J, Kupferschmidt K. Countries test tactics in 'war' against COVID-19. Science 2020; 367(6484):1287-1288..

The closure of schools, a measure adopted in all countries, has been the subject of much debate. Children are rarely affected by COVID-19 and the extent to which they develop asymptomatic infections and transmit the virus is unclear. Although closing schools may have the added benefit of contributing towards ensuring that parents remain at home, this measure may affect the ability of parents, who are health professionals and whose services are of the utmost importance at this time, to work. Furthermore, other negative effects include an increase in the number of children cared for by elderly grandparents, interruption to the supply of free school meals to vulnerable children and, obviously, the fact that children would be denied their right to formal education for months at a time2525 Cohen J, Kupferschmidt K. Countries test tactics in 'war' against COVID-19. Science 2020; 367(6484):1287-1288.. For these reasons, although schools in Austria, the Netherlands and the United Kingdom were closed, an exception was made for the children of key workers such as health professionals2525 Cohen J, Kupferschmidt K. Countries test tactics in 'war' against COVID-19. Science 2020; 367(6484):1287-1288.,2626 Mahase E. Covid-19: schools set to close across UK except for children of health and social care workers. BMJ 2020; 368:m1140.. In the United Kingdom, vulnerable children (recipients of social care) were also allowed to attend school. In addition, the government decided that schools could provide meals to children who usually received them free of charge and announced in the media the creation of a national program of food vouchers2626 Mahase E. Covid-19: schools set to close across UK except for children of health and social care workers. BMJ 2020; 368:m1140.. In Singapore, although schools remained open, measures were adopted to reduce the size of classes and the number of interclass and interschool activities, while rigorous hygiene measures were implemented and recess and lunch breaks were staggered2525 Cohen J, Kupferschmidt K. Countries test tactics in 'war' against COVID-19. Science 2020; 367(6484):1287-1288.,2727 Lee VJ, Chiew CJ, Khong WX. Interrupting transmission of COVID-19: lessons from containment efforts in Singapore. J Travel Med 2020; pii:taaa039..

Some countries such as the United Kingdom, the Netherlands, Sweden and the United States were initially reluctant to adopt social distancing measures2828 The Lancet Respiratory Medicine. COVID-19: delay, mitigate, and communicate. Lancet Respir Med 2020; 8(4):321.,2929 Eurosurveillance Editorial Team. Updated rapid risk assessment from ECDC on the novel coronavirus disease 2019 (COVID-19) pandemic: increased transmission in the EU/EEA and the UK. Euro Surveill 2020; 25:10., advocating the isolation of confirmed cases and of groups at greater risk. Nevertheless, as the epidemic progressed and the epidemiological indicators worsened, these countries were obliged to review their policies and adopt restrictive measures already implemented in other countries. Within a context of rapid spread of the pandemic, with the number of cases and the number of deaths continuing to increase in many countries, the need for social distancing measures and measures to restrict the circulation of people became obvious, with total lockdown sometimes being necessary3030 Deshwal VK. COVID 19: A Comparative Study of Asian, European, American continent. IJSRED 2020; 3:2.. Measures of this nature allow time to be gained in which to organize the healthcare and epidemiological surveillance resources required to control COVID-19. In countries of continental dimensions and very large populations such as India and Brazil, social inequalities are immense and healthcare resources are chronically deficient and unequally distributed. In such countries, the adoption of more rigorous social distancing measures will be a determining factor in minimizing the imminent collapse of healthcare services and avoiding thousands of deaths as a result of lack of care for severe cases of the disease.

What scientific evidence is there on the impactof control measures on the epidemic?

Due to the speed at which the COVID-19 epidemic emerged, many of the epidemic control interventions were introduced simultaneously, and compliance differed from country to country. Therefore, it is difficult to evaluate the effectiveness of each single intervention alone. In general, the studies available involve mathematical models of disease transmission based on observed data and on the simulation of hypothetical scenarios according to which the interventions adopted would be able to reduce transmission of the virus. Simulation studies evaluate responses associated with different contexts and are useful for directing the allocation of resources and taking decisions to maximize the intervention strategies. Few studies have managed to evaluate the actual effectiveness of some of these measures in the dynamics of SARS-CoV-2 transmission.

