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Abstract

Background

Serological surveys have been the gold standard to estimate numbers of SARS-CoV-2 infections, the dynamics of the epidemic, and disease severity. Serological assays have decaying sensitivity with time that can bias their results, but there is a lack of guidelines to account for this phenomenon for SARS-CoV-2.

Aim

Our goal was to assess the sensitivity decay of seroassays for detecting SARS-CoV-2 infections, the dependence of this decay on assay characteristics, and to provide a simple method to correct for this phenomenon.

Methods

We performed a systematic review and meta-analysis of SARS-CoV-2 serology studies. We included studies testing previously diagnosed, unvaccinated individuals, and excluded studies of cohorts highly unrepresentative of the general population (e.g. hospitalised patients).

Results

Of the 488 screened studies, 76 studies reporting on 50 different seroassays were included in the analysis. Sensitivity decay depended strongly on the antigen and the analytic technique used by the assay, with average sensitivities ranging between 26% and 98% at 6 months after infection, depending on assay characteristics. We found that a third of the included assays departed considerably from manufacturer specifications after 6 months.

Conclusions

Seroassay sensitivity decay depends on assay characteristics, and for some types of assays, it can make manufacturer specifications highly unreliable. We provide a tool to correct for this phenomenon and to assess the risk of decay for a given assay. Our analysis can guide the design and interpretation of serosurveys for SARS-CoV-2 and other pathogens and quantify systematic biases in the existing serology literature.

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2023-05-25
2024-04-24
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2023.28.21.2200809
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References

  1. Brazeau NF, Verity R, Jenks S, Fu H, Whittaker C, Winskill P, et al. Estimating the COVID-19 infection fatality ratio accounting for seroreversion using statistical modelling. Commun Med (Lond). 2022;2(1):54.  https://doi.org/10.1038/s43856-022-00106-7  PMID: 35603270 
  2. Herrera-Esposito D, de Los Campos G. Age-specific rate of severe and critical SARS-CoV-2 infections estimated with multi-country seroprevalence studies. BMC Infect Dis. 2022;22(1):311.  https://doi.org/10.1186/s12879-022-07262-0  PMID: 35351016 
  3. Ioannidis JPA. Reconciling estimates of global spread and infection fatality rates of COVID-19: An overview of systematic evaluations. Eur J Clin Invest. 2021;51(5):e13554.  https://doi.org/10.1111/eci.13554  PMID: 33768536 
  4. Levin AT, Hanage WP, Owusu-Boaitey N, Cochran KB, Walsh SP, Meyerowitz-Katz G. Assessing the age specificity of infection fatality rates for COVID-19: systematic review, meta-analysis, and public policy implications. Eur J Epidemiol. 2020;35(12):1123-38.  https://doi.org/10.1007/s10654-020-00698-1  PMID: 33289900 
  5. O’Driscoll M, Ribeiro Dos Santos G, Wang L, Cummings DAT, Azman AS, Paireau J, et al. Age-specific mortality and immunity patterns of SARS-CoV-2. Nature. 2021;590(7844):140-5.  https://doi.org/10.1038/s41586-020-2918-0  PMID: 33137809 
  6. Jones JM, Stone M, Sulaeman H, Fink RV, Dave H, Levy ME, et al. Estimated US infection- and vaccine-induced SARS-CoV-2 seroprevalence based on blood donations, July 2020-May 2021. JAMA. 2021;326(14):1400-9.  https://doi.org/10.1001/jama.2021.15161  PMID: 34473201 
  7. Madhi SA, Kwatra G, Myers JE, Jassat W, Dhar N, Mukendi CK, et al. Population immunity and Covid-19 severity with Omicron variant in South Africa. N Engl J Med. 2022;386(14):1314-26.  https://doi.org/10.1056/NEJMoa2119658  PMID: 35196424 
