key: cord-0258879-xgps35cg
authors: Malagon-Rojas, J. N.; Mercado-Reyes, M.; Toloza-Perez, Y. G.; Parra, E. L.; Palma, R. M.; Munoz, E.; Lopez, R.; Almentero-Correa, J. E.; Rubio, V. V.; Ibanez-Pinilla, E. A.; Tellez-Avila, E. M.; Delgado, G.; Jimenez-Forero, C. P.; Viasus, D.; Galindo, M.; Lagos, L. F.
title: Seroprevalence of the SARS-CoV-2 antibody in healthcare workers: a multicenter cross-sectional study in ten Colombian cities.
date: 2021-07-22
journal: nan
DOI: 10.1101/2021.07.21.21260103
sha: 48019f1acbfc8622024268ca77d440a10b1eccdb
doc_id: 258879
cord_uid: xgps35cg

Background: SARS-CoV-2 affects mainly occupational health populations. Healthcare workers are at constant risk of infection. The objective of this study was to determine the seroprevalence of SARS-CoV-2 in healthcare workers in Colombia. Methods: This study is a cross-sectional study focused on estimating the seroprevalence of SARS-CoV-2 antibodies in healthcare workers from 65 hospitals in 10 cities of Colombia during the second semester of 2020. The seroprevalence was determined using an automated immunoassay (Abbott SARS-CoV-2 CLIA IgG). The study included a survey to establish the sociodemographic variables and the risk of infection. Results: The global seroprevalence of antibodies against SARS-CoV-2 was 35% (95% Bayesian Confidence Interval 33%-37%). All the personnel reported the use of protective equipment. General services personnel and nurses presented the highest rates of seroprevalence among the healthcare workers. Low socioeconomic strata have shown a strong association with seropositivity. Conclusion: This study shows the occupational risk for SARS-CoV-2 infection among healthcare workers. Even though, all the personnel reported the use of protective equipment, the seroprevalence in the general services personnel and nurses was high. Also, it was observed a significant difference by city. The results could be used to perform prevention and control in this exposed population. However, further investigation of these is required to inform sources of infection to improve the control and occupational health practices.

Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) has generated multiple and diverse challenges worldwide in all areas of work. One of the work environments that has attracted the most attention is the provision of health services, given the relevance of health care workers (HCWs) and their role during the pandemic. HCWs possibly have the highest exposure and risk of infection because they are in direct contact with infected patients. The World Health Organization (WHO) estimates that around 14% of reported COVID-19 cases correspond to HCWs even reaching 35% in some countries [1] . By September 2020 in the Americas region, almost 570,000 HCWs were reported with COVID-19, in addition to 2,500 deaths from SARS-CoV-2 [2]. Around the world, it is estimated that the COVID-19 infections among this specific group ranges between 1% and 45.3%, being higher in countries from the North hemisphere [3] [4] [5] [6] [7] [8] [9] [10] . It was indicated that HW's who are male, from ethnic minorities resulted in a higher seroprevalence levels [11] .

To the 1 st July 2021, nearly 4.4 million cases and more than 110,000 COVID-19 related deaths have been reported in Colombia [12] . The country has experienced three peaks: the former between July and August 2020, the second between December 2020 and January 2021 and the last one between April and June 2021. The average effective reproductive number -R0-for the Country during 2020 was 1.09, while the estimated average R0 between January and July 2021 is 0.92 [12] . During the lockdown period, the health system increased its capability of Intensive Care Units -ICU-bed number and boosted health care worker's response and the number of labs able to carry out RT-PCR in the country.

Since the pandemic declared by the WHO began in March 2020 [13] , various active surveillance strategies have been implemented, such as self-reporting of symptoms through mobile applications, the usage of RT-PCR tests regularly, and performing serological tests to the identification of antibodies against SARS-CoV-2 [14] . Due to the costs of surveillance strategies through the identification of nucleic acids, this type of intervention has been poorly adopted among health institutions. Given that up to 50% of SARS-CoV-2 cases correspond to asymptomatic infections [15] , the incidence of SARS-CoV-2 cases based on the notification of confirmed SARS-CoV-2 cases implies a considerable underestimation of the incidence of this virus infection [16] . In this sense, the carrying out of studies allowed us to estimate the proportion of HCWs who have antibodies against SARS-CoV-2. Besides, this type of analysis also provides information about the immune response to the virus, natural susceptibility, as well as useful information when prioritizing the application of the vaccine.