In mid-March, investigators from Imperial College London used a mathematical model to simulate the effect of a series of epidemic control measures, implemented individually or together, in the United Kingdom (specifically Great Britain) and in the United States. The effectiveness of any single intervention seemed limited, indicating that multiple interventions must be used in conjunction to make a substantial impact in reducing transmission of the virus3131 Ferguson N, Laydon D, Nedjati Gilani G, Imai N, Ainslie K, Baguelin M, Bhatia S, Boonyasiri A, Cucunuba Perez ZU, Cuomo-Dannenburg G, Dighe A. Impact of non-pharmaceutical interventions (NPIs) to reduce COVID-19 mortality and healthcare demand. Imperial College COVID-19 Response Team. United Kingdom: Imperial College COVID-19 Response Team, 2020.. Combining less restrictive control measures (isolation of suspected cases, quarantining of contacts and social distancing for the elderly and those at greater risk of the disease) could reduce the peak of demand on healthcare services by two-thirds, also halving the number of deaths. Nevertheless, with this type of strategy, the COVID-19 epidemic would result in hundreds of thousands of deaths and would overwhelm healthcare services, particularly intensive care units (ICUs). For this reason, drastic measures of social distancing applied to the entire population should be the policy of choice, despite the fact that this option will depend on the feasibility of its implementation and on the social contexts3131 Ferguson N, Laydon D, Nedjati Gilani G, Imai N, Ainslie K, Baguelin M, Bhatia S, Boonyasiri A, Cucunuba Perez ZU, Cuomo-Dannenburg G, Dighe A. Impact of non-pharmaceutical interventions (NPIs) to reduce COVID-19 mortality and healthcare demand. Imperial College COVID-19 Response Team. United Kingdom: Imperial College COVID-19 Response Team, 2020..

China initiated a form of isolation in which all cases were hospitalized, not only those requiring hospital care, while simultaneously implementing social distancing for the entire population, resulting in a reduction in transmission. Several studies have estimated that these interventions reduced the mean rate of transmission of COVID-19,as measured by a decrease in the basic reproduction number (R0)3232 Barreto ML, Teixeira MG, Carmo EH. Infectious diseases epidemiology. J Epidemiol Community Health 2006; 60(3):192. to less than 1, i.e. showing that an infected individual can infect on average less than one other person, a situation that is essential if a decrease in the incidence of cases is to be achieved3131 Ferguson N, Laydon D, Nedjati Gilani G, Imai N, Ainslie K, Baguelin M, Bhatia S, Boonyasiri A, Cucunuba Perez ZU, Cuomo-Dannenburg G, Dighe A. Impact of non-pharmaceutical interventions (NPIs) to reduce COVID-19 mortality and healthcare demand. Imperial College COVID-19 Response Team. United Kingdom: Imperial College COVID-19 Response Team, 2020..

A study conducted in Wuhan using COVID-19 data associated with smartphone records concluded that people's mobility was the principal factor in the spread of SARS-CoV-2, both in that city and in other provinces, before implementation of the sanitary cordon1010 Kraemer MU, Yang CH, Gutierrez B, Wu CH, Klein B, Pigott DM, du Plessis L, Faria NR, Li R, Hanage WP, Brownstein JS. The effect of human mobility and control measures on the COVID-19 epidemic in China. Science 2020; pii:eabb4218.. In this respect, restricting the mobility of the population can contribute to delaying the peak of the epidemic, to reducing the number of cases within a city and to avoiding transmission to other locations1010 Kraemer MU, Yang CH, Gutierrez B, Wu CH, Klein B, Pigott DM, du Plessis L, Faria NR, Li R, Hanage WP, Brownstein JS. The effect of human mobility and control measures on the COVID-19 epidemic in China. Science 2020; pii:eabb4218.,2323 Chinazzi M, Davis JT, Ajelli M, Gioannini C, Litvinova M, Merler S, Piontti AP, Mu K, Rossi L, Sun K, Viboud C. The effect of travel restrictions on the spread of the 2019 novel coronavirus (COVID-19) outbreak. Science 2020; pii:eaba9757.,3333 Boldog P, Tekeli T, Vizi Z, Denes A, Bartha FA, Rost G. Risk Assessment of Novel Coronavirus COVID-19 Outbreaks Outside China. J Clin Med 2020; 9:2.,3434 Lau H, Khosrawipour V, Kocbach P, Mikolajczyk A, Schubert J, Bania J, Khosrawipour T. The positive impact of lockdown in Wuhan on containing the COVID-19 outbreak in China. J Travel Med 2020; pii:taaa037.. Measures involving travel restrictions from Wuhan, the quarantining of household contacts and social distancing were responsible for increasing the doubling time in the number of cases of the disease and for slowing disease spread, as measured by the R0, which decreased from 0.98 to 0.913434 Lau H, Khosrawipour V, Kocbach P, Mikolajczyk A, Schubert J, Bania J, Khosrawipour T. The positive impact of lockdown in Wuhan on containing the COVID-19 outbreak in China. J Travel Med 2020; pii:taaa037..

