Seroprevalence and lethality by SARS-CoV-2 in indigenous populations of Latin America and the Caribbean: a systematic review

Introduction

Since the detection of the first case of SARS-CoV-2 in Wuhan, China, in 2019, the propagation of this virus has increased until being declared a pandemic on the 11th of March 2020 (World Health Organization, 2019). The most common mode of transmission is through respiratory droplets and prognosis of the patient depends on several factors including age, severity of disease presentation, comorbidities and response to treatment (Zhou et al., 2021). One of the groups most vulnerable to SARS-CoV-2 is the indigenous population due to the presence of social determinants at an individual, community, and societal level that condition lower health quality. These include higher levels of poverty, malnutrition, lower levels of education, poor access to essential sanitation services, difficulties accessing health care services due to geographical and cultural barriers, and low availability of adequately equipped health care establishments (McLeod et al., 2020; Charlier & Varison, 2020; United Nations, 2021). Likewise, immunological factors and chronic diseases have been reported to increase the susceptibility to infectious disease outbreaks in this group of people (Gelaye et al., 2020). A negative effect on the health status of indigenous people has been described in recent decades due to these diseases with lethality up to six times that found in the general population (McLeod et al., 2020; La Ruche et al., 2009; Food and Agriculture Organization, 2020).

Latin America and the Caribbean (LAC) has presented some of the highest numbers of cases and deaths due to COVID-19 in the world (Johns Hopkins University, 2021). The first regional case of SARS-CoV-2 infection was reported in February 2020 in Brazil, while the first death due to COVID-19 was reported in Argentina in March (Rodriguez-Morales et al., 2020). In LAC, there are over 800 indigenous communities, and together they account for approximately 60 million people, representing 8% of the total population. Thus, LAC presents the highest proportion of indigenous people compared to other inhabitants (United Nations Office for the Coordination of Humanitarian Affairs, 2020). Indigenous populations have conditions that make them vulnerable to the COVID-19 pandemic. These conditions include high levels of poverty, which affect 43% of indigenous households, an average salary 31% lower than that of other workers and lower levels of education with reports indicating that only 20% of indigenous populations obtain conventional education and lower access to health care (United Nations, 2021; United Nations Office for the Coordination of Humanitarian Affairs, 2020). It was to be expected that these historical inequalities would increase during the COVID-19 pandemic, causing indigenous people to be left behind when distributing scarce resources, such as diagnostic tests, personal protective equipment, mechanical ventilators, and medication necessary for the treatment of critically ill patients (United Nations, 2021; Food and Agriculture Organization, 2020), being a scenario that increases the risk of severe disease and death in this group. Thus, tending to the needs of indigenous populations in LAC continues to be a challenge and has been made even greater due to the current events of the pandemic.

To date, an ever-growing number of COVID-19 cases has been reported in all LAC countries (Johns Hopkins University, 2021), including cases among indigenous people in this region (United Nations Office for the Coordination of Humanitarian Affairs, 2020; Pan American Health Organization, 2021a). Regardless, the presence and the impact of the COVID-19 pandemic on mortality in indigenous populations of LAC have seldom been studied. Thus, we carried out a systematic review to estimate the seroprevalence and lethality attributable to COVID-19 in indigenous populations of (LAC). This information could serve as evidence to generate strategies oriented towards better allocation of health resources in this population.

Methods

This systematic review was registered in the PROSPERO database (registration code: CRD42020207862) and reported using the guidelines of the Meta-analysis of Observational Studies in Epidemiology (MOOSE) (Stroup et al., 2000) and Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statements (PRISMA, 2015).

Results

Search results

We obtained a total of 747 unique results from the search after eliminating duplicates. After revision by title and abstract, 26 full-text articles were read. Following evaluation, one study was found to be an editorial, and 10 did not provide data on indigenous people, and were, thus, excluded. In the end, 15 studies complied with the inclusion criteria and are reported below (Fig. 1).

Discussion

This systematic review aimed to summarize the evidence available on the seroprevalence and lethality of infection by SARS-CoV-2 in the indigenous populations of LAC. Only a few non-representative studies measuring outcomes of COVID-19 in the indigenous people of LAC countries were available. In general, only three Latin American countries (Brazil, Mexico, and Colombia) have studied and reported data on seroprevalence and lethality in indigenous populations, including studies at community (12/15) and hospital levels (3/15). Likewise, only 12 studies were designed to evaluate the lethality of COVID-19 in the indigenous population (eight in Brazil). In general, the studies found had a cross-sectional design. The seroprevalence of SARS-CoV-2 was only reported in the indigenous population of Brazil, with values between 4.2 and 81.65%. Regarding lethality, higher values were reported in studies carried out in hospital settings (19.9% to 53.33%) compared to those conducted in a community setting (0% to 48.74%).

