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

Fabrice Carrat^{1

2}, Xavier de Lamballerie³, Delphine Rahib⁴, Hélène Blanché⁵, Nathanael Lapidus^{1

2}, Fanny Artaud⁶, Sofiane Kab^{7

8}, Adeline Renuy^{7

8}, Fabien Szabo de Edelenyi⁹, Laurence Meyer^{10

11}, Nathalie Lydié⁴, Marie-Aline Charles¹², Pierre-Yves Ancel^{13

14}, Florence Jusot¹⁵, Alexandra Rouquette^{10

11}, Stéphane Priet³, Paola Mariela Saba Villarroel³, Toscane Fourié³, Clovis Lusivika-Nzinga¹, Jérôme Nicol¹, Stephane Legot^{7

8}, Nathalie Druesne-Pecollo⁹, Younes Esseddik⁹, Cindy Lai¹⁶, Jean-Marie Gagliolo¹⁷, Jean-François Deleuze⁵, Nathalie Bajos¹⁸, Gianluca Severi^{6

19}, Mathilde Touvier⁹, Marie Zins^{7

8}; for the SAPRIS and SAPRIS-SERO study groups

Affiliations

¹ Sorbonne Université, Inserm, Institut Pierre-Louis d'Epidémiologie et de Santé Publique, Paris, France.
² Département de Santé Publique, APHP.Sorbonne Université, Paris, France.
³ Unité des Virus Émergents, UVE: Aix Marseille Univ, IRD 190, Inserm 1207, IHU Méditerranée Infection, Marseille, France.
⁴ Santé publique France, Saint-Maurice, France.
⁵ Fondation Jean Dausset-CEPH (Centre d'Etude du Polymorphisme Humain), CEPH-Biobank, Paris, France.
⁶ CESP UMR1018, Université Paris-Saclay, UVSQ, Inserm, Gustave Roussy, Villejuif, France.
⁷ Paris University, Paris, France.
⁸ Paris-Saclay University, Inserm UMS 11, Villejuif, France.
⁹ Sorbonne Paris Nord University, Inserm U1153, INRAE U1125, CNAM, Nutritional Epidemiology Research Team (EREN), Epidemiology and Statistics Research Center, University of Paris (CRESS), Bobigny, France.
¹⁰ Université Paris-Saclay, Inserm, CESP U1018, Le Kremlin Bicêtre, France.
¹¹ Service de Santé Publique, APHP.Paris Saclay, Le Kremlin Bicêtre, France.
¹² Ined, Inserm, EFS, UMS Elfe, Aubervilliers, France.
¹³ Obstetrical, Perinatal and Pediatric Epidemiology Research Team, Center for Epidemiology and Statistics Sorbonne Paris Cité, Inserm U1153, Paris Descartes University, Paris, France.
¹⁴ Clinical Research Unit, Center for Clinical Investigation P1419, Cochin Broca Hôtel-Dieu Hospital, Paris, France.
¹⁵ Université Paris-Dauphine, PSL-Research University, LEDa, Paris, France.
¹⁶ Institut de Santé Publique, Pôle Recherche Clinique, Institut National de la Santé et de la Recherche Médicale, Paris, France.
¹⁷ Inserm, Institut Thématique Santé Publique, Paris, France.
¹⁸ IRIS, Inserm/EHESS/CNRS, Aubervilliers, France.
¹⁹ Department of Statistics, Computer Science and Applications, University of Florence, Florence, Italy.

PMID: 34293141
PMCID: PMC8344948
DOI: 10.1093/ije/dyab110

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

Fabrice Carrat et al. Int J Epidemiol. 2021.

. 2021 Nov 10;50(5):1458-1472.

doi: 10.1093/ije/dyab110.

