You are here

  • Home
  • Archive
  • Volume 12, Issue 4
  • COVID-19 among workers of a comprehensive cancer centre between first and second epidemic waves (2020): a seroprevalence study in Catalonia, Spain

Article Text

Article menu
Epidemiology
Original research
COVID-19 among workers of a comprehensive cancer centre between first and second epidemic waves (2020): a seroprevalence study in Catalonia, Spain
  1. Paula Peremiquel-Trillas1,2,3,4,
  2. Anna Saura-Lázaro1,2,
  3. Yolanda Benavente-Moreno1,2,3,
  4. Delphine Casabonne1,2,3,
  5. Eva Loureiro5,6,
  6. Sandra Cabrera7,
  7. Angela Duran8,
  8. Lidia Garrote9,
  9. Immaculada Brao10,
  10. Jordi Trelis4,11,
  11. Maica Galán12,
  12. Francesc Soler13,
  13. Joaquim Julià14,15,
  14. Dolça Cortasa16,
  15. Maria Ángeles Domínguez17,18,19,
  16. Adaia Albasanz-Puig20,21,22,
  17. Carlota Gudiol20,21,22,
  18. Dolors Ramírez-Tarruella23,
  19. Joan Muniesa5,
  20. Juan Pedro Rivas5,
  21. Carles Muñoz-Montplet5,24,25,
  22. Ana Sedano26,
  23. Àngel Plans27,
  24. Beatriz Calvo-Cerrada27,
  25. Candela Calle28,
  26. Ana Clopés29,
  27. Dolors Carnicer-Pont2,30,31,32,
  28. Laia Alemany1,2,3,
  29. Esteve Fernández2,4,30,31,32
  1. 1Cancer Epidemiology Research Programme, Cancer Epidemiology and Prevention Department, Institut Català d’Oncologia (ICO), L’Hospitalet de Llobregat, Spain
  2. 2Epidemiology and Public Health Programme, Institut d’Investigació Biomèdica de Bellvitge (IDIBELL), L’Hospitalet de Llobregat, Spain
  3. 3CIBER of Epidemiology and Public Health (CIBERESP), Madrid, Spain
  4. 4School of Medicine and Clinical Sciences, Universitat de Barcelona, L'Hospitalet de Llobregat, Spain
  5. 5Computer Science Services, Technology & Physics, Institut Català d’Oncologia (ICO), L’Hospitalet de Llobregat, Spain
  6. 6Computational Science and Artificial Intelligence, Schoolof Computer Science of Coruña, University of Coruña (UDC), Coruña, Spain
  7. 7Research Nursing Department, Institut Català d’Oncologia (ICO), Badalona, Spain
  8. 8Nursing Department, Institut Català d’Oncologia (ICO), L’Hospitalet de Llobregat, Spain
  9. 9Nursing Department, Institut Català d'Oncologia, Badalona, Spain
  10. 10Nursing Department, Institut Català d'Oncologia (ICO), Girona, Spain
  11. 11Palliative Care Department and Medical Director, Institut Català d’Oncologia (ICO), L’Hospitalet de Llobregat, Spain
  12. 12Esofagogastric Tumours Functional Unit and Medical Director, Institut Català d’Oncologia (ICO), L’Hospitalet de Llobregat, Spain
  13. 13Pharmacy Service and Medical Director, Institut Català d’Oncologia (ICO), Girona, Spain
  14. 14Palliative Care Department and Medical Director, Institut Català d’Oncologia (ICO), Badalona, Spain
  15. 15School of Medicine and Health Sciences, Universitat Internacional de Catalunya, Barcelona, Spain
  16. 16Medical Director, Institut català d'Oncologia, Tarragona, Spain
  17. 17Microbiology Department, Hospital Universitari de Bellvitge, L'Hospitalet de Llobregat, Spain
  18. 18Infectious Diseases Programme, Institut d’Investigació Biomèdica de Bellvitge (IDIBELL), L'Hospitalet de Llobregat, Spain
  19. 19Department of Pathology Experimental Therapeutics, Universitat de Barcelona, L'Hosìtalet de Llobregat, Spain
  20. 20Infectious Disease Department, Hospital Universitari de Bellvitge, L'Hospitalet de Llobregat, Spain
  21. 21Infectious Disease Unit, Institut català d'Oncologia (ICO), L'Hospitalet de Llobregat, Spain
  22. 22CIBER of Infectious Diseases (CIBERINFEC), Madrid, Spain
  23. 23Preventive Medicine Unit, Institut Català d’Oncologia (ICO), L’Hospitalet de Llobregat, Spain
  24. 24Medical Physics and Radiation Protection Department, Institut Català d’Oncologia (ICO), Girona, Spain
  25. 25Department of Medical Sciences, Universitat de Girona, Girona, Spain
  26. 26Human Resources Department, Institut Català d’Oncologia (ICO), L’Hospitalet de Llobregat, Spain
  27. 27Occupational Health Unit, Institut Català d’Oncologia (ICO), L’Hospitalet de Llobregat, Spain
  28. 28General Direction, Institut Català d'Oncologia (ICO), L'Hospìtalet de Llobregat, Spain
  29. 29Scientific Direction, Institut Català d’Oncologia (ICO), L'Hospitalet de Llobregat, Spain
  30. 30Cancer Prevention and Control Programme, Cancer Epidemiology and Prevention Department, Institut català d'Oncologia (ICO), L'Hospitalet de Llobregat, Spain
  31. 31CIBER of Respiratory Diseases (CIBERES), Madrid, Spain
  32. 32WHO Collaborating Center for Tobacco Control, Institut català d'Oncologia (ICO), L'Hospitalet de Llobregat, Spain
  1. Correspondence to Dr Esteve Fernández; efernandez{at}iconcologia.net

Abstract

Objectives Patients with cancer are at higher risk for severe COVID-19 infection. COVID-19 surveillance of workers in oncological centres is crucial to assess infection burden and prevent transmission. We estimate the SARS-CoV-2 seroprevalence among healthcare workers (HCWs) of a comprehensive cancer centre in Catalonia, Spain, and analyse its association with sociodemographic characteristics, exposure factors and behaviours.

