{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,28]],"date-time":"2026-02-28T04:32:02Z","timestamp":1772253122670,"version":"3.50.1"},"reference-count":42,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2021,6,4]],"date-time":"2021-06-04T00:00:00Z","timestamp":1622764800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>The World Health Organisation recommends monitoring the circulation of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). We investigated anti\u2013SARS-CoV-2 total immunoglobulin (IgT) antibody seroprevalence and in vitro sero-neutralization in Nancy, France, in spring 2020. Individuals were randomly sampled from electoral lists and invited with household members over 5 years old to be tested for anti\u2013SARS-CoV-2 (IgT, i.e., IgA\/IgG\/IgM) antibodies by ELISA (Bio-rad); the sero-neutralization activity was evaluated on Vero CCL-81 cells. Among 2006 individuals, the raw seroprevalence was 2.1% (95% confidence interval 1.5 to 2.9), was highest for 20- to 34-year-old participants (4.7% (2.3 to 8.4)), within than out of socially deprived area (2.5% vs. 1%, p = 0.02) and with than without intra-family infection (p &lt; 10\u22126). Moreover, 25% of participants presented at least one COVID-19 symptom associated with SARS-CoV-2 positivity (p &lt; 10\u221213), with highly discriminant anosmia or ageusia (odds ratio 27.8 [13.9 to 54.5]); 16.3% (6.8 to 30.7) of seropositive individuals were asymptomatic. Positive sero-neutralization was demonstrated in vitro for 31\/43 seropositive subjects. Regarding the very low seroprevalence, a preventive effect of the lockdown in March 2020 can be assumed for the summer, but a second COVID-19 wave, as expected, could be subsequently observed in this poorly immunized population.<\/jats:p>","DOI":"10.3390\/v13061076","type":"journal-article","created":{"date-parts":[[2021,6,7]],"date-time":"2021-06-07T01:56:40Z","timestamp":1623031000000},"page":"1076","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Seroprevalence of SARS-CoV-2, Symptom Profiles and Sero-Neutralization in a Suburban Area, France"],"prefix":"10.3390","volume":"13","author":[{"given":"Anne","family":"G\u00e9gout Petit","sequence":"first","affiliation":[{"name":"IECL, Universit\u00e9 de Lorraine, CNRS, Inria, F-54000 Nancy, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6861-236X","authenticated-orcid":false,"given":"H\u00e9l\u00e8ne","family":"Jeulin","sequence":"additional","affiliation":[{"name":"LCPME, Universit\u00e9 de Lorraine, CNRS, F-54000 Nancy, France"},{"name":"Laboratoire de Virologie, CHRU de Nancy Brabois, F-54500 Vandoeuvre-l\u00e8s-Nancy, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0209-4576","authenticated-orcid":false,"given":"Karine","family":"Legrand","sequence":"additional","affiliation":[{"name":"CIC Epid\u00e9miologie Clinique, CHRU-Nancy, Inserm, Universit\u00e9 de Lorraine, F-54000 Nancy, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nicolas","family":"Jay","sequence":"additional","affiliation":[{"name":"LORIA, CHRU-Nancy, Universit\u00e9 de Lorraine, CNRS, Inria, LORIA, F-54000 Nancy, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Agathe","family":"Bochnakian","sequence":"additional","affiliation":[{"name":"CIC Epid\u00e9miologie Clinique, CHRU-Nancy, Inserm, Universit\u00e9 de Lorraine, F-54000 Nancy, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Pierre","family":"Vallois","sequence":"additional","affiliation":[{"name":"IECL, Universit\u00e9 de Lorraine, CNRS, Inria, F-54000 Nancy, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Evelyne","family":"Schvoerer","sequence":"additional","affiliation":[{"name":"LCPME, Universit\u00e9 de Lorraine, CNRS, F-54000 Nancy, France"},{"name":"Laboratoire de Virologie, CHRU de Nancy Brabois, F-54500 Vandoeuvre-l\u00e8s-Nancy, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Francis","family":"Guillemin","sequence":"additional","affiliation":[{"name":"CIC Epid\u00e9miologie Clinique, CHRU-Nancy, Inserm, Universit\u00e9 de Lorraine, F-54000 Nancy, France"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2021,6,4]]},"reference":[{"key":"ref_1","unstructured":"World Health Organization (2020, May 28). Population-Based Age-Stratified Seroepidemiological Investigation Protocol for Coronavirus 2019 (COVID-19) Infection. Available online: https:\/\/apps.who.int\/iris\/handle\/10665\/332188."