Another study that evaluated travel restrictions in Wuhan, using COVID-19 data from within and outside this urban center for the period from December 2019 to February 2020, found a reduction in transmission at the end of January, coinciding with the introduction of travel restrictions3535 Kucharski AJ, Russell TW, Diamond C, Liu Y, Edmunds J, Funk S, Eggo RM, Sun F, Jit M, Munday JD, Davies N. Early dynamics of transmission and control of COVID-19: a mathematical modelling study. Lancet Infect Dis 2020; S1473-3099(20)30144-4.. In addition, the closure of the airports in China, which occurred around two months after the beginning of the epidemic, led to a delay in the occurrence of new cases outside of Wuhan, both in the rest of China and internationally2323 Chinazzi M, Davis JT, Ajelli M, Gioannini C, Litvinova M, Merler S, Piontti AP, Mu K, Rossi L, Sun K, Viboud C. The effect of travel restrictions on the spread of the 2019 novel coronavirus (COVID-19) outbreak. Science 2020; pii:eaba9757.. Nevertheless, it is estimated that reducing the number of flights by up to 90% would only result in a decrease in the number of cases in other countries if early detection, isolation and behavioral changes in the population such as hand hygiene, avoiding mass gatherings, etc., were implemented and encouraged in conjunction2323 Chinazzi M, Davis JT, Ajelli M, Gioannini C, Litvinova M, Merler S, Piontti AP, Mu K, Rossi L, Sun K, Viboud C. The effect of travel restrictions on the spread of the 2019 novel coronavirus (COVID-19) outbreak. Science 2020; pii:eaba9757..

The reduction in the epidemic in China partially attributed to social distancing triggered the implementation of similar measures in other places. An early study using smartphone tracking data to evaluate the impact of social distancing in Italy reported a reduction of around 40% in travel between regions and a 17% reduction in the rates of social mixing (the number of devices within 50 meters of each other over a 1-hour period) following total lockdown in the country3636 Pepe E, Bajardi P, Gauvin L, Privitera F, Lake B, Cattuto C, Tizzoni M. COVID-19 outbreak response: a first assessment of mobility changes in Italy following national lockdown. medRxiv 2020; 2020.03.22.20039933.. In the northern provinces, in the regions more affected by the disease, the measures implemented to control spread of the virus achieved a reduction of up to 30% in the rate of social contact3636 Pepe E, Bajardi P, Gauvin L, Privitera F, Lake B, Cattuto C, Tizzoni M. COVID-19 outbreak response: a first assessment of mobility changes in Italy following national lockdown. medRxiv 2020; 2020.03.22.20039933..