Design Cross-sectional study (21 May 2020–26 June 2020).

Setting A comprehensive cancer centre (Institut Català d’Oncologia) in Catalonia, Spain.

Participants All HCWs (N=1969) were invited to complete an online self-administered epidemiological survey and provide a blood sample for SARS-CoV-2 antibodies detection.

Primary outcome measure Prevalence (%) and 95% CIs of seropositivity together with adjusted prevalence ratios (aPR) and 95% CI were estimated.

Results A total of 1266 HCWs filled the survey (participation rate: 64.0%) and 1238 underwent serological testing (97.8%). The median age was 43.7 years (p25–p75: 34.8–51.0 years), 76.0% were female, 52.0% were nursing or medical staff and 79.0% worked on-site during the pandemic period. SARS-CoV-2 seroprevalence was 8.9% (95% CI 7.44% to 10.63%), with no differences by age and sex. No significant differences in terms of seroprevalence were observed between onsite workers and teleworkers. Seropositivity was associated with living with a person with COVID-19 (aPR 3.86, 95% CI 2.49 to 5.98). Among on-site workers, seropositive participants were twofold more likely to be nursing or medical staff. Nursing and medical staff working in a COVID-19 area showed a higher seroprevalence than other staff (aPR 2.45, 95% CI 1.08 to 5.52).

Conclusions At the end of the first wave of the pandemic in Spain, SARS-CoV-2 seroprevalence among Institut Català d’Oncologia HCW was lower than the reported in other Spanish hospitals. The main risk factors were sharing household with infected people and contact with COVID-19 patients and colleagues. Strengthening preventive measures and health education among HCW is fundamental.

  • SARS-CoV-2
  • COVID-19
  • seroprevalence
  • antibody
  • health care workers
  • epidemiology

Data availability statement

Data are available on reasonable request.

https://creativecommons.org/licenses/by/4.0/

This is an open access article distributed in accordance with the Creative Commons Attribution 4.0 Unported (CC BY 4.0) license, which permits others to copy, redistribute, remix, transform and build upon this work for any purpose, provided the original work is properly cited, a link to the licence is given, and indication of whether changes were made. See: https://creativecommons.org/licenses/by/4.0/.

https://doi-org.ezproxy.u-pec.fr/10.1136/bmjopen-2021-056637

Statistics from Altmetric.com

    Request Permissions

    If you wish to reuse any or all of this article please use the link below which will take you to the Copyright Clearance Center’s RightsLink service. You will be able to get a quick price and instant permission to reuse the content in many different ways.

    Strengths and limitations of this study

    • Seroepidemiological study with a large sample size settled in a comprehensive cancer centre.

    • Questionnaire completeness was very high, with no variables presenting more than 5% of missing values.

    • Recall bias is possible as the data for the correlates of SARS-CoV-2 infection rely on a self-administered questionnaire.

    • The accomplishment of preventive measures might be overestimated: response and perception biases must be considered, as well as complacency bias.

    • Answers reported in the questionnaire could be influenced by the participants’ knowledge regarding their COVID-19 status.

    Introduction

    Front-line healthcare workers (HCWs) dealing with COVID-19 have higher exposure to SARS-CoV-2 than the general population,1 and they can contribute to the spread of COVID-19 as per their exposure to vulnerable patients. Since the beginning of the pandemic, several studies have been published on SARS-CoV-2 infections prevalence in HCW, although with diverse results. A meta-analysis of 49 studies, including 127 480 HCWs, showed that the overall seroprevalence of SARS-CoV-2 antibodies in the European region was 8.5%.2 HCW in Spain have been highly affected: a total amount of 154 636 cases among HCWs were already officially notified by 2 December 2021 at the onset of the sixth pandemic wave.3 4

    Patients with cancer are vulnerable, presenting a high risk for COVID-19 infection and more severe outcomes due to their immunosuppression status.5 The pandemic has presented unprecedented professional and personal challenges for the oncology community.6 Data are lacking on the seroprevalence of SARS-CoV-2 among HCW in oncological centres, and small sample sizes limit the few published studies. This study aims to estimate the seroprevalence of SARS-CoV-2 and associated sociodemographic and behavioural risk factors among workers of the Catalan Institute of Oncology (ICO), a Comprehensive Cancer Centre comprised of four hospitals in Catalonia (Spain), covering around 40% of the adult population in Catalonia.7

    Participants and methods

    Study design and setting

    A cross-sectional study including blood sample collection and a self-administered questionnaire was conducted between 21 May 2020 and 26 June 2020 in the four ICO centres (L’Hospitalet de Llobregat, Badalona, Tarragona/Terres de l’Ebre and Girona).

    The study population were HCW delivering care and services to patients (directly or indirectly) and support staff, including those who do not deliver care but work in other tasks within the hospital. A total of 1969 employees of ICO were invited to participate in the study through an email that allowed access to the study information. The inclusion criteria were: (1) to be an active worker during the epidemic period, (1 February 2020–26 June 2020) and (2) to be aged ≥18 years. The participants filled in an online epidemiological questionnaire and were scheduled for serology testing by the Occupational Health Department. A total of 1266 HCW filled in the online epidemiological questionnaire (participation rate: 64.3%) and 1238 of them (97.8%) underwent a serology test. Three participants with inconclusive serological results were excluded. The final analysis included 1235 participants (figure 1).

    Figure 1
    Figure 1

    Participants' flow chart in the seroprevalence survey, Catalan Institute of Oncology. 21 May 2020–26 June 2020; Spain.

