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Seroprevalence of anti-SARS-CoV-2 IgG at the first epidemic peak in French Guiana, July 2020

['Claude Flamand', 'Epidemiology Unit', 'Institut Pasteur In French Guiana', 'Cayenne', 'French Guiana', 'Mathematical Modelling Of Infectious Diseases Unit', 'Institut Pasteur', 'Cnrs', 'Paris', 'Christelle Alves Sarmento']

Date: 2022-01 

Abstract Background While Latin America has been heavily affected by the pandemic, only a few seroprevalence studies have been conducted there during the first epidemic wave in the first half of 2020. Methodology/Principal findings A cross-sectional survey was performed between 15 July 2020 and 23 July 2020 among individuals who visited 4 medical laboratories or 5 health centers for routine screening or clinical management, with the exception of symptomatic suggestive cases of covid-19. Samples were screened for the presence of anti-SARS-CoV-2 IgG directed against domain S1 of the SARS-CoV-2 spike protein using the anti-SARS-CoV-2 enzyme-linked immunosorbent assay (ELISA) from Euroimmun. Conclusions/Significance The overall seroprevalence was 15.4% [9.3%-24.4%] among 480 participants, ranging from 4.0% to 25.5% across the different municipalities. The seroprevalence did not differ according to gender (p = 0.19) or age (p = 0.51). Among SARS-CoV-2 positive individuals, we found that 24.6% [11.5%-45.2%] reported symptoms consistent with COVID-19. Our findings revealed high levels of infection across the territory but a low number of resulting deaths, which can be explained by French Guiana’s young population structure.

Author summary While Latin America has been heavily affected by the pandemic, only a few seroprevalence studies have been conducted there during the first epidemic wave in the first half of 2020. A cross-sectional survey was performed between 15 July 2020 and 23 July 2020 among individuals who visited 4 medical laboratories or 5 health centers for routine screening or clinical management, with the exception of symptomatic suggestive cases of covid-19. Samples were screened for the presence of anti-SARS-CoV-2 IgG using the anti-SARS-CoV-2 enzyme-linked immunosorbent assay (ELISA) from Euroimmun. The overall seroprevalence was 15.4% [9.3%-24.4%] among 480 participants, ranging from 4.0% to 25.5% across the different municipalities. The seroprevalence did not differ according to gender (p = 0.19) or age (p = 0.51). Among SARS-CoV-2 positive individuals, we found that 24.6% [11.5%-45.2%] reported symptoms consistent with COVID-19. Our findings revealed high levels of infection across the territory but a low number of resulting deaths, which can be explained by French Guiana’s young population structure.

Citation: Flamand C, Alves Sarmento C, Enfissi A, Bailly S, Beillard E, Gaillet M, et al. (2021) Seroprevalence of anti-SARS-CoV-2 IgG at the first epidemic peak in French Guiana, July 2020. PLoS Negl Trop Dis 15(11): e0009945. https://doi.org/10.1371/journal.pntd.0009945 Editor: Natalie Bowman, University of North Carolina at Chapel Hill School of Medicine, UNITED STATES Received: October 12, 2020; Accepted: October 22, 2021; Published: November 12, 2021 Copyright: © 2021 Flamand et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability: Data are from the EPICOVID19 study belonging to Institut Pasteur, 25 rue du Docteur Roux 75724 Paris Cedex 15 France. Access to data is restricted for legal reasons according to the French CNIL recommendations (Commission Nationale Informatique et Libertes) that require specific authorizations to transfer health individual data from one center to another. The data may be made available after obtaining approval from the French regulatory authority: CNIL, Commission Nationale Informatique et Libertes, 3 Place de Fontenoy TSA 80715 75334 PARIS CEDEX 07, France. Phone (33): 01 53 73 22 00. Request from data transfer can be sent to Clinical Core of the Center for Translational Science of Institut Pasteur, Paris, Tel: + 33 (0) 1.40.61.38.74; Fax: + 33 (0) 1.40.61.39.77; https://research.pasteur.fr/en/team/clinical-core/. Funding: This study was supported by the National Research Agency to CF, the “European Regional Development Fund” (GY0027257) to CF, the “Regional Health Agency of French Guiana” to CF and the « URGENCE COVID-19 » fundraising campaign of Institut Pasteur to CF. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist.