  8. Santos-Hövener C, Neuhauser HK, Rosario AS, Busch M, Schlaud M, Hoffmann R, et al. Serology- and PCR-based cumulative incidence of SARS-CoV-2 infection in adults in a successfully contained early hotspot (CoMoLo study), Germany, May to June 2020. Euro Surveill. 2020;25(47):2001752.  https://doi.org/10.2807/1560-7917.ES.2020.25.47.2001752  PMID: 33243353 
  9. Chapman LAC, Barnard RC, Russell TW, Abbott S, van Zandvoort K, Davies NG, et al. Unexposed populations and potential COVID-19 hospitalisations and deaths in European countries as per data up to 21 November 2021. Euro Surveill. 2022;27(1):2101038.  https://doi.org/10.2807/1560-7917.ES.2022.27.1.2101038  PMID: 34991776 
  10. Duarte N, Yanes-Lane M, Arora RK, Bobrovitz N, Liu M, Bego MG, et al. Adapting serosurveys for the SARS-CoV-2 vaccine era. Open Forum Infect Dis. 2021;9(2):ofab632.  https://doi.org/10.1093/ofid/ofab632  PMID: 35103246 
  11. Gaebler C, Wang Z, Lorenzi JCC, Muecksch F, Finkin S, Tokuyama M, et al. Evolution of antibody immunity to SARS-CoV-2. Nature. 2021;591(7851):639-44.  https://doi.org/10.1038/s41586-021-03207-w  PMID: 33461210 
  12. Choe PG, Kim KH, Kang CK, Suh HJ, Kang E, Lee SY, et al. Antibody responses 8 months after asymptomatic or mild SARS-CoV-2 infection. Emerg Infect Dis. 2021;27(3):928-31.  https://doi.org/10.3201/eid2703.204543  PMID: 33350923 
  13. Peluso MJ, Takahashi S, Hakim J, Kelly JD, Torres L, Iyer NS, et al. SARS-CoV-2 antibody magnitude and detectability are driven by disease severity, timing, and assay. Sci Adv. 2021;7(31):eabh3409.  https://doi.org/10.1126/sciadv.abh3409  PMID: 34330709 
  14. Scheiblauer H, Nübling CM, Wolf T, Khodamoradi Y, Bellinghausen C, Sonntagbauer M, et al. Antibody response to SARS-CoV-2 for more than one year - kinetics and persistence of detection are predominantly determined by avidity progression and test design. J Clin Virol. 2022;146:105052.  https://doi.org/10.1016/j.jcv.2021.105052  PMID: 34920374 
  15. Lohse S, Sternjakob-Marthaler A, Lagemann P, Schöpe J, Rissland J, Seiwert N, et al. German federal-state-wide seroprevalence study of 1st SARS-CoV-2 pandemic wave shows importance of long-term antibody test performance. Commun Med (Lond). 2022;2(1):52.  https://doi.org/10.1038/s43856-022-00100-z  PMID: 35603305 
  16. Shioda K, Lau MSY, Kraay ANM, Nelson KN, Siegler AJ, Sullivan PS, et al. Estimating the cumulative incidence of SARS-CoV-2 infection and the infection fatality ratio in light of waning antibodies. Epidemiology. 2021;32(4):518-24.  https://doi.org/10.1097/EDE.0000000000001361  PMID: 33935138 
  17. Bergeri I, Whelan MG, Ware H, Subissi L, Nardone A, Lewis HC, et al. Global SARS-CoV-2 seroprevalence from January 2020 to April 2022: A systematic review and meta-analysis of standardized population-based studies. PLoS Med. 2022;19(11):e1004107.  https://doi.org/10.1371/journal.pmed.1004107  PMID: 36355774 
  18. Bond KA, Williams E, Nicholson S, Lim S, Johnson D, Cox B, et al. Longitudinal evaluation of laboratory-based serological assays for SARS-CoV-2 antibody detection. Pathology. 2021;53(6):773-9.  https://doi.org/10.1016/j.pathol.2021.05.093  PMID: 34412859 
  19. Flower B, Brown JC, Simmons B, Moshe M, Frise R, Penn R, et al. Clinical and laboratory evaluation of SARS-CoV-2 lateral flow assays for use in a national COVID-19 seroprevalence survey. Thorax. 2020;75(12):1082-8.  https://doi.org/10.1136/thoraxjnl-2020-215732  PMID: 32796119 