Authors

Affiliations

¹ Sorbonne Université, Inserm, Institut Pierre-Louis d'Epidémiologie et de Santé Publique, Paris, France.
² Département de Santé Publique, APHP.Sorbonne Université, Paris, France.
³ Unité des Virus Émergents, UVE: Aix Marseille Univ, IRD 190, Inserm 1207, IHU Méditerranée Infection, Marseille, France.
⁴ Santé publique France, Saint-Maurice, France.
⁵ Fondation Jean Dausset-CEPH (Centre d'Etude du Polymorphisme Humain), CEPH-Biobank, Paris, France.
⁶ CESP UMR1018, Université Paris-Saclay, UVSQ, Inserm, Gustave Roussy, Villejuif, France.
⁷ Paris University, Paris, France.
⁸ Paris-Saclay University, Inserm UMS 11, Villejuif, France.
⁹ Sorbonne Paris Nord University, Inserm U1153, INRAE U1125, CNAM, Nutritional Epidemiology Research Team (EREN), Epidemiology and Statistics Research Center, University of Paris (CRESS), Bobigny, France.
¹⁰ Université Paris-Saclay, Inserm, CESP U1018, Le Kremlin Bicêtre, France.
¹¹ Service de Santé Publique, APHP.Paris Saclay, Le Kremlin Bicêtre, France.
¹² Ined, Inserm, EFS, UMS Elfe, Aubervilliers, France.
¹³ Obstetrical, Perinatal and Pediatric Epidemiology Research Team, Center for Epidemiology and Statistics Sorbonne Paris Cité, Inserm U1153, Paris Descartes University, Paris, France.
¹⁴ Clinical Research Unit, Center for Clinical Investigation P1419, Cochin Broca Hôtel-Dieu Hospital, Paris, France.
¹⁵ Université Paris-Dauphine, PSL-Research University, LEDa, Paris, France.
¹⁶ Institut de Santé Publique, Pôle Recherche Clinique, Institut National de la Santé et de la Recherche Médicale, Paris, France.
¹⁷ Inserm, Institut Thématique Santé Publique, Paris, France.
¹⁸ IRIS, Inserm/EHESS/CNRS, Aubervilliers, France.
¹⁹ Department of Statistics, Computer Science and Applications, University of Florence, Florence, Italy.

PMID: 34293141
PMCID: PMC8344948
DOI: 10.1093/ije/dyab110

Erratum in

Corrigendum to: 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.
Carrat F, de Lamballerie X, Rahib D, Blanché H, Lapidus N, Artaud F, Kab S, Renuy A, Szabo de Edelenyi F, Meyer L, Lydié N, Charles MA, Ancel PY, Jusot F, Rouquette A, Priet S, Saba Villarroel PM, Fourié T, Lusivika-Nzinga C, Nicol J, Legot S, Druesne-Pecollo N, Esseddik Y, Lai C, Gagliolo JM, Deleuze JF, Bajos N, Severi G, Touvier M, Zins M; SAPRIS and SAPRIS-SERO study groups. Carrat F, et al. Int J Epidemiol. 2021 Nov 10;50(5):1755. doi: 10.1093/ije/dyab173. Int J Epidemiol. 2021. PMID: 34453524 Free PMC article. No abstract available.

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.

Keywords: COVID-19; SARS-CoV-2; cohort; general population; risk factors; seroprevalence.

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Figures

**Figure 1**
Proportion of participants with COVID-19-like symptoms and a positive ELISA IgG against the SARS-CoV-2 spike protein (ELISA-S) according to the date of the onset of symptoms.

**Figure 2**
Proportion of participants with a positive ELISA IgG against the SARS-CoV-2 spike protein (ELISA-S) by age (weighted estimates)

**Figure 3**
Risk factors of positive ELISA IgG against the SARS-CoV-2 spike protein (ELISA-S) by French region

See this image and copyright information in PMC

References

1. Koopmans M, Haagmans B. Assessing the extent of SARS-CoV-2 circulation through serological studies. Nat Med 2020;26:1171–72. - PubMed
1. Arora RK, Joseph A, Van Wyk J et al. SeroTracker: a global SARS-CoV-2 seroprevalence dashboard. Lancet Infect Dis 2021;21:e75–e76. - PMC - PubMed
1. Bobrovitz N, Aro ra RK, Cao C et al. Global seroprevalence of SARS-SoV-2 antibodies: a systematic review and meta-analysis. medRxiv 2020; doi:10.1101/2020.11.17.20233460, 18 November preprint: not peer-reviewed.
1. Gudbjartsson DF, Norddahl GL, Melsted P et al. Humoral immune response to SARS-CoV-2 in Iceland. N Engl J Med 2020;383:1724–34. - PMC - PubMed
1. Stringhini S, Wisniak A, Piumatti G et al. Seroprevalence of anti-SARS-CoV-2 IgG antibodies in Geneva, Switzerland (SEROCoV-POP): a population-based study. Lancet 2020;396:313–19. - PMC - PubMed

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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

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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

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