In an attempt to perform a broader modeling of the course of the epidemic in various countries around the world, data from China and from other high-income countries were used to model the effect of three interventions on COVID-19-related mortality3737 Flaxman S, Mishra S, Gandy A. Estimating the number of infections and the impact of non-pharmaceutical interventions on COVID-19 in 11 European countries. United Kingdom: Imperial College COVID-19 Response Team; 2020.. A comparison was made with data from a setting in which social distancing measures were not implemented but where mass testing for COVID-19 is performed, including the isolation of cases and quarantining of contacts (measures already widely reported to be essential). By protecting the elderly, reducing their social contacts by 60%, and reducing social contacts in the general population by 40%, there would be a huge decrease in the number of infections, admissions to hospital and deaths. A drop of up to 67% was estimated in COVID-19-related deaths (median 49%; range 23-67%), representing 20 million lives saved. Nevertheless, the effect of these strategies on reducing the number of infections in low- and medium-income countries could be less, since the elderly in those countries tend to have greater contact with the younger generations. In general, the authors of that study exert caution when discussing the actual impact of these interventions on the reduction in the number of cases of COVID-19 in these countries. If, on the one hand, the demographic structure is characterized by a greater percentage of younger people, on the other hand, a large proportion of the population lives in conditions of social vulnerability, in overcrowded environments and homes, and consists of individuals with chronic morbidities. In settings in which the organization and capacity of the healthcare system are precarious, these factors can contribute to increasing mortality.

A study conducted in Brazil using a mathematical model to estimate the effect of social distancing measures in the greater metropolitan region of São Paulo showed that, without the adoption of social distancing measures, the capacity of the ICUs for COVID-19 would be overwhelmed by 130% in the first month and 14-fold in the second month. The model also suggested that the set of social distancing measures implemented (and their continuation up to the present time) could avoid overwhelming the healthcare system, maintaining capacity at a maximum of 76% and avoiding the death of around 90,000 individuals over the course of the epidemic3838 Ganem F, Mendes FM, Oliveira SB, Porto VB, Araujo W, Nakaya H, Diaz-Quijano FA, Croda J. The impact of early social distancing at COVID-19 Outbreak in the largest Metropolitan Area of Brazil. medRxiv 2020; 2020.04.06.20055103.. Furthermore, the study recommended the use of data on admissions to hospital for severe acute respiratory syndromes (SARS) to monitor the effect of social distancing measures3838 Ganem F, Mendes FM, Oliveira SB, Porto VB, Araujo W, Nakaya H, Diaz-Quijano FA, Croda J. The impact of early social distancing at COVID-19 Outbreak in the largest Metropolitan Area of Brazil. medRxiv 2020; 2020.04.06.20055103.. Another study conducted in Brazil also showed that, at the present moment, maintaining and strengthening current social distancing measures, quarantining and isolating cases, is absolutely vital to avoid the collapse of the healthcare systems in the country3939 Canabarro A, Tenorio E, Martins R, Martins L, Brito S, Chaves R. Data-Driven Study of the COVID-19 Pandemic via Age-Structured Modelling and Prediction of the Health System Failure in Brazil amid Diverse Intervention Strategies. medRxiv 2020; 2020.04.03.20052498.. Other studies, still at the prepublication stage, describe similar findings, arguing that the more restrictive the measures, the more effective they are in reducing the number of affected individuals and the faster the end of the epidemic will be reached4040 Hou J, Hong J, Ji B, Dong B, Chen Y, Ward MP, Tu W, Jin Z, Hu J, Su Q, Wang W. Changing transmission dynamics of COVID-19 in China: a nationwide population-based piecewise mathematical modelling study. medRxiv 2020; 2020.03.27.20045757.,4141 Yang Q, Yi C, Vajdi A, Cohnstaedt LW, Wu H, Guo X, Scoglio CM. Short-term forecasts and long-term mitigation evaluations for the COVID-19 epidemic in Hubei Province, China. medRxiv 2020; 2020.03.27.20045625..

Finally, a rapid Cochrane review performed to evaluate the effectiveness of quarantine measures in avoiding deaths due to COVID-19 included 22 papers on epidemics such as SARS, MERS and COVID-19 published up to March 12, 2020, ten of which deal with the current epidemic4242 Nussbaumer-Streit B, Mayr V, Dobrescu AI, Chapman A, Persad E, Klerings I, Wagner G, Siebert U, Christof C, Zachariah C, Gartlehner G. Quarantine alone or in combination with other public health measures to control COVID-19: a rapid review. Cochrane Database Syst Rev 2020; 4:CD013574.. The synthesis of the studies included, most of which used a mathematical model, indicated that quarantining is an effective measure to reduce the number of cases of COVID-19; however, to achieve effective control of the disease, quarantine must be implemented together with other control measures4242 Nussbaumer-Streit B, Mayr V, Dobrescu AI, Chapman A, Persad E, Klerings I, Wagner G, Siebert U, Christof C, Zachariah C, Gartlehner G. Quarantine alone or in combination with other public health measures to control COVID-19: a rapid review. Cochrane Database Syst Rev 2020; 4:CD013574..

