Antibody status and cumulative incidence of SARS-CoV-2 infection among adults in three regions of France following the first lockdown and associated risk factors: a multicohort study

  1. Fabrice Carrat
  2. Xavier de Lamballerie
  3. Delphine Rahib
  4. Hélène Blanché
  5. Nathanael Lapidus
  6. Fanny Artaud
  7. Sofiane Kab
  8. Adeline Renuy
  9. Fabien Szabo de Edelenyi
  10. Laurence Meyer
  11. Nathalie Lydié
  12. Marie-Aline Charles
  13. Pierre-Yves Ancel
  14. Florence Jusot
  15. Alexandra Rouquette
  16. Stéphane Priet
  17. Paola Mariela Saba Villarroel
  18. Toscane Fourié
  19. Clovis Lusivika-Nzinga
  20. Jérôme Nicol
  21. Stephane Legot
  22. Nathalie Druesne-Pecollo
  23. Younes Esseddik
  24. Cindy Lai
  25. Jean-Marie Gagliolo
  26. Jean-François Deleuze
  27. Nathalie Bajos
  28. Gianluca Severi
  29. Mathilde Touvier
  30. Marie Zins
  31. for the SAPRIS and SAPRIS-SERO study groups

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Abstract

Background

We aimed to estimate the seropositivity to anti-SARS-CoV-2 antibodies in May–June 2020 after the first lockdown period in adults living in three regions in France and to identify the associated risk factors.

Methods

Between 4 May 2020 and 23 June 2020, 16 000 participants in a survey on COVID-19 from an existing consortium of three general adult population cohorts living in the Ile-de-France (IDF) or Grand Est (GE) (two regions with high rate of COVID-19) or in the Nouvelle-Aquitaine (NA) (with a low rate) were randomly selected to take a dried-blood spot for anti-SARS-CoV-2 antibodies assessment with three different serological methods (ClinicalTrial Identifier #NCT04392388). The primary outcome was a positive anti-SARS-CoV-2 ELISA IgG result against the spike protein of the virus (ELISA-S). Estimates were adjusted using sampling weights and post-stratification methods. Multiple imputation was used to infer the cumulative incidence of SARS-CoV-2 infection with adjustments for imperfect tests accuracies.

Results

The analysis included 14 628 participants, 983 with a positive ELISA-S. The weighted estimates of seropositivity and cumulative incidence were 10.0% [95% confidence interval (CI): 9.1%, 10.9%] and 11.4% (95% CI: 10.1%, 12.8%) in IDF, 9.0% (95% CI: 7.7%, 10.2%) and 9.8% (95% CI: 8.1%, 11.8%) in GE and 3.1% (95% CI: 2.4%, 3.7%) and 2.9% (95% CI: 2.1%, 3.8%) in NA, respectively. Seropositivity was higher in younger participants [odds ratio (OR) = 1.84 (95% CI: 1.79, 6.09) in <40 vs 50–60 years old and OR = 0.56 (95% CI: 0.42, 0.74) in ≥70 vs 50–60 years old)] and when at least one child or adolescent lived in the same household [OR = 1.30 (95% CI: 1.11, 1.53)] and was lower in smokers compared with non-smokers [OR = 0.71 (95% CI: 0.57, 0.89)].

Conclusions

Seropositivity to anti-SARS-CoV-2 antibodies in the French adult population was ≤10% after the first wave. Modifiable and non-modifiable risk factors were identified.

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  1. Version published to 10.1093/ije/dyab110
  2. ScreenIT

    SciScore for 10.1101/2020.09.16.20195693: (What is this?)

    Please note, not all rigor criteria are appropriate for all manuscripts.

    Table 1: Rigor

    Institutional Review Board StatementConsent: 21 Ethical approval and written or electronic informed consent were obtained from each participant before enrolment in the original cohort.
    IRB: The SAPRIS survey was approved by the Inserm ethics committee (approval #20-672 dated March 30, 2020).
    Randomization20 We randomly selected 16,000 of the participants of the SAPRIS survey for this study who agreed to be tested and who were residents from one of the three French administrative regions: Ile-de-France (IDF) or Grand Est (GE), i.e. the two regions with the highest reported cumulated rates of COVID-19 at the end of the lockdown period, or Nouvelle-Aquitaine (NA), a region with a low reported rate.
    Blindingnot detected.
    Power Analysisnot detected.
    Sex as a biological variablenot detected.
    Cell Line Authenticationnot detected.