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"102923","DOI":"10.1016\/j.transci.2020.102923","article-title":"Seroprevalence of SARS-CoV-2 antibodies among healthy blood donors in Karachi, Pakistan","volume":"59","author":"Younas","year":"2020","journal-title":"Transfus. Apher. Sci."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"McLaughlin, C.C., Doll, M.K., Morrison, K.T., McLaughlin, W.L., O\u2019Connor, T., Sholukh, A.M., Bossard, E.L., Phasouk, K., Ford, E.S., and Diem, K. (2020). High Community SARS-CoV-2 Antibody Seroprevalence in a Ski Resort Community, Blaine County, Idaho, US. Preliminary Results. medRxiv.","DOI":"10.1101\/2020.07.19.20157198"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"2001031","DOI":"10.2807\/1560-7917.ES.2020.25.24.2001031","article-title":"Prevalence of SARS-CoV-2 specific neutralising antibodies in blood donors from the Lodi Red Zone in Lombardy, Italy, as at 06 April 2020","volume":"25","author":"Percivalle","year":"2020","journal-title":"Eurosurveillance"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"e10","DOI":"10.1016\/j.jinf.2020.09.021","article-title":"Seroprevalence of SARS-CoV-2 significantly varies with age: Preliminary results from a mass population screening","volume":"81","author":"Pagani","year":"2020","journal-title":"J. Infect."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1955","DOI":"10.1093\/infdis\/jiaa579","article-title":"High Seroprevalence of Anti-SARS-CoV-2 Antibodies in Chelsea, Massachusetts","volume":"22","author":"Naranbhai","year":"2020","journal-title":"J. Infect. Dis."},{"key":"ref_7","first-page":"e108","article-title":"Seroprevalence of SARS-CoV-2 IgM and IgG antibodies in an asymptomatic population in Sergipe, Brazil","volume":"4","author":"Borges","year":"2020","journal-title":"Rev. Panam. Salud Publica"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1415","DOI":"10.1093\/ije\/dyaa159","article-title":"COVID-19 and the \u2018rediscovery\u2019 of health inequities","volume":"49","author":"Kawachi","year":"2020","journal-title":"Int. J. Epidemiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"e1390","DOI":"10.1016\/S2214-109X(20)30387-9","article-title":"SARS-CoV-2 antibody prevalence in Brazil: Results from two successive nationwide serological household surveys","volume":"8","author":"Hallal","year":"2020","journal-title":"Lancet Glob. Health"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Liu, W., Liu, L., Kou, G., Zheng, Y., Ding, Y., Ni, W., Wang, Q., Tan, L., Wu, W., and Tang, S. (2020). Evaluation of nucleocapsid and spike protein-based enzyme-linked immunosorbent assays for detecting antibodies against SARS-CoV-2. J. Clin. Microbiol., 58.","DOI":"10.1128\/JCM.00461-20"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Flehmig, B., Schindler, M., Ruetalo, N., Businger, R., Bayer, M., Haage, A., Kirchner, T., Klingel, K., Normann, A., and Pridzun, L. (2020). Persisting Neutralizing Activity to SARS-CoV-2 over Months in Sera of COVID-19 Patients. Viruses, 12.","DOI":"10.3390\/v12121357"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"e1","DOI":"10.1016\/j.cmi.2020.11.013","article-title":"Prevalence of SARS-CoV-2 IgG antibodies in an area of northeastern Italy with a high incidence of COVID-19 cases: A population-based study","volume":"27","author":"Stefanelli","year":"2021","journal-title":"Clin. Microbiol Infect."},{"key":"ref_13","first-page":"1422","article-title":"Rapid isolation and profiling of a diverse panel of human monoclonal antibodies targeting the SARS-CoV-2 spike protein","volume":"26","author":"Zost","year":"2020","journal-title":"bioRxiv"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Dogan, M., Kozhaya, L., Placek, L., Gunter, C.L., Yigit, M., Hardy, R., Plassmeyer, M., Coatney, P., Lillard, K., and Bukhari, Z. (2020). Novel SARS-CoV-2 specific antibody and neutralization assays reveal wide range of humoral immune response during COVID-19. medRxiv.","DOI":"10.1101\/2020.07.07.20148106"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"112937","DOI":"10.1016\/j.jim.2020.112937","article-title":"Comparative analyses of SARS-CoV-2 binding (IgG, IgM, IgA) and neutralizing antibodies from human serum samples","volume":"489","author":"Mazzini","year":"2021","journal-title":"J. Immunol. Methods"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Klingler, J., Weiss, S., Itri, V., Liu, X., Oguntuyo, K.Y., Stevens, C., Ikegame, S., Hung, C.