    Epidemiological questionnaire and study variables

    An epidemiological questionnaire was programmed online to collect information regarding sociodemographic characteristics, working information, compliance of personal protective equipment (PPE) measures at work, at home and history of previous COVID-19 infection (online supplemental material). The questionnaire was developed based on previous epidemiological studies conducted within the ICO centres, and a modified version was used in another seroprevalence study performed among university personnel of the University of Barcelona.8

    Sociodemographic characteristics included information on age and sex, ICO centre of recruitment, presence of comorbidities, smoking history, pregnancy and cohabitants.

    Work-related conditions included the professional category, teleworking status, type of shift, working on a COVID-19 area, contact with COVID-19 cases, contact with biological samples and reporting to be exposed to COVID-19.

    Concerning PPE measures at work, participants were asked about feeling protected with PPE and compliance with PPE measures. Regarding the application of preventive measures outside the working setting, participants were asked if they got a shower after leaving the workplace or when arriving home, if they changed clothes after work or on home arrival, as well as about hand washing and use of face mask when shopping. Information about COVID-19 cases and protective measures were also collected among those participants reporting cohabitants. Participants were also asked about the type of transport used to go to work.

    Participants were asked about a previous diagnosis of COVID-19 performed by rRT-PCR or serology test and date of diagnosis, as well as reporting COVID-19 compatible symptoms, and the type of symptoms.

    SARS-CoV-2 laboratory testing

    Serum samples from participants at L’Hospitalet, Girona and Tarragona/Terres de l’Ebre were studied at the Microbiology Department of Hospital de Bellvitge and samples from HCWs at ICO Badalona were analysed at the MetroNord Regional Clinical Laboratory, using the same procedures and techniques in both laboratories. Detection of SARS-CoV-2 antibodies was carried out using the quantitative SARS-CoV-2 S1/S2 IgG LIAISON test (DiaSorin, Vercelli, Italy) on the LIAISON XL platform, following the manufacturer’s instructions. This test discriminates among negative (<12AU/mL; with 3.8 as IgG detection limit), equivocal (12.0–15.0AU/mL) and positive (>15.0AU/mL) subjects. In those cases in which (1) IgG anti S1/S2 quantification was higher than the limit of detection (ie, >3.8AU/mL) but did not reach the limit of discrimination (ie,<15AU/mL) and/or (2) when the HCW answered the questionnaire saying that he or she had been diagnosed of COVID-19 but IgG anti S1/S2 where lower than 15 AU/mL, an additional serological study was performed using a different antigen (N) as a target. In this case, a SARS-CoV-2 IgG test (Abbott Diagnostics, Sligo, Ireland) was run on an Architect i2000 platform. This test discriminates among negative (<1.4Index (S/C)) and positive (≥1.4Index (S/C)) subjects.

    Case definition

    A seropositive case of SARS-CoV-2 was defined as seropositivity to IgG independently of previous self-reported results.

    Patient and public involvement

    No patient was involved in the study.

    Statistical analysis

    Crude global and by subgroups SARS-CoV-2 seroprevalence and 95% CIs were calculated. Differences in the distribution of study variables between seropositive and seronegative participants were assessed using χ2 test for categorical variables, and parametric or non-parametric tests were performed for normal and non-normal continuous variables, respectively. Prevalence ratios (PR) and 95% CIs were estimated using Poisson regression models with robust variance.9 Adjusted PRs (aPRs) were used for statistically significant variables in the bivariate analysis and those considered relevant for the study design. Thus, adjusted models included sex, ICO centre of recruitment, age, type of HCW, teleworking and cohabitants. Linear trends for variables with ordinal categories was based in the likelihood ratio test of the model with the ordinal variable as a continuous one. P values were based on two-sided hypothesis tests and considered significant at p<0.05. All analyses were conducted using Stata V.16.0 (StataCorp).

    Results

    A total of 1235 HCWs with serological results (figure 1) were included in the analysis: 76.0% were female, the median age was 43.7 years (p25–p75: 34.8–51.0 years), 52.2% were nursing or medical staff and 18.6% of the participants teleworked full time during the study period (table 1). Up to 14.7% of the participants reported at least one comorbidity. Regarding smoking habits, 16.0% were current smokers and 28.2% reported to be former smokers (table 1). Seven women were pregnant, and none of them showed seropositivity.

    View this table:
    Table 1

    Sociodemographic characteristics associated with SARS-CoV-2 positive serology among study participants (N=1235)

    The overall crude SARS-CoV-2 seroprevalence was 8.9% (95% CI 7.44% to 10.63%), with no statistically significant differences by neither age group nor sex, and the seroprevalence for nursing and medical staff was 11.6% (95% CI 9.37% to 14.34%). After fully adjustment, the main determinants of higher seroprevalence included working at ICO Girona compared with workers at ICO L’Hospitalet (aPR 1.52, 95% CI 0.97 to 2.38) and nursing or medical staff compared with other groups (aPR 2.04, 95% CI 1.33 to 3.14) (table 1).