Healthcare workers are the most exposed to the risk of infection with the new SARS-CoV-2. This study aimed to determine the seroprevalence of antibodies against SARS-CoV-2 among HCWs in Colombia, along with describing the associations between seroprevalence and occupational exposure to SARS-CoV-2 in ten Colombian cities.

This study was a cross-sectional of health care workers across medical services in ten cities of Colombia from September to November 2020. The study was designed following the recommendations from the Strobe Statement for observational studies [17] .

A cross-sectional study with non-probability sampling was designed in health workers from public and private hospitals in 10 cities in Colombia. To calculate the sample size, an expected seroprevalence of 30% (p = 0.30), (q = 1-0.30 = 0.70) was taken with a marginal sampling error of ± 2% (δ = 0.02) and a confidence level = 95 % (α = 0.05, Zα = 1.96). A 10% loss percentage was stablished to calculate a minimum sample size of 2,241 participants. We used the definition of HW designated by the WHO providers of health care attention [18] . The public and private hospitals (IPS) were chosen using the municipal records, choosing the clinical and hospitals who concentrated 80% of the attention of COVID-19 cases in the municipality. Health workers were invited to participate through the personnel office. Participants in the study were selected from a list of voluntaries in each IPS. The selection was performed using a random number generator in Excel®. We included personal either directly or indirectly involved in the health care attention: doctors, nurses, pharmacists, physiotherapists, respiratory therapists, bacteriologists, health care technicians, admission assistants and even general services (catering and cleaning staff) and security personnel [18] .

Serum samples obtained from 6-7 ml of venous blood were collected. Samples were refrigerated and transported to a local laboratory. Later, samples were centrifuged to separate the serum and were stored at -30 ° C to -80 ° C until processing. The detection of total antibodies was made by the Chemiluminescence technique "SARS-CoV-2 Total (COV2T) Advia Centaur -Siemens". The Advia Centaur -Siemens test detects serum total antibodies against the SARS-CoV-2 virus. According to the manufacturer, the range of index values oscillates between 0.05 and 10 (cut-off point of reactive= >10).

The CLIA test was selected after performing a secondary validation with samples from the Colombian population. The sensitivity and specificity of the test were 86% (95% CI 79 -91) and 99% (95 CI 96 -100) respectively [19] .

An electronic questionnaire was applied online using Google Forms®. The questions were based on the guidelines from WHO [18] . The questionnaire included questions for sociodemographic characterization, usage of personal protective equipment, characterization of work conditions and dwelling, and previous exposure to COVID-19. Also, participants who declared having had COVID-19 were asked whether their insurance recognized their COVID-19 episode as being work-related.

A Spanish version of the questionnaire is available (Supplementary material 1). Five experts were asked to perform a virtual judgment to validate the content of the instrument [20] . The criteria included clarity, coherence, relevance, and sufficiency. The criteria were evaluated on a 1-5 scale by each expert. Finally, the questionnaire was validated by 300 health care workers from Bogota.

Sociodemographic characteristics of health care workers were described for each city. For the quantitative variables, means and standard deviation were estimated. Subsequently, a bivariate analysis was performed comparing the nominal or ordinal variables regarding the presence or absence of antibodies against SARS-CoV-2, analyzed using Pearson's chi-square test with Yates correction. In the case of quantitative variables, the Spearman correlation was used. The level of statistical significance established was p < 0.05. A Poisson regression model was applied to test the relationship between the results of the CLIA tests dependent variable and the theoretical variables. Associations were presented in Prevalence Ratios (PR) with 95% confidence intervals (CI). The statistical analysis was conducted using R (version 4.0.3). It was estimated the overall crude frequencies of seropositivity tests. Later, the crude seroprevalence was stratified by age, sex, ethnicity, and role at the IPS. For both cases, crude . CC-BY-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review)

The copyright holder for this preprint this version posted July 22, 2021. ; https://doi.org/10.1101/2021.07.21.21260103 doi: medRxiv preprint seroprevalence was adjusted using the Bayesian method in R 2.21.2 (pack RStan) [21] using the data of sensitivity and specificity reported in previous studies carried out using CLIA in Colombian populations [19] . Also, 95% Bayesian Credibility Intervals (BCI) were obtained.

The model was run according to the following equation:

Real Prevalence= Adjusted prevalence *Sensitivity + (1−Adjusted prevalence) * (1 − Specificity).