  20. McCance K, Wise H, Simpson J, Batchelor B, Hale H, McDonald L, et al. Evaluation of SARS-CoV-2 antibody point of care devices in the laboratory and clinical setting. PLoS One. 2022;17(3):e0266086.  https://doi.org/10.1371/journal.pone.0266086  PMID: 35358263 
  21. Perez-Saez J, Zaballa ME, Yerly S, Andrey DO, Meyer B, Eckerle I, et al. , Specchio-COVID19 Study Group. Persistence of anti-SARS-CoV-2 antibodies: immunoassay heterogeneity and implications for serosurveillance. Clin Microbiol Infect. 2021;27(11):1695.e7-12.  https://doi.org/10.1016/j.cmi.2021.06.040  PMID: 34245905 
  22. Chia WN, Zhu F, Ong SWX, Young BE, Fong SW, Le Bert N, et al. Dynamics of SARS-CoV-2 neutralising antibody responses and duration of immunity: a longitudinal study. Lancet Microbe. 2021;2(6):e240-9.  https://doi.org/10.1016/S2666-5247(21)00025-2  PMID: 33778792 
  23. Di Germanio C, Simmons G, Kelly K, Martinelli R, Darst O, Azimpouran M, et al. SARS-CoV-2 antibody persistence in COVID-19 convalescent plasma donors: Dependency on assay format and applicability to serosurveillance. Transfusion. 2021;61(9):2677-87.  https://doi.org/10.1111/trf.16555  PMID: 34121205 
  24. He Z, Ren L, Yang J, Guo L, Feng L, Ma C, et al. Seroprevalence and humoral immune durability of anti-SARS-CoV-2 antibodies in Wuhan, China: a longitudinal, population-level, cross-sectional study. Lancet. 2021;397(10279):1075-84.  https://doi.org/10.1016/S0140-6736(21)00238-5  PMID: 33743869 
  25. Lumley SF, Wei J, O’Donnell D, Stoesser NE, Matthews PC, Howarth A, et al. The duration, dynamics, and determinants of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) antibody responses in individual healthcare workers. Clin Infect Dis. 2021;73(3):e699-709.  https://doi.org/10.1093/cid/ciab004  PMID: 33400782 
  26. Wheatley AK, Juno JA, Wang JJ, Selva KJ, Reynaldi A, Tan HX, et al. Evolution of immune responses to SARS-CoV-2 in mild-moderate COVID-19. Nat Commun. 2021;12(1):1162.  https://doi.org/10.1038/s41467-021-21444-5  PMID: 33608522 
  27. Levin AT, Owusu-Boaitey N, Pugh S, Fosdick BK, Zwi AB, Malani A, et al. Assessing the burden of COVID-19 in developing countries: systematic review, meta-analysis and public policy implications. BMJ Glob Health. 2022;7(5):e008477.  https://doi.org/10.1136/bmjgh-2022-008477  PMID: 35618305 
  28. Fei Y, Xu H, Zhang X, Musa SS, Zhao S, He D. Seroprevalence and infection attack rate of COVID-19 in Indian cities. Infect Dis Model. 2022;7(2):25-32.  https://doi.org/10.1016/j.idm.2022.03.001  PMID: 35287277 
  29. Cromer D, Juno JA, Khoury D, Reynaldi A, Wheatley AK, Kent SJ, et al. Prospects for durable immune control of SARS-CoV-2 and prevention of reinfection. Nat Rev Immunol. 2021;21(6):395-404.  https://doi.org/10.1038/s41577-021-00550-x  PMID: 33927374 
  30. Davies NG, Abbott S, Barnard RC, Jarvis CI, Kucharski AJ, Munday JD, et al. Estimated transmissibility and impact of SARS-CoV-2 lineage B.1.1.7 in England. Science. 2021;372(6538):eabg3055.  https://doi.org/10.1126/science.abg3055  PMID: 33658326 
  31. Carpenter B, Gelman A, Hoffman MD, Lee D, Goodrich B, Betancourt M, et al. Stan: a probabilistic programming language. J Stat Softw. 2017;76(1):1-32.  https://doi.org/10.18637/jss.v076.i01  PMID: 36568334 
  32. Guidotti E, Ardia D. COVID-19 data hub. J Open Source Softw. 2020;5(51):2376.  https://doi.org/10.21105/joss.02376 
  33. Arora RK, Joseph A, Van Wyk J, Rocco S, Atmaja A, May E, et al. SeroTracker: a global SARS-CoV-2 seroprevalence dashboard. Lancet Infect Dis. 2021;21(4):e75-6.  https://doi.org/10.1016/S1473-3099(20)30631-9  PMID: 32763195 
  34. Karger AB, Brien JD, Christen JM, Dhakal S, Kemp TJ, Klein SL, et al. The serological sciences network (SeroNet) for COVID-19: depth and breadth of serology assays and plans for assay harmonization. MSphere. 2022;7(4):e0019322.  https://doi.org/10.1128/msphere.00193-22  PMID: 35703544 