    Seroprevalence among on-site workers was 8.8% (95% CI 7.15% to 10.71%) (table 2). Onsite workers were younger, assisting HCWs and reported more frequently rRT-PCR previous to serology than teleworkers, but no differences were observed in sex, self-reported comorbidities, smoking history, cohabiting with COVID-19 positive case between them and teleworkers (online supplemental material). Among this group (N=981) of professionals who never or occasionally teleworked SARS-CoV-2 seropositivity was not associated with not working in a COVID-19 area (aPR 1.29, 95% CI 0.81 to 2.06), nor being in contact with COVID-19 biological samples (aPR 1.30, 95% CI 0.77 to 2.20) nor being in contact with patients with COVID-19 (aPR 1.09, 95% CI 0.66 to 1.79) were associated with SARS-CoV-2 positivity (table 2). On-site nursing or medical staff who worked in a COVID-19 area had twofold SARS-CoV-2 seroprevalence than others who did not work in COVID-19 area (aPR 2.45, 95% CI 1.08 to 5.52). Seropositivity was higher among those whom referred being exposed by interacting with colleagues (aPR 3.26, 95% CI 1.49 to 7.15). On-site workers who self-reported symptoms of COVID-19 were almost 10-fold more likely to be seropositive than those who did not (aPR: 9.5, 95% CI 5.34 to 17.03). Most of the on-site workers were highly adherent to the recommendation of hand hygiene at work. Hand washing before eating or working, were followed by more than 97% of on-site workers, whereas around 24% of them reported not hand hygiene after working or a low frequency of handwashing during the workday. In relation to protective measures at work, 17.4% of the on-site workers did not feel protected with PPE, and 12.1% did not use PPE with confirmed or suspicious COVID-19 cases. About colleagues’ behaviour, 2 m safety distance from colleagues when having lunch was reported to be unfollowed by 14.1% (table 2).

    View this table:
    Table 2

    Occupational factors associated with SARS-CoV-2 positive serology among on-site workers (N=981)

    Concerning the correlates of seropositivity according to household factors for all participants (table 3), seropositivity was associated with living with a COVID-19 positive person (aPR 3.86, 95% CI 2.49 to 5.98). Up to 17.3% of the participants did not take a shower nor change clothes on home arrival, but the majority (99.0%) did hand hygiene. The least followed hand hygiene home practices were after money, phone and other personal tools manipulation and after nose blowing, coughing or sneezing (23.5% and 22.7%). However, not following protection measures or hand hygiene at home were associated with a higher SARS-CoV-2 seroprevalence.

    View this table:
    Table 3

    Household factors associated with SARS-CoV-2 positive serology among study participants (n=1235)

    Clinical characteristics were collected for those participants (N=469) who reported a rRT-PCR performed previous to serology (online supplemental material). The majority of the patients with a positive serology and reporting a positive rRT-PCR presented compatible COVID-19 symptoms (74.4%). Among seropositive patients, the most common symptoms were arthromyalgia, cough, headache, asthenia and anosmia. Reporting a positive rRT-PCR when presenting compatible symptoms was associated with a threefold higher prevalence of seropositivity (aPR 3.10, 95% CI 1.78 to 5.31). An increased number of compatible symptoms was also associated with a higher seroprevalence (aPR 7.4, 95% CI 1.78 to 5.31, for presenting four or more symptoms compared with no symptoms).

    Discussion

    Despite the impact of COVID-19 in oncological patients,10 there are scarce SARS-CoV-2 seroprevalence studies in comprehensive cancer centres with large sample sizes. The global SARS-CoV-2 seroprevalence was 8.9% during the first wave of the COVID-19 pandemic, lower than expected, owing to the presumed higher risk among HCW. Also, it was lower than the reported estimates in two studies performed among HCW in Catalonia between March-April and May 2020, showing a seroprevalence of 11.2%11 and 10.3%,12 respectively. In all cases, the seroprevalence was higher than in the general population, estimated to be of a maximum of 7.4% in the Barcelona metropolitan area when the study was conducted.13 Seroprevalence studies interpretation must be related to the average COVID-19 prevalence at the time of blood collection. Both of the mentioned studies were carried out earlier than ours, which was performed approximately 1 month later (21 June 2020 May–26 June 2020), and 2 months after the first-wave peak in Catalonia (23 March).14 Another explanation for this lower seroprevalence in our Centre concerns the participation: all active HCW, regardless of their teleworking status during the previous months or work absenteeism, were invited to participate and most did (64%). In contrast, Garcia-Basteiro et al’s11 and Barallat et al’s12 studies comprised general hospitals10 11 and primary healthcare centres12 in which the incidence could be higher than in a monographic cancer centre.

    Several studies regarding COVID-19 infections in HCW in Spain have been published, although showing diverse results. In a tertiary-care hospital in Mallorca, with low regional seroprevalence in the general population (<2%), the prevalence of infected HCW (n=2210) was 2.8%.15 Varona et al performed a cross-sectional study evaluating 6038 employees from the healthcare system of 17 hospitals across four regions in Spain (Madrid, Catalonia, Galicia and Castilla-Leon), showing an 11% seropositivity for SARS-CoV-2 IgG.16 Finally, other studies in Madrid reported a seroprevalence between 16.6% and 36.5% among HCW in areas with high COVID-19 prevalence.17–19 These studies revealed seroprevalence of SARS-CoV-2 IgG antibodies in HCW tend to be higher than in the general population, at variance according to regional COVID-19 incidence.

    The prevalence of SARS-CoV-2 antibodies among HCW has been increasingly investigated in many other countries showing a broad range of outcomes. So far, two systematic reviews estimated an overall seroprevalence of SARS-CoV-2 antibodies of 8.7% and 8.0% among 127 480 HCW and 168 200 HCW, respectively, before vaccination started.2 20 Seroprevalence was higher in studies conducted in North America (12.7%) compared with those conducted in Europe (8.5%), Africa (8.2) and Asia (4%).2

    In Europe, seroprevalence rates among HCW in Germany, Denmark and Belgium were low (1.6%, 4.0% and 6.4%, respectively).21–23 These studies were conducted during early stages of the epidemic, and therefore, they derived that infection was community acquired. Also, the Belgian study, with a sample size of almost 30 000 HCW, notes that the high availability of PPE, high standards of infection prevention and PCR screening in symptomatic staff, coupled with contact tracing and quarantine, might explain the relatively low seroprevalence.23 An study performed in Lombardy, Italy,24 one of the Italian regions most hit by the first epidemic wave, showed a seroprevalence of 7.4% (3.8%–11.0%), similar to the observed in the Catalan studies.11 12 Sweden and the UK were the two European countries reporting the highest seropositivity rates among HCW: 19.1% and between 18.0% and 45.3%, respectively.25–27 In the UK, this high seroprevalence was settled in London during the week with the highest number of new cases in the city in the first wave, with around 15% seropositivity among the general population. In the USA, the prevalence of infection among HCW was 10.7%, despite high variation, as low as 1.1% in California28 to 13.7% in New York State.29