-T., Enyindah-Asonye, G., and Amanat, F. (2020). Role of IgM and IgA Antibodies in the Neutralization of SARS-CoV-2. medRxiv.","DOI":"10.1101\/2020.08.18.20177303"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Sholukh, A.M., Fiore-Gartland, A., Ford, E.S., Hou, Y.J., Tse, V., Kaiser, H., Park, A., Lempp, F.A., Germain, R.S., and Bossard, E. (2020). Evaluation of SARS-CoV-2 neutralization assays for antibody monitoring in natural infection and vaccine trials. medRxiv.","DOI":"10.1101\/2020.12.07.20245431"},{"key":"ref_18","first-page":"2000094","article-title":"First cases of coronavirus disease 2019 (COVID-19) in France: Surveillance, investigations and control measures, January 2020","volume":"25","author":"Stoecklin","year":"2020","journal-title":"Eurosurveillance"},{"key":"ref_19","first-page":"2447","article-title":"Long-term ACE Inhibitor\/ARB Use Is Associated With Severe Renal Dysfunction and Acute Kidney Injury in Patients With Severe COVID-19: Results From a Referral Center Cohort in the Northeast of France","volume":"71","author":"Oussalah","year":"2020","journal-title":"Clin. Infect. Dis Off. Publ Infect. Dis Soc. Am."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"982","DOI":"10.1136\/jech-2011-200311","article-title":"Construction of an adaptable European transnational ecological deprivation index: The French version","volume":"66","author":"Pornet","year":"2012","journal-title":"J. Epidemiol. Community Health"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"208","DOI":"10.1126\/science.abc3517","article-title":"Estimating the burden of SARS-CoV-2 in France","volume":"369","author":"Salje","year":"2020","journal-title":"Science"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"3","DOI":"10.3917\/rdli.053.0003","article-title":"Un indicateur de mesure de la pr\u00e9carit\u00e9 et de la \u00ab sant\u00e9 sociale \u00bb : Le score EPICES: L\u2019exp\u00e9rience des Centres d\u2019examens de sant\u00e9 de l\u2019Assurance maladie","volume":"53","author":"Labbe","year":"2007","journal-title":"Rev. Ires."},{"key":"ref_23","unstructured":"(2021, January 21). Case Definition for Coronavirus Disease 2019 (COVID-19), as of 3 December 2020. European Centre for Disease Prevention and Control. Available online: https:\/\/www.ecdc.europa.eu\/en\/covid-19\/surveillance\/case-definition."},{"key":"ref_24","unstructured":"INSEE (2020, May 28). Population par sexe et groupe d\u2019\u00e2ges [Internet]. Available online: https:\/\/www.insee.fr\/fr\/statistiques\/2381474."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Chavent, M., Kuentz-Simonet, V., Liquet, B., and Saracco, J. (2012). ClustOfVar: An R Package for the Clustering of Variables. J. Stat. Softw., 50.","DOI":"10.18637\/jss.v050.i13"},{"key":"ref_26","unstructured":"Siegel, S., and Castellan, N.J. (1988). Nonparametric Statistics for the Behavioral Sciences, McGraw-Hill."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"165878","DOI":"10.1016\/j.bbadis.2020.165878","article-title":"Insights into SARS-CoV-2 genome, structure, evolution, pathogenesis and therapies: Structural genomics approach","volume":"1866","author":"Naqvi","year":"2020","journal-title":"Biochim. Biophys. Acta BBA\u2014Mol. Basis Dis."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Simula, E.R., Manca, M.A., Jasemi, S., Uzzau, S., Rubino, S., Manchia, P., Bitti, A., Palermo, M., and Sechi, L.A. (2020). HCoV-NL63 and SARS-CoV-2 Share Recognized Epitopes by the Humoral Response in Sera of People Collected Pre- and during CoV-2 Pandemic. Microorganisms, 8.","DOI":"10.3390\/microorganisms8121993"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"778","DOI":"10.1093\/cid\/ciaa310","article-title":"Profiling Early Humoral Response to Diagnose Novel Coronavirus Disease (COVID-19)","volume":"71","author":"Guo","year":"2020","journal-title":"Clin. Infect. Dis."