Introduction The world’s attention remains focused on the spread of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), that causes coronavirus disease 2019 (COVID-19), and the implementation of drastic control measures to limit its expansion. By the end of July 2020, more than 17 million confirmed cases and approximately 650,000 deaths have been reported worldwide [1]. With more than 4,500,000 cases and 190,000 deaths, Latin America has been particularly affected by the crisis [1]. A thorough evaluation of the proportion that has already been infected by SARS-CoV-2 and is likely immunized is important to estimate the level of herd immunity of the population [2] and to inform public health decision making. Data on laboratory molecular -confirmed cases do not capture the full extent of viral circulation because a majority of infected individuals have asymptomatic or mild infections and may therefore not seek care [3,4]. In contrast, population immunity is typically estimated through cross-sectional surveys of representative samples using serological tests. Numerous serological surveys were conducted in affected countries during or at the end of the first COVID-19 epidemic wave [5]. Most of the serological studies already available in July 2020 have been carried out in continental Europe [6–12] and in the United States [13–16]. Although Latin America has been heavily affected by the pandemic, only a few seroprevalence studies have been conducted across the continent, meaning the underlying level of infection remains largely unknown [5,17,18]. French Guiana, a French overseas department with 290,000 inhabitants [19], located in Latin America in the Amazonian forest complex experienced a large SARS-CoV-2 epidemic wave. A territory-wide lockdown was set up from March 17th 2020 concomitantly with the rest of French territories, at a time when five imported cases and one secondary case were being confirmed on the territory [20]. The lockdown resulted in limited viral transmission until it was ended on May 11th 2020. In the middle of June there was a rapid intensification of viral circulation over a large part of the territory with 917 confirmed cases of COVID-19 detected from March 4th 2020 to June 11th 2020 [21]. This was followed by the implementation of strict mitigation measures such as curfews and local lockdowns in the course of June and July. The epidemic peaked at the beginning of July with 4,440 cumulative confirmed cases [22], followed by a gradual slowing down throughout the territory. Between March 4 and September 17, 9,623 cases (3,310 per 100,000 inhabitants) of COVID-19 and 65 hospital deaths (22.3 per 100,000 inhabitants) of COVID-19 were detected in French Guiana [23]. As the disease severity is reduced in younger individuals [24], we can suspect that many infections are likely to have been missed in this territory which has a much younger population (mean age of 25,1 versus 32,1 for Latin America and 42,3 for mainland France) [19]. In order to understand the underlying level of infection, we conducted a cross-sectional study within the general population, estimated the seroprevalence of SARS-CoV-2 and assessed its distribution in age groups and geographical areas.