    Despite SARS-CoV-2 seropositivity rate in oncological HCW has significant implications for oncological patients, scant research has been done. The only study published with a large sample size was in Tokyo, Japan, and it showed a very low seroprevalence of 0.67% among 1,190 HCW. It was performed at the end of the first wave in Japan, between the 3 August 2020 and the 30 October 2020, so this may explain the lower seroprevalence compared with our estimation. A French study performed among 663 HCW and 1011 patients with cancer, after the end of the first wave, showed also low seroprevalence both for HCW and patients (1.8% and 1.7%, respectively).30 Other studies that have been published were based on small sample sizes and showed very variable seroprevalence rates.22 31–35

    In our study, we found no differences in HCW seroprevalence according to sex, age and presence of comorbidities. Current or past smoking was however inversely associated to SARS-CoV-2 seroprevalence. Early studies in selected cohorts of COVID-19 patients showed a paradoxical higher risk of SARS-CoV-2 infection among non-smokers36 while ever smokers showed higher risk of COVID-19 progression, including severity of the disease, intensive care unit admission and death.37

    It is worth mentioning that, unlike most of the other published seroepidemiological studies among HCW, this study was performed among all the HCWs of the institution, regardless they did full-time telework during the study period (21.6%). No differences by telework were found, and among all study participants the main factor associated with SARS-CoV-2 seropositivity was living with a COVID-19 case, with a 1.5 times higher probability, similarly to what has been described in other studies.2 20 This finding supports the importance of community dissemination of the infection also for HCWs.

    Our study shows that among on-site HCW in an oncological centre, working as medical care staff (nursing, nursing assistant, resident physicians and specialists) in COVID-19 areas stood out as one of the main factors associated with developing SARS-CoV-2 antibodies. Published results regarding the possibility of in-hospital infection among HCW and transmission at work are controversial. Some studies did not find any relation between working in COVID-19 unit or professional category with seropositivity11 24 whereas other studies reported that seroprevalence was strongly associated with patient related work.16 21 22 25

    Contact with colleagues at work is potentially a risky situation for transmission among HCW as well as the relaxation of protective measures at the end of the working day. In our study, the on-site HCW who reported being exposed to COVID-19 by other colleagues presented an almost fourfold probability of being seropositive. Most of the HCWs declared to follow the protective measures at the workplace, and no differences in seroprevalence were found according to protective measures and hand hygiene.

    Protecting HWC health is of paramount importance for reducing morbidity and mortality, reducing transmission and maintaining the health system capacity.38 Thus, international health authorities recommend screening strategies for SARS-CoV-2 infection in exposed or high-risk HCW39 as well as massive COVID-19 vaccination.40

    Significant differences exist in SARS-CoV-2 testing between countries, and existing programmes focus on screening symptomatic rather than asymptomatic staff. Published studies point out the fact that screening should be performed regardless of the absence of typical symptoms for COVID-19 disease. It has been demonstrated that seroconversion can occur in HCW who have suffered no previous symptoms of SARS-CoV-2 infection41 42 as asymptomatic transmission is very relevant in SARS-CoV-2 spread.42 43 Thus, the approach for mass testing of both symptomatic and asymptomatic HCW could mitigate workforce depletion by unnecessary quarantine, reduce spread in atypical, mild or asymptomatic cases; and protect patients and healthcare workforce.

    Among the potential limitations of the study, some recall bias is possible as the data for the correlates of SARS-CoV-2 infection rely on a self-administered questionnaire. Also, response and perception biases must be considered, as well as complacency bias. Results, especially those regarding the accomplishment of preventive measures, might be overestimated. Answers reported in the questionnaire could be influenced by the participants’ knowledge regarding their COVID-19 status. However, this study is the first seroepidemiological study with such a large sample size settled in an oncological health centre. The sufficient sample size and high response rate (64.3%) are strengths of the study, although information regarding non-participants was not collected, and we cannot disregard a potential participation bias. However, the distribution by age and sex was similar between participants and non-participants and a possible reason for no participation is that professionals from ICO-Badalona had previously participated in an HCW county seroprevalence survey.12 Also, the fact that the information of the study and the questionnaire was published online and sent by email, as well as the short period of time stablished to respond to it, could have limited the participation. Questionnaire completeness was very high, with no variables presenting more than 5% of missing values.

    In conclusion, SARS-CoV-2 seroprevalence among ICO HCW at the end of the first wave of the pandemic was lower than the reported in other Catalan hospitals, but higher than among the general population living in the area. Whereas the main risk factor was living with infected people, among on-site workers, contact with colleagues was associated with SARS-CoV-2 infection. Knowing the seroprevalence rate and follow-up evaluation of persistence may help hospitals to characterise the staff at risk, rationalise their placement, prioritise the use of PPE, thereby potentially reducing the risk of infection. Follow-up studies to evaluate long-term durability of antibodies among HCW will be of interest, after the introduction of COVID-19 vaccination among HCW, to better promote infection control in this group. Strengthening preventive measures and health education among HCW is fundamental, especially in oncological departments and centres.

    Data availability statement

    Data are available on reasonable request.

    Ethics statements

    Patient consent for publication

    Ethics approval

    The present study was approved by the Hospital Universitari de Bellvitge Ethics Committee (PR205/20). The study follows the Helsinki Declaration and subsequent amendments, and Spanish data confidentiality laws (General data protection regulation Organic Law 3/2018, EU General data protection Regulation 2016/679 and Law 14/2007 for biomedical research). All participants signed an informed consent form after receiving information of the study and prior to obtaining biological samples. The biological material obtained was kept at ICO and processed under the appropriate measures to preserve the confidentiality of the results and data.