The study proposal and protocol were approved by the ethics committee of Instituto Nacional de Salud (CEMIN 012/2020). We have obtained written informed consent from each participant in the study.

A total of 4042 healthcare workers were included in the study in 65 health centers in 10 cities. The questionnaire was completed by 82% (n=3294) of the participants. The mean age was 36.45 ± 10.5 years old. Most of the participants belonged to socioeconomic strata two and three (63.4%). Most of the participants were nurses (34.9%) and general practitioners (10.1%). The distribution of participants by cities were Bogotá (n=677; 16.7%), Bucaramanga (n=508; 12.6%), Cali (n=500; 12.4%), Medellín (n=470; 11.6%), Barranquilla (n=434; 10.7%), Cucuta (n=423; 10.5%), Villavicencio (n=395; 9.8%), Ipiales (n=388; 9.6%), Leticia (n=176; 4.4%), and Guapi (n=71; 1.8%) ( Figure 1 ).

The prevalence of self-declared SARS-CoV-2 infection was 30.06% (95% CI 29.01% -32.22%; n=995). The percentage of workers who declared having been diagnosed with the PCR test was 89.54% (95% CI 87.49 % -91.3%; n=891). The proportion of seropositivity among the workers who declared the COVID-19 infection was 81% (95% CI 77.50%-84.0%). The proportion of workers who received legal recognition of COVID-19 infection as a work-related disease was 40.60% (95% CI 37.50% -43.70%; n=404).

. CC-BY-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted July 22, 2021. ; https://doi.org/10.1101/2021.07.21.21260103 doi: medRxiv preprint

The adherence to using protective equipment such as face masks (disposable surgical and N95) was 100% among HCW. It was observed that male participants tend to perform a lower number of protective elements (Chi 2 = 44.69, p = 0.00001). Participants who declared having been vaccinated against Influenza during the last year have a lower proportion of seroconversion than those who did not receive the vaccine (Chi 2 = 9.7425, p = 0.0001).

The global seroprevalence was 35% (95% BCI 33.0%-37.0%). The highest seroprevalence by cities was found in Guapi (71%), Villavicencio (54%), and Barranquilla (44%) ( Table 1 ). No significant difference was found between male and female HCWs concerning seropositivity. In the bivariate analysis, there was an association between the seroprevalence and occupation, age, socioeconomic strata, and educational level (p <0.05) ( Table 1 ). There was an association between seropositivity and families with two or more members (Chi 2 = 7.74; p=0.005).

The seropositivity was higher among personal from general services 48% (95% CI 37%-59%) and nurses 46% (95% CI 42%-49%) ( Figure 2 ). The occupation with the lowest seropositivity rate was physiotherapist 7% (95% CI 0%-18%). A reversed social gradient was found out between the presence of antibodies against SARS-CoV-2 and socioeconomic level (Chi 2 = 100.87; p trend = 0.0000001) ( Figure 3 ).

The multivariate model showed that participants from lower socioeconomic strata have more chance of having a reactive CLIA test (Table 2) . Besides, HCWs with blood type AB (+) compared with type O (+) were 68% more likely to have a reactive CLIA test. People who work in the emergency room and hospitalization were more likely to have a reactive CLIA test (by 57% and 37% respectively). Participants who worked in ICU and COVID services had not increased their risk of having a reactive test and were not significant in the multivariate model (Table 2 ).

Health care workers are a population with a high-risk of acquiring SARS-CoV-2 infection due to direct contact with patients [7, 22, 23] . We conducted a study to assess the seroprevalence of SARS-CoV-2 infection associated with characteristic demographics and the occupation of HCWs from 65 hospitals and medical centers in ten Colombian cities. We observed overall seroprevalence of 32%. Except Bucaramanga (26%), the seroprevalence was higher among workers in cities with less than 1.5 million inhabitants: Guapi (71%), Villavicencio (54%), Leticia (43%), and Ipiales (37%). The seroprevalence in cities with larger populations was lower: Bogotá (34%), Cali (35%), Cúcuta (27%) and Medellín (22%).