Therefore, there are strong indications that the strategies used to control the spread of the epidemic are effective when the isolation of cases and quarantining of contacts are combined with a set of social distancing measures that encompass the entire population4242 Nussbaumer-Streit B, Mayr V, Dobrescu AI, Chapman A, Persad E, Klerings I, Wagner G, Siebert U, Christof C, Zachariah C, Gartlehner G. Quarantine alone or in combination with other public health measures to control COVID-19: a rapid review. Cochrane Database Syst Rev 2020; 4:CD013574.. In general, data on the effectiveness of single measures are sparse3131 Ferguson N, Laydon D, Nedjati Gilani G, Imai N, Ainslie K, Baguelin M, Bhatia S, Boonyasiri A, Cucunuba Perez ZU, Cuomo-Dannenburg G, Dighe A. Impact of non-pharmaceutical interventions (NPIs) to reduce COVID-19 mortality and healthcare demand. Imperial College COVID-19 Response Team. United Kingdom: Imperial College COVID-19 Response Team, 2020.; however, it is extremely unlikely that they would be effective, since asymptomatic individuals, including children and adults, contribute to the chain of transmission of the disease. Furthermore, it is of the utmost importance that screening and the isolation of cases and contacts are enhanced in combination with social distancing measures3434 Lau H, Khosrawipour V, Kocbach P, Mikolajczyk A, Schubert J, Bania J, Khosrawipour T. The positive impact of lockdown in Wuhan on containing the COVID-19 outbreak in China. J Travel Med 2020; pii:taaa037.. Chart 2 summarizes the principal measures, and their respective impacts, as evaluated in the studies included in this narrative review.

Chart 2
Principal effects of non-pharmaceutical interventions in the COVID-19 epidemic as analyzed in the scientific literature.

What is the current epidemiological situation in Brazil and what constitutes adequate measures to control the epidemic?

The first case of COVID-19 in Latin America was registered in Brazil on February 25, 2020 and consisted of a 61-year old male from São Paulo who had recently returned from a trip to Lombardy in Italy. Following laboratory confirmation of COVID-19, the patient, who had mild symptoms of the disease, was given the standardized care recommended by the epidemiological surveillance authorities and told to self-isolate at home while contacts were investigated among family members, at the hospital where he received care and on the flight back from Italy.

Since then, the epidemic has spread in the country and, on April 16, 2020, there were already 30,718 confirmed cases and 1,926 deaths throughout Brazil, with an incidence of 14.51/100,000 inhabitants4343 Rede CoVida [Internet]. Painel Coronavírus Brasil. Salvador: Rede CoVida; 2020. [cited 2020 Apr 16]. Available from: http://www.covid19br.org.
http://www.covid19br.org...
. The entire academic community was mobilized nationwide, with the creation of several national networks formed to combat COVID-194444 Silva AAM. Sobre a possibilidade de interrupção da epidemia pelo coronavírus (COVID-19) com base nas melhores evidências científicas disponíveis. Rev Bras Epidemiol 2020; 23:e200021.. The large number of samples for laboratory testing that remained untested due to the impossibility of increasing testing capacity points to major underreporting.

Although legislation regarding measures with which to tackle COVID-19 has been in place in the country since February 7, 2020, i.e. before the epidemic was officially recognized in the country, President Jair Bolsonaro has given little importance to it. In fact, he is one of the few world leaders who refuse to recognize the threat constituted by the virus. There are numerous articles in the media repeating his public statements against the measures implemented in the states and municipalities and encouraging his followers on social media sites to disobey the social distancing recommendations. An open political conflict began between the president and the then Minister of Health, Luiz Henrique Mandetta, who defended the measures recommended by the WHO and until recently supported the more rigorous measures implemented locally and regionally to control COVID-19. At the beginning of April, following rumors regarding his imminent removal from office, which indeed occurred on April 16, Mandetta began to recommend “relaxation” of the social distancing measures implemented in the states and municipalities from April 13 onwards.