    Acknowledgments

    The authors acknowledge all the healthcare workers who participated in the study as well as all the ICO staff involved in the logistics of the different aspects of the study. We thank CERCA Programme/Generalitat de Catalunya for institutional support.

    References

    1. ↵
      1. Ng K,
      2. Poon BH,
      3. Kiat Puar TH, et al
      . COVID-19 and the risk to health care workers: a case report. Ann Intern Med 2020;172:766–7.doi:10.7326/L20-0175pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/32176257
      OpenUrlCrossRefPubMed
    2. ↵
      1. Galanis P,
      2. Vraka I,
      3. Fragkou D, et al
      . Seroprevalence of SARS-CoV-2 antibodies and associated factors in healthcare workers: a systematic review and meta-analysis. J Hosp Infect 2021;108:120–34.doi:10.1016/j.jhin.2020.11.008pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/33212126
      OpenUrlCrossRefPubMed
    3. ↵
      1. Informe n° 56
      . Situación de COVID-19 en España. Casos diagnosticados a partir de 10 de Mayo. Instituto de Salud Carlos III; red Nacional de Vigilancia Epidemiológica. España, 2020. Available: https://www.isciii.es/QueHacemos/Servicios/VigilanciaSaludPublicaRENAVE/EnfermedadesTransmisibles/Documents/INFORMES/Informes%20COVID-19/Informe%20COVID-19.%20N%c2%ba%2056_09%20de%20diciembre%20de%202020.pdf
    4. ↵
      1. Centro de Coordinación de Alertas y, Emergencias Sanitarias
      . Actualización no 517. Enfermedad por el coronavirus (COVID-19). 03.12.2021 [Internet]. Available: https://www.sanidad.gob.es/profesionales/saludPublica/ccayes/alertasActual/nCov/documentos/Actualizacion_517_COVID-19.pdf [Accessed 01 Feb 2022].
    5. ↵
      1. Dai M,
      2. Liu D,
      3. Liu M, et al
      . Patients with cancer appear more vulnerable to SARS-CoV-2: a multicenter study during the COVID-19 outbreak. Cancer Discov 2020;10:783.doi:10.1158/2159-8290.CD-20-0422pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/32345594
      OpenUrlAbstract/FREE Full Text
    6. ↵
      1. Leung MST,
      2. Lin SG,
      3. Chow J, et al
      . COVID-19 and oncology: service transformation during pandemic. Cancer Med 2020;9:7161–71.doi:10.1002/cam4.3384pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/32810386
      OpenUrlPubMed
    7. ↵
      Institut Catal d’Oncologia [Internet]. Available: http://ico.gencat.cat/ca/l_institut/ [Accessed 19 Mar 2021].
    8. ↵
      1. Videla S,
      2. Otero A,
      3. Martí S, et al
      . Prevalence of SARS-CoV-2 infection at the University of Barcelona during the third COVID-19 pandemic wave in Spain. Int J Environ Res Public Health 2021;18:6526.doi:10.3390/ijerph18126526pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/34204383
      OpenUrlPubMed
    9. ↵
      1. Barros AJD,
      2. Hirakata VN
      . Alternatives for logistic regression in cross-sectional studies: an empirical comparison of models that directly estimate the prevalence ratio. BMC Med Res Methodol 2003;3:1–13.doi:10.1186/1471-2288-3-21pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/14567763
      OpenUrlCrossRefPubMed
    10. ↵
      1. Richards M,
      2. Anderson M,
      3. Carter P, et al
      . The impact of the COVID-19 pandemic on cancer care. Nature Cancer 2020;1:565–7.doi:10.1038/s43018-020-0074-y
      OpenUrl
    11. ↵
      1. Garcia-Basteiro AL,
      2. Moncunill G,
      3. Tortajada M, et al
      . Seroprevalence of antibodies against SARS-CoV-2 among health care workers in a large Spanish reference Hospital. Nat Commun 2020;11:1–9.doi:10.1038/s41467-020-17318-x
      OpenUrlCrossRefPubMed
    12. ↵
      1. Barallat J,
      2. Fernández-Rivas G,
      3. Quirant-Sánchez B, et al
      . Seroprevalence of SARS-CoV-2 IgG specific antibodies among healthcare workers in the Northern metropolitan area of Barcelona, Spain, after the first pandemic wave. PLoS One 2020;15:e0244348.doi:10.1371/journal.pone.0244348pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/33370363
      OpenUrlPubMed
    13. ↵
      1. Pollán M,
      2. Pérez-Gómez B,
      3. Pastor-Barriuso R, et al
      . Prevalence of SARS-CoV-2 in Spain (ENE-COVID): a nationwide, population-based seroepidemiological study. Lancet 2020;396:535–44.doi:10.1016/S0140-6736(20)31483-5pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/32645347
      OpenUrlCrossRefPubMed
    14. ↵
      COVID-19 data and indicators. Sistemes d’Informació dels Serveis d’Atenció Prim ria- SISAP, Institut Catal de la Salut, Departament de Salut, Generalitat de Catalunya. [Internet], 2020. Available: http://eines.portalics/covid/ [Accessed 19 Mar 2021].
    15. ↵
      1. Rodriguez A,
      2. Arrizabalaga-Asenjo M,
      3. Fernandez-Baca V, et al
      . Seroprevalence of SARS-CoV-2 antibody among healthcare workers in a university hospital in Mallorca, Spain, during the first wave of the COVID-19 pandemic. Int J Infect Dis 2021;105:482–6.doi:10.1016/j.ijid.2021.02.104pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/33647507
      OpenUrlPubMed
    16. ↵
      1. Varona JF,
      2. Madurga R,
      3. Peñalver F, et al
      . Seroprevalence of SARS-CoV-2 antibodies in over 6000 healthcare workers in Spain. Int J Epidemiol 2021;50:400–9.doi:10.1093/ije/dyaa277pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/33434269
      OpenUrlPubMed
    17. ↵
      1. Galán MI,
      2. Velasco M,
      3. Casas ML
      . SARS-CoV-2 Seroprevalence Among All Workers in a Teaching Hospital in Spain: Unmasking The Risk [Internet]. medRxiv 2020:2020.05.29.20116731.
    18. ↵
      1. Pérez-García F,
      2. Pérez-Zapata A,
      3. Arcos N, et al
      . Severe acute respiratory coronavirus virus 2 (SARS-CoV-2) infection among hospital workers in a severely affected institution in Madrid, Spain: a surveillance cross-sectional study. Infect Control Hosp Epidemiol 2021;42:803–9.doi:10.1017/ice.2020.1303pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/33118904
      OpenUrlPubMed
    19. ↵
      1. Cantero M,
      2. Millán-Pérez R,
      3. Muñez E, et al
      . SARS-COV-2 seroprevalence among all healthcare workers in a tertiary hospital in Spain. Infect Dis 2022;54:8–15.doi:10.1080/23744235.2021.1963468pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/34424122
      OpenUrlPubMed
    20. ↵
      1. Kayı İlker,
      2. Madran B,
      3. Keske Şiran, et al
      . The seroprevalence of SARS-CoV-2 antibodies among health care workers before the era of vaccination: a systematic review and meta-analysis. Clin Microbiol Infect 2021;27:1242–9.doi:10.1016/j.cmi.2021.05.036pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/34116205
      OpenUrlPubMed
    21. ↵
      1. Korth J,
      2. Wilde B,
      3. Dolff S, et al
      . SARS-CoV-2-specific antibody detection in healthcare workers in Germany with direct contact to COVID-19 patients. J Clin Virol 2020;128:104437.doi:10.1016/j.jcv.2020.104437pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/32434708