  35. Axfors C, Ioannidis JPA. Infection fatality rate of COVID-19 in community-dwelling elderly populations. Eur J Epidemiol. 2022;37(3):235-49.  https://doi.org/10.1007/s10654-022-00853-w  PMID: 35306604 
  36. Freitas NEM, Santos EF, Leony LM, Silva ÂAO, Daltro RT, Vasconcelos LCM, et al. Double-antigen sandwich ELISA based on chimeric antigens for detection of antibodies to Trypanosoma cruzi in human sera. PLoS Negl Trop Dis. 2022;16(3):e0010290.  https://doi.org/10.1371/journal.pntd.0010290  PMID: 35275913 
  37. Wu FB, Ouyan HQ, Tang XY, Zhou ZX. Double-antigen sandwich time-resolved immunofluorometric assay for the detection of anti-hepatitis C virus total antibodies with improved specificity and sensitivity. J Med Microbiol. 2008;57(Pt 8):947-53.  https://doi.org/10.1099/jmm.0.47835-0  PMID: 18628493 
  38. Stringhini S, Zaballa ME, Pullen N, Perez-Saez J, de Mestral C, Loizeau AJ, et al. Seroprevalence of anti-SARS-CoV-2 antibodies 6 months into the vaccination campaign in Geneva, Switzerland, 1 June to 7 July 2021. Euro Surveill. 2021;26(43):2100830.  https://doi.org/10.2807/1560-7917.ES.2021.26.43.2100830  PMID: 34713799 
  39. Theel ES, Slev P, Wheeler S, Couturier MR, Wong SJ, Kadkhoda K. The role of antibody testing for SARS-CoV-2: is there one? J Clin Microbiol. 2020;58(8):e00797-20.  https://doi.org/10.1128/JCM.00797-20  PMID: 32350047 
  40. Pérez-Olmeda M, Saugar JM, Fernández-García A, Pérez-Gómez B, Pollán M, Avellón A, et al. Evolution of antibodies against SARS-CoV-2 over seven months: Experience of the nationwide seroprevalence ENE-COVID study in Spain. J Clin Virol. 2022;149:105130.  https://doi.org/10.1016/j.jcv.2022.105130  PMID: 35305377 
  41. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372(71):n71.  https://doi.org/10.1136/bmj.n71  PMID: 33782057 
  42. Mallon PWG, Tinago W, Leon AG, McCann K, Kenny G, McGettrick P, et al. Dynamic change and clinical relevance of postinfectious SARS-CoV-2 antibody responses. Open Forum Infect Dis. 2021;8(8):ofab122.  https://doi.org/10.1093/ofid/ofab122  PMID: 34377721 
  43. Eberhardt KA, Dewald F, Heger E, Gieselmann L, Vanshylla K, Wirtz M, et al. Evaluation of a new spike (S)-protein-based commercial immunoassay for the detection of anti-SARS-CoV-2 IgG. Microorganisms. 2021;9(4):733.  https://doi.org/10.3390/microorganisms9040733  PMID: 33807490 
  44. McGregor R, Craigie A, Jack S, Upton A, Moreland NJ, Ussher J. The persistence of neutralising antibodies up to 11 months after SARS-CoV-2 infection in the southern region of New Zealand. medRxiv; 2021 [cited 2022 Sep 7]. p. 2021.10.26.21265501. Available from: https://www.medrxiv.org/content/10.1101/2021.10.26.21265501v1 https://doi.org/10.1101/2021.10.26.21265501  https://doi.org/10.1101/2021.10.26.21265501 
  45. Knabl L, Mitra T, Kimpel J, Rössler A, Volland A, Walser A, et al. High SARS-CoV-2 seroprevalence in children and adults in the Austrian ski resort of Ischgl. Commun Med (Lond). 2021;1(1):4.  https://doi.org/10.1038/s43856-021-00007-1  PMID: 34870284 
  46. Pollán M, Pérez-Gómez B, Pastor-Barriuso R, Oteo J, Hernán MA, Pérez-Olmeda M, et al. Prevalence of SARS-CoV-2 in Spain (ENE-COVID): a nationwide, population-based seroepidemiological study. Lancet. 2020;396(10250):535-44.  https://doi.org/10.1016/S0140-6736(20)31483-5  PMID: 32645347 
  47. Samore MH, Looney A, Orleans B, Greene T, Seegert N, Delgado JC, et al. Probability-based estimates of severe acute respiratory syndrome coronavirus 2 seroprevalence and detection fraction, Utah, USA. Emerg Infect Dis. 2021;27(11):2786-94.  https://doi.org/10.3201/eid2711.204435  PMID: 34469285 