Regarding the seroprevalence of indigenous populations, the studies identified only evaluated the Brazilian indigenous population using small sample sizes; the study with the largest sample reported a seroprevalence of 5.4%. After reviewing the available literature, we found that there is also scarce information regarding the seroprevalence of SARS-CoV-2 in the indigenous populations of other regions of the world. One study in the indigenous population of Alaska reported that the prevalence of SARS-CoV-2 infection reached 1.3% (Hatcher et al., 2020), a value within the range found in studies in the indigenous population of Brazil reported in this review. We emphasize that Brazil is one of the countries with the highest number of cases of COVID-19 in the world (3^rd place), with approximately 19 million cases by July 2021 (Johns Hopkins University, 2021). Studies presenting results regarding the seroprevalence of SARS-CoV-2 in other LAC countries were not found. However, in countries such as Bolivia (Fondo para el Desarrollo de los Pueblos Indígenas de América Latina y el Caribe, 2020a), Peru (Centro Nacional de Epidemiología Prevención y Control de Enfermedades, 2021), Ecuador (Castro, 2020), Venezuela (Pan American Health Organization, 2021b), and Colombia (Organización Panamericana de la Salud, 2020), cases of COVID-19 have been reported in the indigenous populations. During the COVID-19 pandemic, a deficit of diagnostic tests, lack of masks, and the suspension of health programs in indigenous communities have been described (Reinders et al., 2020), being a situation that could lead to a decline in health care in these communities as well as an underestimation of the prevalence of COVID-19 in indigenous populations. Thus, health care for this historically vulnerable group should be prioritized during times of crisis. Additionally, given that most countries report official information on COVID-19 without disaggregating it according to ethnicity (Fondo para el Desarrollo de los Pueblos Indígenas de América Latina y el Caribe, 2020b), it is necessary to overcome the deficiencies in the data recording process to evaluate the impact of COVID-19 or other diseases in indigenous communities.

Regarding lethality, differences were found among the studies evaluating the Brazilian population (23% and 53.3% in the hospital setting; 0% to 48.74% in the community setting) and the Mexican population (19.9% in the hospital setting). The difference in the lethality among the studies reported and the fact that higher lethality has been reported in hospital settings could be due to indigenous patients with more severe forms of COVID-19 being concentrated in the hospital setting, raising the lethality due to COVID-19 among the patients that received medical care in a hospital setting. Until July 13th, 2021, Brazil (534,233) and Mexico (235,058) reported two of the highest numbers of deaths due to COVID-19 worldwide (second and fourth place, respectively) (Johns Hopkins University, 2021). Regarding the number of COVID-19 cases in these countries, the lethality due to COVID-19 in the general population in Mexico is the highest in the world with 9.06%, being 2.80% in Brazil (Johns Hopkins University, 2021). Similar to the outcomes of seroprevalence of SARS-CoV-2, we found no study on lethality due to COVID-19 in other countries of LAC. Nevertheless, deaths due to COVID-19 in the indigenous population of other Latin American countries such as Bolivia, Peru, Colombia, and Ecuador show hundreds of deaths due to COVID-19 in indigenous communities (Fondo para el Desarrollo de los Pueblos Indígenas de América Latina y el Caribe, 2020a; Castro, 2020; Organización Panamericana de la Salud, 2020; Fondo para el Desarrollo de los Pueblos Indígenas de América Latina y el Caribe, 2021). The trust for the development of indigenous communities in LAC stated that by December 2020 over 73,000 cases of COVID-19 and 21,000 deaths had been reported among indigenous communities of the amazon region. Many of these communities were already vulnerable due to poor levels of sanitation and dependence on income from daily manual labor, and many were left to fend for themselves due to being geographically isolated opting to turn towards traditional medicine as a means of combatting illness (Fondo para el Desarrollo de los Pueblos Indígenas de América Latina y el Caribe, 2021). Considering the potential sub-registration of cases and deaths due to COVID-19 in these countries, the predisposition of indigenous populations, and limitations in the availability of diagnostic tests, COVID-19 may be an important cause of mortality in indigenous people.