In this political setting in which a serious political crisis is compounding the health crisis, control measures, including social distancing, have been implemented by the state governors and municipal mayors (and sometimes by the Judiciary), particularly in the states most affected by the epidemic. The administrative autonomy of the states and municipalities in areas such as health, education and business, guaranteed in the federal constitution, limits the possibility of direct interference by the federal government in decisions made by local governments. This has been a subject of debate in the Supreme Court and up to the present time recognition of the autonomy of the states and municipalities with respect to the adoption of emergency measures regarding public health has been upheld.

Chart 3 describes the measures adopted in Brazil in some of the states in which the epidemic has been more severe and in Bahia, one of the first states to adopt social distancing measures. The complete Chart is presented as supplementary material (Chart S1). In general, practical measures to restrict circulation and prevent mass gatherings have already been put into practice, to greater and lesser degrees. Nevertheless, the federal government, by minimizing the importance of social distancing and publicly opposing the measures adopted in the states and municipalities, may well undermine the population's willingness to comply with them.

Chart 3
COVID-19 control measures implemented at state and federal level in Brazil, presented for a selection of Brazilian states, together with the number of notified cases per 100,000 inhabitants, updated on April 16, 2020.

Although no studies have yet been published on the degree to which the Brazilian population is complying with these measures, in a survey conducted by Datafolha 1,511 individuals were interviewed between April 1 and 3, with results showing that 76% were in agreement with maintaining social distancing to control the epidemic despite the economic damage resulting from these measures. Support was highest in the northeast of the country (81%) and lowest in the south (70%) (Figure 1). Nevertheless, a quarter of those interviewed reported that they had to leave their homes to go to work or to perform other activities.

Figure 1
Performance of activities of daily living during social distancing in Brazil, April 1-3, 2020 (Source: Datafolha).

Some indicators supplied by Google, obtained from smartphone records, suggest that there was a reduction of 70% of peoples movements in parks, of 71% in people engaging in commercial and leisure activities and of 64% in people circulating in transport hubs (Figure 2). However, as shown in the Datafolha survey, a significant proportion of the population is unable to stop working or cannot work from home and, in this respect, the reduction in mobility was of 34%.

Figure 2
Changes in social mobility according to the type of setting in Brazil on March 29, 2020 in relation to February 16, 2020 (Source: COVID-19 Community Mobility Report: google.com/covid19/mobility).

Despite support by the population for social distancing measures, however insufficient these may be, the Ministry of Health, on April 6 (hence still under the jurisdiction of Mandetta) expressed intention to relax these measures4545 Brasil. Ministério da Saúde (MS). Boletim Epidemiológico Especial 7: doença pelo coronavírus 2019. Brasília: MS; 2020., at a time when the epidemic was still on the increase, not yet having reached its peak, even in São Paulo where the first cases in Brazil were registered. The states were recommended to transition to selective distancing if the number of confirmed cases did not exceed 50% of the capacity of the healthcare facilities already in existence prior to the pandemic. In places where the incidence rate was 50% higher than the national rate, social distancing measures should be maintained until supplies and equipment (hospital beds, personal protective equipment, mechanical ventilators and laboratory testing) and healthcare teams were sufficient available.

The decision to relax social distancing measures and the criteria adopted by the Ministry of Health should be discussed in the light of the information available in the international scientific literature, which, contrary to those proposed for Brazil, has based its decisions on monitoring the speed of transmission of the epidemic and, consequently, as a function of the increase in the number of infected individuals, the number of cases of the disease and the number of deaths.

Relaxing or ending social distancing measures is a delicate issue, since maintaining control of the pandemic until a vaccine is available could require the population's routine activities of daily living to be curtailed for many months, with economic implications and consequent high costs for the lives of the population. On the other hand, the possibility has been suggested of ending the more rigorous social distancing measures, allowing some infections to occur, preferably in low-risk groups such as children or young adults so that a large part of the population gains immunity (the so-called “herd immunity”).

