The emergence of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the causative agent of 2019 coronavirus disease (COVID-19), has led to over 200,000 death/month globally in approximately 2 years (1). Deaths, hospitalizations, long-term sequela, and work absence are among the COVID-19-associated factors that have led to economic depression (2). Especially in low- and middle-income countries, such as Africa and Latin America, where budget constraints are constant and reinforced under economic uncertainties, science, and public health funding may become at risk. Indeed, the percentage of sequenced SARS-CoV-2 genomes among confirmed cases is lower in these countries than in wealthier nations (3, 4).

SARS-CoV-2 surveillance has been built on influenza monitoring networks (5). In brief, State laboratories share samples from syndromic patients (under different levels of assistance, from immediate attention to deceased patients) with National Influenza Centers (NIC), which subsequently consolidate with World Health Organization (WHO) Collaborating Centers (CC) the variants to be prioritized for regular vaccine updates and pandemic preparedness. However, besides this standard surveillance component, SARS-CoV-2 has led to extra caution in workplaces to avoid COVID-19 (6), differently than any other emerging pathogens. In the occupational environment, SARS-CoV-2 testing is a powerful approach in providing valuable information to decision-makers to adopt measures to mitigate the spread of the virus, preserving a healthy workplace and productivity.

Thus, SARS-CoV-2 pandemics imposed a necessity that occupational health programs adapt to organize and implement the early identification of workers with SARS-CoV-2 positive diagnosis (6) and even vaccine advocacy. Nevertheless, the natural history of COVID-19 is challenging because asymptomatic and pre-symptomatic patients may impose a risk of virus spread among co-workers (7). In companies with an implemented occupational health system, routine systematic testing of workers, regardless of their symptoms, could provide recommendations for self-quarantine, avoiding SARS-CoV-2 spread, and better monitoring the clinical evolution of COVID-19.

As SARS-CoV-2 spilled over in the wet market in Wuhan, China, workers from there were among the very first patients with COVID-19, including the most likely patient “zero” (8). Apparently, in this market, two independent episodes posed the risk of SARS-CoV-2 spillover from animals to human (9), reinforcing the notion that this workplace was endowed with substantial risk for the emergence of new viruses. Although ‘pneumonia of unknown origin' was the diagnosis assigned to the initial patients who underwent hospitalization, COVID-19 hospitalization was necessary in 5–7% of the initial cases, meaning that occupational health surveillance in Wuhan's wet market could have identified SARS-CoV-2 among the other 95–93% of persons with asymptomatic or mild symptoms (8) and allowed earlier contingency of the very first infected individuals. Although the wet market was most likely the epicenter of the virus spillover, other workplaces with lower risks of virus emergence also contribute to SARS-CoV-2 chains of transmission (10, 11).

SARS-CoV-2 surveillance must be a priority to properly represent viral genetic diversity within a community. Beyond regular surveillance, occupational health can readily provide opportunities for early detection. SARS-CoV-2 pathogenesis and ability to escape the humoral immune response may vary among the variants of concern (VoC) (12), making it necessary to effectively and efficiently identify COVID-19 clusters to categorize the viral lineages. Indeed, the Gamma, Delta, and Omicron VoCs emerged from uncertain origins (13–15). Thus, every opportunity to catalog SARS-CoV-2 genetic diversity should be taken to fulfill the phylogenetical and epidemiological puzzle imposed by this virus. Among these opportunities, the integration of occupational health and SARS-CoV-2 surveillance has been proposed (16). Still, it has never been tested whether programs in workplaces have the sensitivity to detect variants and lineages with similar trends as regular “influenza-like” surveillance programs.

In Rio de Janeiro, Brazil, centralized infrastructures support social and health programs for industries and other entrepreneurial activities (National Industrial Apprenticeship Service, SENAI; and Industry Social Service, SESI). From September 2020 to May 2021, the SESI Innovation Center for Occupational Health has supported industrial and service companies in this State to implement and perform the detection of SARS-CoV-2 through RT-PCR (17). From May 2021 forward, SARS-CoV-2 genome sequencing was implemented to reinforce the molecular surveillance associated with occupational health. Therefore, we evaluated the SARS-CoV-2 genetic diversity in workers from Rio de Janeiro and correlated these findings to those from regular surveillance programs.