To date, international organizations such as the Pan American Health Organization have required governments of LAC countries to implement measures to slow the spread of COVID-19 in indigenous communities, including increasing the number of health workers and medical supplies, as well as providing diagnostic tests for COVID-19 and vaccines and treatments for this disease when available (Pan American Health Organization, 2021a). The need to adopt emergency measures to protect this population was demonstrated in Brazil, where a supreme court (August 2020) exposed the Brazilian government’s failure to protect the indigenous population from the impact of COVID-19 after an indigenous leader had died from this disease (Álvares, 2021). It should be noted that in countries with indigenous communities in the Amazon area, including Brazil, Colombia, and Peru, the presence of illegal extractive activities generates a great environmental and direct impact on the health of these communities by exploiting the resources used for their subsistence and requiring them to move from their territory, likely facilitating the introduction and spread of COVID-19 (Villén-Pérez et al., 2020; Langlois, 2020; Swenson et al., 2011). Regarding the previous issue, the Brazilian court also pointed out the need to expel illegal gold miners from protected areas (Álvares, 2021). Therefore, it is urgent that governments take measures to control activities that could introduce COVID-19 and cause environmental impacts that affect the health of indigenous communities.

Indigenous communities have taken an active role in their protection against COVID-19. In LAC, for example, it is described that indigenous communities in Brazil, such as Paiter Suruí and Parque Ingidena do Xingu established voluntary quarantines in March 2020 (Charlier & Varison, 2020). Furthermore, in Peru, it has been described that the majority of the communities of the rural districts Nauta, Parinari, and Sequena prohibited the entry of people not belonging to the community. However, half of these communities did allow residents to travel to the cities for commercial and social reasons, and the prohibition of social events was only abided by a third of the communities since the control measure, decreed by the Peruvian government, competes with their daily routine (Reinders et al., 2020). Although it is described that the measures taken by governments to control the spread of COVID-19 towards indigenous communities have been deficient (Fondo para el Desarrollo de los Pueblos Indígenas de América Latina y el Caribe, 2020b), it should be emphasized that mistrust in authority and disbelief in the existence and severity of the pandemic likely influenced outcomes (Fondo para el Desarrollo de los Pueblos Indígenas de América Latina y el Caribe, 2020b; Meneses-Navarro et al., 2020). Therefore, effective, culturally appropriate communication strategies with the communities should be established to transmit accurate information about COVID-19 (Meneses-Navarro et al., 2020). These strategies should also include the participation of community representatives (United Nations Office for the Coordination of Humanitarian Affairs, 2020; Fondo para el Desarrollo de los Pueblos Indígenas de América Latina y el Caribe, 2020b). Authorities could also establish differentiated lockdowns according to the number of individuals affected by COVID-19 in the indigenous communities to reduce the impact in the activities of these populations.

This review has some limitations. Although we sought to be comprehensive in terms of information sources, including a regional bibliographic database such as LILACS as well as a search engine such as Google Scholar and including documents in the main languages of the LAC countries, there may be publications in the gray literature on the study subject that would not have been collected as they were not indexed in the information sources used. Likewise, we found few studies from few LAC countries examining COVID-19 in the indigenous population. Also, there were limitations regarding the information provided in the studies evaluated; for example, in some cases, no information on the recruitment criteria of the participants or type of test used to detect positive SARS-CoV-2 cases was available. Furthermore, there is variability in the reporting of results, which did not allow a meta-analysis to be carried out. Despite this, being that this study is the first systematic review to summarize the evidence available on the seroprevalence and lethality of SARS-CoV-2 infection in the indigenous population of LAC, we consider that the use of a search strategy with exhaustive key terms allowed an adequate approach to the problem under study.

Conclusions

In conclusion, this systematic review found that there is limited evidence on the seroprevalence and lethality of SARS-CoV-2 in the indigenous population of LAC. The few studies identified described the presence of COVID-19 in indigenous people of Brazil, Mexico, and Colombia. COVID-19 is a cause of death in these LAC indigenous populations, although there were differences in the lethality reported in hospital and community settings during the pandemic. In order not to leave anyone behind, future investigations with a prospective design should aim to use standardized methods that allow comparability among the studies of seroprevalence and lethality of SARS-CoV-2 in this population, this data should be made readily available to allow evaluation of the true impact of COVID-19 in indigenous people, who have historically had inequality in access to medical care.

Supplemental Information