Discussion We report the first serosurvey for the detection of SARS-CoV-2 antibodies in French Guiana. We found that 15.4% [9.3%-24.4%] of the population was seropositive two weeks after the peak of the first epidemic wave. Assuming a two or three-week delay for seroconversion, our estimation reflects the level of infection of the population at the end of June or beginning of July, which roughly corresponds to the epidemic peak. Our results indicate that by that time, at least 44,660 [26,970–70,760] of French Guiana’s 290,000 population had been affected by the virus, more than 10 times the official count of 4,440 confirmed cases reported by public health surveillance system by the first week of July [22]. Various investigators have shown that seroprevalence levels in South American populations during the first epidemic wave were much higher than those reported in European cities and countries [30]. It appeared in countries such as Peru, Colombia, Argentina and Brazil, that the highest values came from low-income populations. The relationship with poverty has already been demonstrated in different studies [30]. In Brazil, one of the bordering countries in French Guiana, seroprevalence estimates varied markedly across the country’s cities and regions, from below 1.0% in most cities in the south and center-west regions to up to 25.0% in the city of Breves in the Amazon (North) region [17]. Nevertheless, overall seroprevalence was estimated at 1.4% (95% CI 1.3–1.6). In contrast, our findings highlighted high but also relatively homogeneous levels of infection in most municipalities, ranging from 10% to 20%. The case fatality rate of COVID-19 was low during the outbreak as there were 65 COVID-19 related deaths from the beginning of the outbreak up to September 17 [23] across the territory while about 45,000 people have been infected at the beginning of July. This was probably due in part to the young age of the population of French Guiana. Younger populations are likely to have more social ties than older populations, and therefore physical distancing may be more difficult to implement than in countries with ageing populations. Furthermore, since young people are less susceptible to disease severity, they may be less likely to adopt physical distancing measures when they are infected and potentially contagious in a context of high level of transmission [31]. Seroprevalence was higher in men than in women (19.6% versus 10.4%), which could reflect a different exposure potentially related to a greater number of contacts and exposure situations in men than in women but this difference was not significant in our study. Although several population-based studies have demonstrated differences in seroprevalence rates between male and female subjects, most of them indicate that seroprevalence does not differ significantly between men and women [32]. Our study has several limitations inherent in the study design. Our approach made it possible to obtain rapid estimates of the impact of the epidemic. However, convenience sampling may result in a lack of population representation if part of the general population has lower access to the laboratories and health centers participating in the study. In our study, we observed a significant under-representation of men and children under 15 years of age, related to the structure of the population typically visiting laboratories and health centers, and therefore performed a post-stratification adjustment. However, this may have led to large confidence intervals for some of parameter estimates. In addition, sample size calculation was determined to obtain a sufficient point estimate of territory-wide prevalence estimates but not to study risk factors of infection. A few municipalities with no laboratory or health centers were not represented. However, the municipalities represented by the laboratories and health centers involved in the study are home to 90% of the population, so that our estimates are likely a good reflection of the situation across the territory. We may underestimate infection levels if precarious populations are at higher risk of infection and have limited access to health facilities. Furthermore, it is also possible that sampled individuals who were routinely monitored for pregnancy or chronic health problems took more precautions and reduced their exposure to the virus. Although it is difficult to assess the representativeness of the sample, the relatively easy access to health care and diagnostic facilities in Guyana, particularly in the larger population centers represented in our study, may have limited coverage bias. Additionally, it is possible that infected people did not develop specific SARS-CoV-2 antibodies or that these antibodies were not detected by our assay. Since the study was performed shortly after the peak of the epidemic, a proportion of individuals infected at the peak may not have seroconverted by the time of sample collection. With the exception of anosmia, which is already known as a common and distinctive features of SARS-CoV-2 infection [33,34], symptoms were not significantly more frequently reported by seropositive than seronegative individuals. In conclusion, we found that at least 15.4% of the population in French Guiana was infected by SARS-CoV-2 by the time the epidemic peaked in July. Our estimates are close to the infection attack rate of SARS-COV-2 of 17.6% [17.2%, 18.0%] estimated in a recent modeling study conducted to characterize the epidemic dynamics and to evaluate the impact of control measures that were implemented to contain the epidemic in French Guiana [35]. This corresponds to an elevated infection burden given the relatively limited mortality, which can be explained by French Guiana’s young population structure.

Acknowledgments We are grateful to all field workers, collaborators, technical and medical staff from Health Centers Department of Cayenne Hospital Center and biological laboratories and health centers involved in the EPI-COVID-19 project. We thank Bhety LABEAU, David MOUA, Laetitia BREMAND, Sylvie ALOEPOE, Elisabeth CHAN from Institut Pasteur in French Guiana, Nathalie JOLLY from Clinical Core of the Center for Translational Research of Institut Pasteur. We also thank Sophie GAULIN, Lysiane ROMAIN, Véronique TOGNERI and Tadens MPWENE from La Liberté.

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