Brazil and other Latin American countries struggle to combat COVID-19, including limitations to access diagnosis, intensive care units, and vaccines. Consequently, overcrowded megalopoleis, such as the City of Rio de Janeiro, have a case-fatality ratio of 7.1%, almost two times higher than its State and Country (26, 27). If the City or State of Rio de Janeiro were a country, it would fit among the three regions with the highest death rates in the world (1). Nevertheless, the percentage of sequenced SARS-CoV-2 genomes per confirmed case is low in Brazil, 0.3 genomes per 1,000 confirmed cases (4, 28). Given that Brazil has more representative sequences deposited in GISAID than any other South American country, other Latin American countries struggle to catalog the SARS-CoV-2 genetic diversity (4, 28). In Brazilian studies analyzing circulating SARS-CoV-2 variants using health surveillance programs, only a small subset of samples, around 1%, were sequenced (14, 29). In low- and middle-income countries, which are overwhelmed by the COVID-19 pandemic, most of the resources in public health are consumed by patient assistance, leaving a limited budget for disease prevention and prediction through continuous surveillance.

COVID-19 severely impacted Brazil (1), and, despite the limitation of cataloging only a subset of virus genomes, the pangolin lineages B.1.1.28 and B.1.1.33 are the most representative (Dashboard—Genomahcov—Fiocruz). The Gamma VoC also evolved from the B.1.1.28 lineage (14). The introduction of B.1.1.28 and B.1.1.33 likely occurred early in 2020, which overlaps with the Brazilian Carnival (30, 31), when no specific lockdown or self-quarantine measures were implemented. Stochastic events are thus not only associated with SARS-CoV-2 spillover from animal to humans (8) but also with virus dissemination. The SARS-CoV-2 spillover was associated with occupational risk for the workers at the wet market in Wuhan (8). When surveillance programs based on symptomatic patients identified the first cases of SARS-CoV-2, over 90% of asymptomatic or mildly affected individuals were likely circulating (8). Therefore, routine testing becomes an important tool to communicate public health surveillance systems early.

Our data points out that companies with implemented occupation health surveillance for COVID-19 may have an adequate and timely opportunity to increase awareness of the genetic diversity of circulating strains of SARS-CoV-2. Indeed, it has been proposed that occupational health should be an integral component of the response to COVID-19 (6, 16). Still, it is here that we document the experience from Rio de Janeiro, where a centralized Center for Occupational Health has reduced the dependence on governmental funding to catalog SARS-CoV-2 genetic diversity and find VoC with similar trends to a regular surveillance system. By sequencing representative samples, around 20%, from a cohort with characteristics than those on regular SARS-CoV-2 genomic surveillance networks, we even found: i) the primo-identification of the B.1.139 and A.2.5 viral genomes in Brazil; and ii) an improved dating of Delta VoC evolution, by identifying earlier cases of associated with AY-related genomes. We interpret that SARS-CoV-2 molecular testing of workers, independently of symptoms, has allowed an earlier opportunity to identify variants than regular health surveillance programs. These regular programs are primarily dependent on the spontaneous demand of syndromic patients and the cataloging of viral genetic diversity from hospitalized and deceased individuals, which may take weeks after the onset of illness to be identified.

With the emergence of variants that escape the humoral immune response (12), companies must continuously monitor their workers for SARS-CoV-2. Under the auspicious of this investigation, we interpret that SARS-CoV-2-positive samples from occupation health programs should be considered as necessary as those from regular health surveillance programs to expand our awareness knowledge on virus genetic diversity and VoC emergence. We propose continuously performing occupational health surveillance to screen for other communicable diseases and identify possible chains of transmission.

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found in the article in the legend of Figure 1 and the Supplementary Material.

The studies involving human participants were reviewed and approved by National Committee of Research Ethics and by the Ethics Committee of Hospital Universitário Clementino Fraga Filho under protocol number 4,317,270. The patients/participants provided their written informed consent to participate in this study.

SK and AF-N coordinated the cohort. BF, BM, AC, and JG performed the sequencing. JA, JG, and TS analyzed the data. SK, AF-N, and TS conceptualized the study. All authors prepared the manuscript.

Funding was provided by Industry Federation of Rio de Janeiro (FIRJAN), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES)-Finance Code 001. CNPq, CAPES and FAPERJ also support the National Institutes of Science and Technology Program (INCT-IDPN, 465313/2014-0).

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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