  48. Tadesse EB, Endris AA, Solomon H, Alayu M, Kebede A, Eshetu K, et al. Seroprevalence and risk factors for SARS-CoV-2 Infection in selected urban areas in Ethiopia: a cross-sectional evaluation during July 2020. Int J Infect Dis. 2021;111:179-85.  https://doi.org/10.1016/j.ijid.2021.08.028  PMID: 34411720 
  49. Murhekar MV, Bhatnagar T, Selvaraju S, Saravanakumar V, Thangaraj JWV, Shah N, et al. SARS-CoV-2 antibody seroprevalence in India, August-September, 2020: findings from the second nationwide household serosurvey. Lancet Glob Health. 2021;9(3):e257-66.  https://doi.org/10.1016/S2214-109X(20)30544-1  PMID: 33515512 
  50. Ayub T, Raja MW, Khan SMS, Haq I, Qureshi MA, Majid S, et al. Seroprevalence of SARS CoV 2 specific Ig G antibodies in District Srinagar, Kashmir: a population based study. Int J Community Med Public Health. 2021;8(4):1792.  https://doi.org/10.18203/2394-6040.ijcmph20211236 
  51. Khan SMS, Qurieshi MA, Haq I, Majid S, Ahmad J, Ayub T, et al. Seroprevalence of SARS-CoV-2-specific IgG antibodies in Kashmir, India, 7 months after the first reported local COVID-19 case: results of a population-based seroprevalence survey from October to November 2020. BMJ Open. 2021;11(9):e053791.  https://doi.org/10.1136/bmjopen-2021-053791  PMID: 34556519 
  52. Murhekar MV, Bhatnagar T, Thangaraj JWV, Saravanakumar V, Santhosh Kumar M, Selvaraju S, et al. , ICMR serosurveillance group. Seroprevalence of IgG antibodies against SARS-CoV-2 among the general population and healthcare workers in India, June-July 2021: A population-based cross-sectional study. PLoS Med. 2021;18(12):e1003877.  https://doi.org/10.1371/journal.pmed.1003877  PMID: 34890407 
  53. Murhekar MV, Bhatnagar T, Thangaraj JWV, Saravanakumar V, Kumar MS, Selvaraju S, et al. SARS-CoV-2 seroprevalence among the general population and healthcare workers in India, December 2020-January 2021. Int J Infect Dis. 2021;108:145-55.  https://doi.org/10.1016/j.ijid.2021.05.040  PMID: 34022338 
  54. Thiruvengadam R, Chattopadhyay S, Mehdi F, Desiraju BK, Chaudhuri S, Singh S, et al. Longitudinal serology of SARS-CoV-2-infected individuals in India: a prospective cohort study. Am J Trop Med Hyg. 2021;105(1):66-72.  https://doi.org/10.4269/ajtmh.21-0164  PMID: 34003792 
  55. Tea F, Ospina Stella A, Aggarwal A, Ross Darley D, Pilli D, Vitale D, et al. SARS-CoV-2 neutralizing antibodies: Longevity, breadth, and evasion by emerging viral variants. PLoS Med. 2021;18(7):e1003656.  https://doi.org/10.1371/journal.pmed.1003656  PMID: 34228725 
  56. Garritsen A, Scholzen A, van den Nieuwenhof DWA, Smits APF, Datema ES, van Galen LS, et al. Two-tiered SARS-CoV-2 seroconversion screening in the Netherlands and stability of nucleocapsid, spike protein domain 1 and neutralizing antibodies. Infect Dis (Lond). 2021;53(7):498-512.  https://doi.org/10.1080/23744235.2021.1893378  PMID: 33684020 
  57. Muecksch F, Wise H, Batchelor B, Squires M, Semple E, Richardson C, et al. Longitudinal serological analysis and neutralizing antibody levels in coronavirus disease 2019 convalescent patients. J Infect Dis. 2021;223(3):389-98.  https://doi.org/10.1093/infdis/jiaa659  PMID: 33140086 
  58. Kahre E, Galow L, Unrath M, Haag L, Blankenburg J, Dalpke AH, et al. Kinetics and seroprevalence of SARS-CoV-2 antibodies: a comparison of 3 different assays. Sci Rep. 2021;11(1):14893.  https://doi.org/10.1038/s41598-021-94453-5  PMID: 34290329 
  59. Kumar MS, Thangaraj JWV, Saravanakumar V, Selvaraju S, Kumar CPG, Sabarinathan R, et al. Monitoring the trend of SARS-CoV-2 seroprevalence in Chennai, India, July and October 2020. Trans R Soc Trop Med Hyg. 2021;115(11):1350-2.