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Poston, D., Weisblum, Y., Wise, H., Templeton, K., Jenks, S., Hatziioannou, T., and Bieniasz, P. (2020). Absence of SARS-CoV-2 neutralizing activity in pre-pandemic sera from individuals with recent seasonal coronavirus infection. Clin Infect Dis., ciaa1803.","DOI":"10.1101\/2020.10.08.20209650"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1038\/s41586-021-03207-w","article-title":"Evolution of Antibody Immunity to SARS-CoV-2","volume":"591","author":"Gaebler","year":"2021","journal-title":"Nature."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"540","DOI":"10.1016\/j.ijid.2020.12.014","article-title":"Dynamic Anti-Spike Protein Antibody Profiles in COVID-19 Patients","volume":"103","author":"Bao","year":"2020","journal-title":"Int. J. Infect. Dis."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"114031","DOI":"10.1016\/j.jviromet.2020.114031","article-title":"Comparison of potency assays to assess SARS-CoV-2 neutralizing antibody capacity in COVID-19 convalescent plasma","volume":"288","author":"Scholz","year":"2021","journal-title":"J. Virol. Methods"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Wiens, K.E., Mawien, P.N., Rumunu, J., Slater, D., Jones, F.K., Moheed, S., Caflish, A., Bior, B.K., Jacob, I.A., and Lako, R.L.L. (2021). Seroprevalence of anti-SARS-CoV-2 IgG antibodies in Juba, South Sudan: A population-based study. medRxiv.","DOI":"10.1101\/2021.03.08.21253009"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Shaw, J.A., Meiring, M., Cummins, T., Chegou, N.N., Claassen, C., Plessis, N.D., Flinn, M., Hiemstra, A., Kleynhans, L., and Leukes, V. (2021). Higher SARS-CoV-2 seroprevalence in workers with lower socioeconomic status in Cape Town, South Africa. PLoS ONE, 16.","DOI":"10.1371\/journal.pone.0247852"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Sykes, W., Mhlanga, L., Swanevelder, R., Glatt, T.N., Grebe, E., Coleman, C., Pieterson, N., Cable, R., Welte, A., and van den Berg, K. (2021). Prevalence of anti-SARS-CoV-2 antibodies among blood donors in Northern Cape, KwaZulu-Natal, Eastern Cape, and Free State provinces of South Africa in January 2021. Res. Sq.","DOI":"10.21203\/rs.3.rs-233375\/v1"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"e144930","DOI":"10.1172\/JCI144930","article-title":"Clinical, laboratory, and temporal predictors of neutralizing antibodies to SARS-CoV-2 among COVID-19 convalescent plasma donor candidates","volume":"131","author":"Boonyaratanakornkit","year":"2021","journal-title":"J. Clin. Investig."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"917","DOI":"10.1038\/s41591-021-01318-5","article-title":"Sensitivity of infectious SARS-CoV-2 B.1.1.7 and B.1.351 variants to neutralizing antibodies","volume":"27","author":"Planas","year":"2021","journal-title":"Nat. Med."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"143","DOI":"10.2307\/3654932","article-title":"Determinants of Electoral Non-Registration and Sensitive Neighbourhoods in France","volume":"59","author":"Shon","year":"2004","journal-title":"Population"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Martin, J., Klapsa, D., Wilton, T., Zambon, M., Bentley, E., Bujaki, E., Fritzsche, M., Mate, R., and Majumdar, M. (2020). Tracking SARS-CoV-2 in Sewage: Evidence of Changes in Virus Variant Predominance during COVID-19 Pandemic. Viruses, 12.","DOI":"10.3390\/v12101144"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1103","DOI":"10.1126\/science.abg7404","article-title":"Immunity to SARS-CoV-2 variants of concern","volume":"371","author":"Altmann","year":"2021","journal-title":"Science"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1016\/j.tim.2020.11.002","article-title":"COVID-19 Antibody Tests: A Valuable Public Health Tool with Limited Relevance to Individuals","volume":"29","author":"West","year":"2021","journal-title":"Trends Microbiol."}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/6\/1076\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T06:11:05Z","timestamp":1760163065000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/6\/1076"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6,4]]},"references-count":42,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2021,6]]}},"alternative-id":["v13061076"],"URL":"https:\/\/doi.org\/10.3390\/v13061076","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2021.02.10.21250862","asserted-by":"object"}]},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,6,4]]}}}