      OpenUrlCrossRefPubMed
    22. ↵
      1. Iversen K,
      2. Bundgaard H,
      3. Hasselbalch RB, et al
      . Risk of COVID-19 in health-care workers in Denmark: an observational cohort study. Lancet Infect Dis 2020;20:1401–8.doi:10.1016/S1473-3099(20)30589-2pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/32758438
      OpenUrlCrossRefPubMed
    23. ↵
      1. Steensels D,
      2. Oris E,
      3. Coninx L, et al
      . Hospital-Wide SARS-CoV-2 antibody screening in 3056 staff in a tertiary center in Belgium. JAMA 2020;324:195–7.doi:10.1001/jama.2020.11160pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/32539107
      OpenUrlPubMed
    24. ↵
      1. Sotgiu G,
      2. Barassi A,
      3. Miozzo M, et al
      . SARS-CoV-2 specific serological pattern in healthcare workers of an Italian COVID-19 forefront Hospital. BMC Pulm Med 2020;20:1–6.doi:10.1186/s12890-020-01237-0pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/32727446
      OpenUrlCrossRefPubMed
    25. ↵
      1. Rudberg A-S,
      2. Havervall S,
      3. Månberg A, et al
      . SARS-CoV-2 exposure, symptoms and seroprevalence in healthcare workers in Sweden. Nat Commun 2020;11:1–8.doi:10.1038/s41467-020-18848-0
      OpenUrlCrossRefPubMed
    26. ↵
      1. Pallett SJC,
      2. Rayment M,
      3. Patel A, et al
      . Point-Of-Care serological assays for delayed SARS-CoV-2 case identification among health-care workers in the UK: a prospective multicentre cohort study. Lancet Respir Med 2020;8:885–94.doi:10.1016/S2213-2600(20)30315-5pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/32717210
      OpenUrlPubMed
    27. ↵
      1. Houlihan CF,
      2. Vora N,
      3. Byrne T, et al
      . SARS-CoV-2 virus and antibodies in front-line Health Care Workers in an acute hospital in London: Preliminary results from a longitudinal study [pre-print]. Available: https://www.medrxiv.org/content/10.1101/2020.06.08.20120584v1
    28. ↵
      1. Brant-Zawadzki M,
      2. Fridman D,
      3. Robinson PA, et al
      . SARS-CoV-2 antibody prevalence in health care workers: preliminary report of a single center study. PLoS One 2020;15:e0240006.doi:10.1371/journal.pone.0240006pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/33180782
      OpenUrlCrossRefPubMed
    29. ↵
      1. Moscola J,
      2. Sembajwe G,
      3. Jarrett M, et al
      . Prevalence of SARS-CoV-2 antibodies in health care personnel in the new York City area. JAMA 2020;324:893–5.doi:10.1001/jama.2020.14765pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/32780804
      OpenUrlPubMed
    30. ↵
      1. Ladoire S,
      2. Goussot V,
      3. Redersdorff E, et al
      . Seroprevalence of SARS-CoV-2 among the staff and patients of a French cancer centre after first lockdown: the canSEROcov study. Eur J Cancer 2021;148:359–70.doi:10.1016/j.ejca.2021.02.027pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/33780664
      OpenUrlPubMed
    31. ↵
      1. Favara DM,
      2. McAdam K,
      3. Cooke A, et al
      . SARS-CoV-2 infection and antibody seroprevalence among UK healthcare professionals working with cancer patients during the first wave of the COVID-19 pandemic. Clin Oncol 2021;33:667–75.doi:10.1016/j.clon.2021.04.005pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/33941453
      OpenUrlPubMed
    32. ↵
      1. Epstude J,
      2. Harsch IA
      . Seroprevalence of COVID-19 antibodies in the cleaning and oncological staff of a municipal clinic. GMS Hyg Infect Control 2020;15:5–9.doi:10.3205/dgkh000353pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/32733782
      OpenUrlPubMed
    33. ↵
      1. Fuereder T,
      2. Berghoff AS,
      3. Heller G, et al
      . SARS-CoV-2 seroprevalence in oncology healthcare professionals and patients with cancer at a tertiary care centre during the COVID-19 pandemic. ESMO Open 2020;5:e000889.doi:10.1136/esmoopen-2020-000889pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/32878898
      OpenUrlAbstract/FREE Full Text
    34. ↵
      1. Fong D,
      2. San Nicolò KO,
      3. Alber M, et al
      . Evaluating the longitudinal effectiveness of preventive measures against COVID-19 and seroprevalence of IgG antibodies to SARS-CoV-2 in cancer outpatients and healthcare workers. Wien Klin Wochenschr 2021;133:359–63.doi:10.1007/s00508-020-01807-6pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/33502609
      OpenUrlPubMed
    35. ↵
      1. Marra A,
      2. Generali D,
      3. Zagami P, et al
      . Seroconversion in patients with cancer and oncology health care workers infected by SARS-CoV-2. Ann Oncol 2021;32:113–9.doi:10.1016/j.annonc.2020.10.473pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/33098994
      OpenUrlPubMed
    36. ↵
      1. Simons D,
      2. Shahab L,
      3. Brown J, et al
      . The association of smoking status with SARS-CoV-2 infection, hospitalisation and mortality from COVID-19: a living rapid evidence review with Bayesian meta-analyses (version 12). Qeios 2021.doi:10.32388/UJR2AW.15
    37. ↵
      1. Patanavanich R,
      2. Glantz SA
      . Smoking is associated with COVID-19 progression: a meta-analysis. In: Nicotine and tobacco research. 22. Oxford University Press, 2020: 1653–6.doi:10.1093/ntr/ntaa082
      OpenUrlCrossRefPubMed
    38. ↵
      COVID-19: protecting health-care workers. COVID-19 prioritization of diagnostic testing. Lancet 2020;395:922.
    39. ↵
      1. CDC
      . The importance of COVID-19 vaccination for healthcare personnel. Available: https://www.cdc.gov/coronavirus/2019-ncov/vaccines/recommendations/hcp.html
    40. ↵
      1. Black JRM,
      2. Bailey C,
      3. Przewrocka J, et al
      . COVID-19: the case for health-care worker screening to prevent Hospital transmission. Lancet 2020;395:1418–20.doi:10.1016/S0140-6736(20)30917-Xpmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/32305073
      OpenUrlCrossRefPubMed
    41. ↵
      1. Rivett L,
      2. Sridhar S,
      3. Sparkes D, et al
      . Screening of healthcare workers for SARS-CoV-2 highlights the role of asymptomatic carriage in COVID-19 transmission. Elife 2020;9:1–20.doi:10.7554/eLife.58728pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/32392129
      OpenUrlCrossRefPubMed
    42. ↵
      1. Shields A,
      2. Faustini SE,
      3. Perez-Toledo M, et al
      . SARS-CoV-2 seroprevalence and asymptomatic viral carriage in healthcare workers: a cross-sectional study. Thorax 2020;75:1089–94.doi:10.1136/thoraxjnl-2020-215414pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/32917840
      OpenUrlAbstract/FREE Full Text
    43. ↵
      1. Bai Y,
      2. Yao L,
      3. Wei T, et al
      . Presumed asymptomatic carrier transmission of COVID-19. JAMA 2020;323:1406–7.doi:10.1001/jama.2020.2565pmid:http://www-ncbi-nlm-nih-gov.ezproxy.u-pec.fr/pubmed/32083643
      OpenUrlCrossRefPubMed