  60. Šmigelskas K, Petrikonis K, Kasiulevičius V, Kalėdienė R, Jakaitienė A, Kaselienė S, et al. SARS-CoV-2 seroprevalence in Lithuania: results of national population survey. Acta Med Litu. 2021;28(1):48-58.  https://doi.org/10.15388/Amed.2020.28.1.2  PMID: 34393628 
  61. Kennedy JL, Forrest JC, Young SG, Amick B, Williams M, James L, et al. Temporal variations in seroprevalence of severe acute respiratory syndrome coronavirus 2 infections by race and ethnicity in Arkansas. Open Forum Infect Dis. 2022;9(5):ofac154.  https://doi.org/10.1093/ofid/ofac154  PMID: 35493126 
  62. Sullivan PS, Siegler AJ, Shioda K, Hall EW, Bradley H, Sanchez T, et al. Severe acute respiratory syndrome coronavirus 2 cumulative incidence, United States, August 2020-December 2020. Clin Infect Dis. 2022;74(7):1141-50.  https://doi.org/10.1093/cid/ciab626  PMID: 34245245 
  63. Bushnik T, Earl S, Clark J, Cabot J. COVID-19 infection in the Canadian household population. Health Rep. 2022;33(4):24-33."https://pubmed.ncbi.nlm.nih.gov/35442611" PMID: 35442611 
  64. Schonfeld D, Fernández H, Ramírez J, Acosta D, Becerra J, Wettstein M, et al. SARS-CoV-2 seroprevalence in the city of Puerto Madryn: Underdiagnosis and relevance of children in the pandemic. PLoS One. 2022;17(3):e0263679.  https://doi.org/10.1371/journal.pone.0263679  PMID: 35286328 
  65. Ojeda DS, Gonzalez Lopez Ledesma MM, Pallarés HM, Costa Navarro GS, Sanchez L, Perazzi B, et al. Emergency response for evaluating SARS-CoV-2 immune status, seroprevalence and convalescent plasma in Argentina. PLoS Pathog. 2021;17(1):e1009161.  https://doi.org/10.1371/journal.ppat.1009161  PMID: 33444413 
  66. Longueira Y, Polo ML, Turk G, Laufer N, InViV working group, Biobanco de Enfermedades Infecciosas Colección COVID19 working group. Dynamics of SARS-CoV-2-specific antibodies among COVID19 biobank donors in Argentina. Heliyon. 2021;7(10):e08140.  https://doi.org/10.1016/j.heliyon.2021.e08140  PMID: 34642643 
  67. Dorigatti I, Lavezzo E, Manuto L, Ciavarella C, Pacenti M, Boldrin C, et al. SARS-CoV-2 antibody dynamics and transmission from community-wide serological testing in the Italian municipality of Vo’. Nat Commun. 2021;12(1):4383.  https://doi.org/10.1038/s41467-021-24622-7  PMID: 34282139 
  68. Kar SS, Sarkar S, Murali S, Dhodapkar R, Joseph NM, Aggarwal R. Prevalence and time trend of SARS-CoV-2 infection in Puducherry, India, August-October 2020. Emerg Infect Dis. 2021;27(2):666-9.  https://doi.org/10.3201/eid2702.204480  PMID: 33496645 
  69. Herlinda O, Bella A, Kusnadi G, Swasthika Nurshadrina D, Thoriq Akbar M, Nida S, et al. Seroprevalence of antibodies against SARS-Cov-2 in the high impacted sub-district in Jakarta, Indonesia. PLoS One. 2021;16(12):e0261931.  https://doi.org/10.1371/journal.pone.0261931  PMID: 34941968 
  70. Laxmaiah A, Rao NM, Arlappa N, Babu J, Kumar PU, Singh P, et al. SARS-CoV-2 seroprevalence in the city of Hyderabad, India in early 2021. IJID Reg. 2022;2:1-7.  https://doi.org/10.1016/j.ijregi.2021.10.009  PMID: 35721436 
  71. National Institute of Infectious Diseases. 2021 seroepidemiological survey report for novel coronavirus infection. Tokyo: National Institute of Infectious Diseases. [Accessed: 7 Sep 2022]. Japanese. Available from: https://www.mhlw.go.jp/content/10900000/000934787.pdf