The principal limitation in the Ministry of Health's proposed criteria for relaxing the social distancing measures is that these are based solely on the capacity of the healthcare services, as measured by indicators of the offer and structure of the services. Hence, they fail to take into consideration the surveillance and monitoring indicators of the pandemic in each one of the Brazilian municipalities such as, for example, the number of suspected and confirmed cases, the number of admissions to hospital for acute respiratory syndromes, mortality, R0 and doubling time. Furthermore, the epidemic is at different stages in the different parts of the country. As suggested by the European commission4646 European Comission. A European roadmap to lifting coronavirus containment measures. 2020 [cited 2020 Apr 16]. Available from: https://ec.europa.eu/info/live-work-travel-eu/health/coronavirus-response/european-roadmap-lifting-coronavirus-containment-measures_en
https://ec.europa.eu/info/live-work-trav...
, the criteria for relaxing social distancing measures must include: 1) a significant decrease and stabilization for a sustained period of the number of cases and the number of admissions to hospital due to the disease; 2) sufficient health system capacity, including the occupation rate for ICUs, the availability of health care workers and medical material; 3) appropriate monitoring capacity,including large-scale testing capacity to quickly detect and isolate infected individuals and quarantine contacts, and, if possible, the application of rapid testing to monitor herd immunity.

In addition, up to the present moment, the Ministry of Health has failed to make clear what has to be taken into consideration when measuring the capacity of healthcare services, although the number of hospital beds, personal protective equipment (PPE), mechanical ventilators and laboratory testing are already covered, apparently indicating that priority is being given to the more specialized services. Given that in Brazil there are marked social and regional inequalities in the distribution of healthcare services and in access to those services, particularly those of greater complexity, we are aware that not everyone who needs care will receive it. Therefore, the collapse not only of hospital services but indeed of the entire healthcare network is predictable.

Chart 4
COVID-19 control measures implemented at state and federal level in Brazil and the number of notified cases per 100,000 inhabitants, updated on April 16, 2020.

Social distancing measures cannot be implemented without analyzing the progression of the disease, as monitored by health surveillance measures. This is the only possible way of defining the moment at which the interventions can be temporarily relaxed for relatively short windows of time in case it becomes necessary to reintroduce measures if or whenthe number of cases starts to rise again3131 Ferguson N, Laydon D, Nedjati Gilani G, Imai N, Ainslie K, Baguelin M, Bhatia S, Boonyasiri A, Cucunuba Perez ZU, Cuomo-Dannenburg G, Dighe A. Impact of non-pharmaceutical interventions (NPIs) to reduce COVID-19 mortality and healthcare demand. Imperial College COVID-19 Response Team. United Kingdom: Imperial College COVID-19 Response Team, 2020.. The criteria adopted in various countries for relaxing social distancing measures have prioritized monitoring the speed of transmission of the virus and, as a consequence, the number of infected individuals and of existing cases.

Imperial College London proposed the systematic inclusion of data on hospital admissions in surveillance systems on which decisions to activate and deactivate social distancing are based, rather than opting for interventions of fixed duration. Measures can then be adapted for use at regional and state level. Since the pandemic does not occur in a synchronized fashion, local policies can be more effective, reaching levels of suppression comparable with those at national level, even if in effect for a shorter period. Estimates for Great Britain indicate that nationwide social distancing strategies would need to be kept in force for at least two-thirds of the time until a vaccine becomes available3131 Ferguson N, Laydon D, Nedjati Gilani G, Imai N, Ainslie K, Baguelin M, Bhatia S, Boonyasiri A, Cucunuba Perez ZU, Cuomo-Dannenburg G, Dighe A. Impact of non-pharmaceutical interventions (NPIs) to reduce COVID-19 mortality and healthcare demand. Imperial College COVID-19 Response Team. United Kingdom: Imperial College COVID-19 Response Team, 2020..