    Supplementary materials

    • Supplementary Data

      This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.

    Footnotes

    • DC-P, LA and EF are joint senior authors.

    • Twitter @PeremiquelPaula, @scabrerajaime, @JordiTrelis, @Carlotasway3, @CMunozMontplet, @CandelaCalle, @stvfdz

    • PP-T and AS-L contributed equally.

    • Contributors EF, DC-P, AP, CC, AC and AS-L contributed to study design. SC, AD, LG, IB, JT, MG, FS, JJ, DC, BC-C, DR-T, CG, AA-P and AP accrued participants and care for blood collection at ICO centres. Laboratory analyses were coordinated by MADL. The questionnaire was designed by DC-P and EF, and revised by PP-T, AS-L, YBM, DC, AP and LA. Questionnaire’s implementation was done by EL, JM, JPR and CM-M. Data were analysed by YB and DC. PP-T, AS-L, YB, DC, LA, and EF interpreted the initial results and designed the tables. All authors contributed to interpretation of results. The first draft of the manuscript was prepared by PP-T and AS-L and EF. PP-T, AS-L, YB, DC, LA, DC-P and EF were the main contributors to the writing of the manuscript. All authors assisted in manuscript review. The co-senior authors had full access to all the data in the study for interpretation and had final responsibility for manuscript generation and review, and the decision to submit for publication. EF is the guarantor.

    • Funding This work was supported by the Catalan Institute of Oncology. PP-T is partially supported by the Instituto de Salud Carlos III (ISCIII), Government of the Kingdom of Spain, cofunded by FEDER funds/European Regional Development Fund (ERDF)-a way to build Europe (CM19/00216). The Ministry of Universities and Research, Government of Catalonia partly supports EF and DCP (2017SGR319) and PP-T, AS-L, YBM, DC and LA (2017SGR1085).

    • Competing interests JJ received research funding from Kyowa Kirin and from Angelini Pharma for congress attendance. The Cancer Epidemiology Research Programme has received grants from Merck & Co., Roche, GSK, IDT, Hologic and Seegene.

    • Patient and public involvement Patients and/or the public were not involved in the design, or conduct, or reporting, or dissemination plans of this research.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.