  72. Kshatri JS, Bhattacharya D, Kanungo S, Giri S, Palo SK, Parai D, et al. Serological surveys to inform SARS-CoV-2 epidemic curve: a cross-sectional study from Odisha, India. Sci Rep. 2021;11(1):10551.  https://doi.org/10.1038/s41598-021-89877-y  PMID: 34006960 
  73. Kshatri JS, Bhattacharya D, Praharaj I, Mansingh A, Parai D, Kanungo S, et al. Seroprevalence of SARS-CoV-2 in Bhubaneswar, India: findings from three rounds of community surveys. Epidemiol Infect. 2021;149:e139.  https://doi.org/10.1017/S0950268821000972  PMID: 33902776 
  74. Gudbjartsson DF, Norddahl GL, Melsted P, Gunnarsdottir K, Holm H, Eythorsson E, et al. Humoral immune response to SARS-CoV-2 in Iceland. N Engl J Med. 2020;383(18):1724-34.  https://doi.org/10.1056/NEJMoa2026116  PMID: 32871063 
  75. Goto A, Go H, Miyakawa K, Yamaoka Y, Ohtake N, Kubo S, et al. Sustained neutralizing antibodies 6 months following infection in 376 Japanese COVID-19 survivors. Front Microbiol. 2021;12:661187.  https://doi.org/10.3389/fmicb.2021.661187  PMID: 34025615 
  76. Alkharaan H, Bayati S, Hellström C, Aleman S, Olsson A, Lindahl K, et al. Persisting salivary IgG against SARS-CoV-2 at 9 months after mild COVID-19: a complementary approach to population surveys. J Infect Dis. 2021;224(3):407-14.  https://doi.org/10.1093/infdis/jiab256  PMID: 33978762 
  77. Sharma N, Sharma P, Basu S, Saxena S, Chawla R, Dushyant K, et al. The seroprevalence of severe acute respiratory syndrome coronavirus 2 in Delhi, India: a repeated population-based seroepidemiological study. Trans R Soc Trop Med Hyg. 2022;116(3):242-51.  https://doi.org/10.1093/trstmh/trab109  PMID: 34339514 
  78. Satpati PS, Sarangi SS, Gantait KS, Endow S, Mandal NC, Panchanan K, et al. Sero-surveillance (IgG) of SARS-CoV-2 among asymptomatic general population of Paschim Medinipur, West Bengal, India. medRxiv; 2020.09.12.20193219 .  https://doi.org/10.1101/2020.09.12.20193219 
  79. Warszawski J, Beaumont AL, Seng R, de Lamballerie X, Rahib D, Lydié N, et al. Prevalence of SARS-Cov-2 antibodies and living conditions: the French national random population-based EPICOV cohort. BMC Infect Dis. 2022;22(1):41.  https://doi.org/10.1186/s12879-021-06973-0  PMID: 35000580 
  80. Carrat F, de Lamballerie X, Rahib D, Blanché H, Lapidus N, Artaud F, et al. 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. Int J Epidemiol. 2021;50(5):1458-72.  https://doi.org/10.1093/ije/dyab110  PMID: 34293141 
  81. Ghose A, Bhattacharya S, Karthikeyan AS, Kudale A, Monteiro JM, Joshi A, et al. Community prevalence of antibodies to SARS-CoV-2 and correlates of protective immunity in an Indian metropolitan city. medRxiv; 2020.11.17.20228155 .  https://doi.org/10.1101/2020.11.17.20228155 
  82. Gornyk D, Harries M, Glöckner S, Strengert M, Kerrinnes T, Bojara G, et al. SARS-CoV-2 seroprevalence in Germany - A population based sequential study in five regions. Rochester, NY: Social Science Research Network; 2021. Preprint. Available from:
  83. Robert Koch Institute (RKI). Corona-Monitoring lokal. [Local corona monitoring]. Berlin: RKI. [Accessed: 7 Sep 2022]. German. Available from: https://www.rki.de/DE/Content/Gesundheitsmonitoring/Studien/cml-studie/Factsheet_Straubing.html
  84. Alvim RGF, Lima TM, Rodrigues DAS, Marsili FF, Bozza VBT, Higa LM, et al. From a recombinant key antigen to an accurate, affordable serological test: Lessons learnt from COVID-19 for future pandemics. Biochem Eng J. 2022;186:108537.  https://doi.org/10.1016/j.bej.2022.108537  PMID: 35874089 