The experiences in China and South Korea have shown that suppression of the epidemic is possible over the short term; however, it is not known whether this is maintained over the long term and if the social and economic costs of the interventions adopted up to now could be reduced. China, which managed to stop progression of the epidemic with social distancing measures implemented in conjunction with the isolation of cases, started to relax these measures after they had been in force for three months. This relaxing of the measures is accompanied by rigorous monitoring of the epidemiological situation so as to permit rapid reversal should the number of cases start to increase again. This will, without doubt, help direct strategies in other countries3131 Ferguson N, Laydon D, Nedjati Gilani G, Imai N, Ainslie K, Baguelin M, Bhatia S, Boonyasiri A, Cucunuba Perez ZU, Cuomo-Dannenburg G, Dighe A. Impact of non-pharmaceutical interventions (NPIs) to reduce COVID-19 mortality and healthcare demand. Imperial College COVID-19 Response Team. United Kingdom: Imperial College COVID-19 Response Team, 2020..

Major uncertainties still remain regarding the effectiveness of the measures and to what extent the population will spontaneously adopt risk-reduction behavior. Therefore, it is impossible to establish the precise duration of the measures, except that it will probably be several months. Nevertheless, the only certainty at the moment is that future decisions regarding the moment at which measures can be safely relaxed and for how long will have to be based on continuous and rigorous epidemiological surveillance3131 Ferguson N, Laydon D, Nedjati Gilani G, Imai N, Ainslie K, Baguelin M, Bhatia S, Boonyasiri A, Cucunuba Perez ZU, Cuomo-Dannenburg G, Dighe A. Impact of non-pharmaceutical interventions (NPIs) to reduce COVID-19 mortality and healthcare demand. Imperial College COVID-19 Response Team. United Kingdom: Imperial College COVID-19 Response Team, 2020..

Final considerations and recommendations

The COVID-19 epidemic is still on the increase in all the Brazilian states and Federal District. The political crisis, aggravated by the change in command at the Ministry of Health, introduces further uncertainties regarding the policies to be adopted by the federal government. The scientific findings presented in this review strongly suggest that, taken in conjunction, isolating cases, quarantining contacts and implementing large-scale social distancing measures, particularly those aimed at reducing social contact by at least 60%, can potentially reduce transmission of the disease. Although there is little in the literature on the subject in the particular setting of Brazil, the prior experience of countries in Asia and Europe suggests that social distancing strategies should be strengthened, should be intersectoral and must be coordinated between different government and regional agencies with the aim of reaching the end of the epidemic as quickly as possible and avoiding second and subsequent waves of the virus.

Implementation in Brazil is undoubtedly an enormous challenge. The marked social inequalities in the country, with a large percentage of the population living in a state of poverty and an increasing number of homeless people, in addition to the large prison population, may facilitate transmission and hamper the adoption of social distancing. In addition, the large proportion of informal workers means that policies of social protection and support for vulnerable segments of the population will have to be instituted to guarantee the sustainability and effectiveness of COVID-19 containment measures. Minimum income guarantees for the entire population, as well as policies that guarantee the jobs of those in the formal job market, are crucial in ensuring the survival of individuals, particularly, but not exclusively, while measures are in place that restrict economic activities.

Finally, it is vital to strengthen the surveillance system at all three levels of the National Health Service. This includes: developing indicators with which to evaluate the progression of the epidemic; systematically disclosing notification data, separated by municipality and sanitary district; increasing testing capacity to identify asymptomatic, pre-symptomatic and symptomatic infected individuals, hospitalized cases and deaths resulting from COVID-19; precisely defining suspected and confirmed cases based on clinical and laboratory criteria; and continuously evaluating the implementation, effectiveness and the impact of control strategies. Only then will it be possible to provide data on which to base decision-making regarding the continuation of social distancing measures and the right moment at which to relax them.

Acknowledgments

JMP is funded by the NIHR Global Health Research Program. EMLA has a CNPq Research Productivity Scholarship.

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Publication Dates

  • Publication in this collection
    05 June 2020
  • Date of issue
    June 2020

History

  • Received
    18 Apr 2020
  • Accepted
    20 Apr 2020
  • Published
    22 Apr 2020
ABRASCO - Associação Brasileira de Saúde Coletiva Rio de Janeiro - RJ - Brazil
E-mail: revscol@fiocruz.br