Comparing our findings with the reported seroprevalence of SARS-CoV-2 antibodies in the general population in Colombia (September -December 2020) [24] , except for Bucaramanga (32%), the seroprevalence in the HWC tended to be lower in cities located in the North . CC-BY-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted July 22, 2021. ; https://doi.org/10.1101/2021.07.21.21260103 doi: medRxiv preprint region (Barranquilla 55%, Cúcuta 40% and Medellín 27%). Nevertheless, the seroprevalence of SARS-CoV-2 antibodies in HCWs in cities from the Central, Southern and Western region of the country were higher than the reported in the general population (Bogota 30%, Leticia 59%, Villavicencio 34%, Guapi 68%, and Ipiales 35% [24] .

The seroprevalence in HCWs from Bogota was higher than in a previous study in one hospital in the city carried out in August 2020 (8.26%) [25] but similar to the seroprevalence reported in a cohort of airport workers in Bogotá (September 2020) [26] .

The reported seroprevalence of antibodies against SARS-CoV-2 in HCWs was greater than that reported in the studies conducted during the second semester of 2020 in North America (12.7%), Africa (8.2%) and Asia (4%) [27] . Besides, reports from studies carried out in European countries are lower than our results: Denmark (4.04%), England (24.4%), Germany 4.36% [28] , Greece 1.26% [29], Italy (14.4%), and Switzerland 1% [30] .

We have found no differences in the distribution of seroprevalence between males and females. This issue has been approached in several seroprevalence studies. A recent metanalyses has reported that seroprevalence levels were higher among male HW's [11] . Another systematic review observed a higher seroprevalence ratios among males [27] . This association may be correlated that men tend to show less adherence to protective protocols compared to women [31] . In our study we observed that men seem to be less willing to use all personal protection items compared to women.

Also, we observed that occupations that are performed mostly by women were associated with a higher risk of infection. It has been stated that gender is a social determinant of health, linked to the health disparities among the COVID-19 pandemic [32] . Also, it was highlighted that personal protective equipment does not protect female HW's as well as their male's colleagues. It has been pointed out, for example, that the glasses do not fit their faces, the gloves are too long, the face shields collide with the chest, making it uncomfortable to perform procedures [33, 34] . These conditions constitute a relevant concern considering that the COVID-19 pandemic has highlighted the extent to which society depends on women, both in the first line of response in the health sector, as well as at homes. Women constitute the majority of the workforce in the health sector [35] and in Colombia more than 70% of healthcare workers are women [36] . Nevertheless, these statistics do not include personnel involved in activities of cleaning and catering. Women have an increased risk of contracting SARS-CoV-2 given the close interaction with patients and visitors amidst shortages of personal protective equipment [32] . Also, women are concentrated in roles requiring the closest, prolonged contact with patients [37] .

We did not observed differences on seroprevalence levels regarding the ethnicity. Nevertheless, several authors have reported that exposition levels are higher among Afro-Americans and Hispanics [11, 27, 38] .

Also, an association between the presence of antibodies in serum and the social stratum in which the worker resides was found. It was observed that there is a reverse gradient in the . CC-BY-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted July 22, 2021. ; https://doi.org/10.1101/2021.07.21.21260103 doi: medRxiv preprint seroprevalence proportion; as far as the stratum increases, the proportion of people with a reactive test for antibodies decreases. These findings have been previously described at the community level, showing the association between socioeconomic aspects and COVID-19 transmission [39] , COVID-19 severity [40] , and antibody presence [41] . Nevertheless, to our knowledge, this is the first report showing the links between seroprevalence and socioeconomic strata among the health care workers. A study carried out among group workers of high risk for SARS-CoV-2 transmission have stated that prevention programs should include extra-labor risk-factors such as including recommendations for biological protection at home, supermarket, and other places, [42] . In this sense, various authors have indicated that most of the COVID-19 cases took place in places such as home [43, 44] . Considering that only 40% of the self-declared COVID-19 cases were recognized as linked to occupational activities, extra-occupational risk factors such as positive close contact at home, family size, and house conditions should be studied in detail to understand the SARS-CoV-2 transmission in HCWs [45] .

Additionally, the regression model found out that participants who work in the emergency room and hospitalization were more likely to have antibodies against SARS-CoV-2. Conversely, workers from ICU and COVID services had not increased their risk of having a reactive test. These findings differ from the literature reports which have stated that people working on COVID-19 units have an increased risk of having a positive SARS-CoV-2 antibody test [8, 46, 47] . Nevertheless, our results have shown that participants who work in emergency services showed a significant increase in the risk of having an antibody reactive test. A&E characteristics vary depending on the location, clinical specialties, and availability of technology. Most of the emergency services in Colombia have not divided the attention of respiratory cases from other emergencies. Also, patients could stay for longer periods waiting for diagnosis, treatment, or transference. These work conditions may increase the exposure risk of HCWs in emergency areas Studies have shown a slightly increased infection among non-O types. Also, the risk of intubation decreased in type A [48] . Here, we observed an increased risk in the AB blood types. However, this result may contribute to the knowledge of blood type and the relationship with the role of the infection with COVID-19.