    Table 2: Resources

    Antibodies
    SentencesResources
    Eluates were processed with a commercial Elisa test (Euroimmun®, Lübeck, Germany) to detect anti-SARS-CoV-2 antibodies (IgG) directed against the S1 domain of the spike protein of the virus (ELISA-S).
    anti-SARS-CoV-2
    suggested: None
    All samples with an ELISA-S test optical density ratio ≥ 0.7 were also tested with an ELISA test to detect IgG antibodies against the SARS-CoV-2 nucleocapsid protein (Euroimmun®, Lübeck, Germany, ELISA-NP) and with an in-house micro-neutralization assay to detect neutralizing anti-SARS-CoV-2 antibodies (SN), as described elsewhere.20 Briefly, we used VeroE6 cells cultured in 96-well microplates, 100 TCID50 of the SARS-CoV-2 strain BavPat1 (courtesy of Pr.
    SARS-CoV-2 nucleocapsid protein
    suggested: (Bioss Cat# bsm-41414M, RRID:AB_2848129)
    Experimental Models: Cell Lines
    SentencesResources
    All samples with an ELISA-S test optical density ratio ≥ 0.7 were also tested with an ELISA test to detect IgG antibodies against the SARS-CoV-2 nucleocapsid protein (Euroimmun®, Lübeck, Germany, ELISA-NP) and with an in-house micro-neutralization assay to detect neutralizing anti-SARS-CoV-2 antibodies (SN), as described elsewhere.20 Briefly, we used VeroE6 cells cultured in 96-well microplates, 100 TCID50 of the SARS-CoV-2 strain BavPat1 (courtesy of Pr.
    VeroE6
    suggested: JCRB Cat# JCRB1819, RRID:CVCL_YQ49)
    Software and Algorithms
    SentencesResources
    Covariates: The association of seroprevalence was evaluated in relation to age, gender, socio-demographic characteristics, BMI, chronic conditions (according to a pre-specified list), tobacco and alcohol use before the lockdown.
    Covariates
    suggested: None
    Other analyses were performed with SAS 9·4 software (SAS Institute Inc.
    SAS Institute
    suggested: (Statistical Analysis System, RRID:SCR_008567)

    Results from OddPub: We did not detect open data. We also did not detect open code. Researchers are encouraged to share open data when possible (see Nature blog).

    Results from LimitationRecognizer: We detected the following sentences addressing limitations in the study:
    Our study has several limitations. First, the primary endpoint is based on a test that does not have a 100% sensitivity and specificity. Thus, certain participants were probably misclassified. We used manufacturer-defined cutoff points for positivity, although the test performance can increased by using other positive and negative cut-off values.38 However, prevalence correction using these reported test performances or by the manufacturer are not applicable to our study, since the use of capillary blood on DBS and the elution procedures do not correspond to the reported experimental conditions. To overcome this limitation, we used a statistical imputation model to estimate the performance of ELISA-S, showing a sensitivity and specificity > 97.5%. The seroprevalence levels and the risk factors identified on multivariable analysis with MI were identical to those obtained with ELISA-S, which supports the robustness of our primary results. The second potential limitation is that the selected adult population in each region may not be representative. Certain social categories were probably under- or over-represented, and although selection and participation biases were accounted for with an appropriate weighting and raking method, our findings cannot be considered to be strictly representative of the general adult population in these regions. Nevertheless, the large number of subjects from all social categories makes it possible to draw robust conclusions on the factors associate...

    Results from TrialIdentifier: We found the following clinical trial numbers in your paper:

    IdentifierStatusTitle
    NCT04392388RecruitingHealth, Perception, Practices, Relations and Social Inequali…

    Results from Barzooka: We did not find any issues relating to the usage of bar graphs.

    Results from JetFighter: We did not find any issues relating to colormaps.

    Results from rtransparent:
    • Thank you for including a conflict of interest statement. Authors are encouraged to include this statement when submitting to a journal.
    • Thank you for including a funding statement. Authors are encouraged to include this statement when submitting to a journal.
    • No protocol registration statement was detected.

    About SciScore

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  3. Version published to 10.1101/2020.09.16.20195693 on medRxiv