The present study has limitations. First, the aspects related to the design of the research. A cross-sectional study was formulated and carried out between September and December 2020. Also, the characteristics of the sampling may introduce a selection bias among the workers who have been previously infected. Second, the health care workers answered the survey in different moments of the pandemic, even several months after having COVID-19 episode, which may introduce a recall bias. Likewise, we do not control or implement so methodology to determine if the exposure was occupational or if the disease was caused outside to the medical centers. In addition, the used test to identify antibodies against SARS-COV-2 did not allow to quantify the differences in antibody titers among the reactive participants. In this sense, we couldn´t perform an analysis including the role that the job position played in the generation or not of antibodies against SARS-CoV-2. Finally, the study . CC-BY-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted July 22, 2021. ; https://doi.org/10.1101/2021.07.21.21260103 doi: medRxiv preprint did not evaluate the inadequate use of personal protective equipment that has been associated with an increased risk of COVID-19 [49] [50] [51] . As well as the source of contagion was not determined in the study. However, though it could be a main key issue to the protection and to ensure treatment and recovery of the health worker.

In conclusion, to our knowledge, this is the first national study to quantify the level of seropositivity to SARS-CoV-2 in healthcare workers in the Andean region. The impact of the transmission in HCWs varies significantly from one city to another. Our findings have important implications both for understanding the spread of SARS-CoV-2 and for planning control programs in this population, as it could be the information of seroprevalence before the introduction of the SAR-CoV-2 vaccine. 

The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.

None declared.

Not required.

The study proposal and protocol were approved by the ethics committee of Instituto Nacional de Salud (CEMIN 012/2020) and the Research Ethics Committee from Universidad del Norte (223/10/2020). We have obtained written informed consent from each participant in the study.

The study protocol and anonymized individual participant data that underlie the results reported in this manuscript, may be shared with investigators whose proposed use of the data has been approved by the independent review committee of Instituto Nacional de Salud. Data can be provided for individual participant data meta-analysis or other projects comparing the seroprevalence estimates in different regions. The proposals should be directed to the . CC-BY-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted July 22, 2021. ; https://doi.org/10.1101/2021.07.21.21260103 doi: medRxiv preprint corresponding author at jmalagon@ins.gov.co. To gain access, data requesters will need to sign a data access agreement, confirmed by JMR as principal investigator.

The authors thank the hundreds of volunteers, community leaders, health institutions, and the thousands of participants of the study. Special thanks to Secretarias de Salud Distritales and Secretarias de Salud Departamentales from the cities involved in the study. A special thanks to the public institutions, Armada Nacional de Colombia, Policía Nacional de Colombia, Fontur, SATENA, and civil organizations that facilitated the transfers of personnel in the field and the logistics of the study in each city. Special recognition for the support of the field epidemiologists' team of the Field-Epidemiology-Training-Program (FETP) from Colombia. A special thanks goes to the collaborator team Magdalena Weisner, Gloria Puerto, Lyda Muñoz-Galindo, María Teresa Herrera, Jhonantan Reales, Edwin Cárdenas-Villamil, Jessica Ortíz, Ligia Ovideo and Liliana Serrano. A special thanks to healthcare workers of all medical centers in the country who have treated patients with COVID-19 since the beginning of the pandemic. Recognition and honors to the health personnel who lost their lives in this noble fight and to those who continue in this tough challenge. Finally, authors want to thank to Owen Harrison for his valuable comments in the final version of the manuscript.

The present research was financed by the Instituto Nacional de Salud . CC-BY-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted July 22, 2021. ; https://doi.org/10.1101/2021.07.21.21260103 doi: medRxiv preprint . CC-BY-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) . CC-BY-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review)

The copyright holder for this preprint this version posted July 22, 2021 . CC-BY-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. . CC-BY-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review)

The copyright holder for this preprint this version posted July 22, 2021. ; https://doi.org/10.1101/2021.07.21.21260103 doi: medRxiv preprint

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The authors declare no competing interests.