  85. Vanshylla K, Cristanziano VD, Kleipass F, Dewald F, Schommers P, Gieselmann L, et al. Kinetics and correlates of the neutralizing antibody response to SARS-CoV-2. bioRxiv; 2021.01.26.428207. https://doi.org/10.1101/2021.01.26.428207
  86. Parrott JC, Maleki AN, Vassor VE, Osahan S, Hsin Y, Sanderson M, et al. Prevalence of SARS-CoV-2 antibodies in New York City adults, June-October 2020: a population-based survey. J Infect Dis. 2021;224(2):188-95.  https://doi.org/10.1093/infdis/jiab296  PMID: 34086923 
  87. Ärzteblatt DÄG Redaktion Deutsches. SARS-CoV-2 Seroprevalence in Germany. A population-based sequential study in seven Regions (03.12.2021). Dtsch Arztebl Int. 2021;118:824. https://doi.org/10.3238/arztebl.m2021.0364
  88. Robert Koch Institute (RKI). Seroepidemiologische Studie zur Abschätzung der Verbreitung von SARS-CoV-2 in der Bevölkerung an besonders betroffenen Orten in Deutschland. Corona-Monitoring local. Abschlussbericht 2021. [Seroepidemiological study to estimate the spread of SARS-CoV-2 in the population in particularly affected locations in Germany. Llocal corona monitoring. Final report 2021]. Berlin: RKI; 2021. German. Available from: https://www.rki.de/DE/Content/Gesundheitsmonitoring/Studien/cml-studie/Dokumente/Abschlussbericht_2021.pdf?__blob=publicationFile
  89. Neuhauser H, Schaffrath Rosario A, Butschalowsky H, Haller S, Hoebel J, Michel J, et al. Germany’s low SARS-CoV-2 seroprevalence confirms effective containment in 2020: Results of the nationwide RKI-SOEP study. medRxiv. 2021.11.22.21266711.  https://doi.org/10.1101/2021.11.22.21266711  https://doi.org/10.1101/2021.11.22.21266711 
  90. Ward H, Atchison C, Whitaker M, Ainslie KEC, Elliott J, Okell L, et al. SARS-CoV-2 antibody prevalence in England following the first peak of the pandemic. Nat Commun. 2021;12(1):905.  https://doi.org/10.1038/s41467-021-21237-w  PMID: 33568663 
  91. Ward H, Cooke GS, Atchison C, Whitaker M, Elliott J, Moshe M, et al. Prevalence of antibody positivity to SARS-CoV-2 following the first peak of infection in England: Serial cross-sectional studies of 365,000 adults. Lancet Reg Health Eur. 2021;4:100098.  https://doi.org/10.1016/j.lanepe.2021.100098  PMID: 33969335 
  92. Ward H, Atchison C, Whitaker M, Donnelly CA, Riley S, Ashby D, et al. Increasing SARS-CoV-2 antibody prevalence in England at the start of the second wave: REACT-2 Round 4 cross-sectional study in 160,000 adults. medRxiv. 2021.07.21.21260926 https://doi.org/10.1101/2021.07.21.21260926 
  93. Iruzubieta P, Fernández-Lanas T, Rasines L, Cayon L, Álvarez-Cancelo A, Santos-Laso A, et al. Feasibility of large-scale population testing for SARS-CoV-2 detection by self-testing at home. Sci Rep. 2021;11(1):9819.  https://doi.org/10.1038/s41598-021-89236-x  PMID: 33972607 
  94. Haveri A, Ekström N, Solastie A, Virta C, Österlund P, Isosaari E, et al. Persistence of neutralizing antibodies a year after SARS-CoV-2 infection in humans. Eur J Immunol. 2021;51(12):3202-13.  https://doi.org/10.1002/eji.202149535  PMID: 34580856 
  95. Finnish Institute for Health and Welfare (THL). Study by THL and Welfare and the City of Helsinki. Antibodies elicited by coronavirus infection persist for at least four months. Helsinki: THL; 2020. Available from: https://thl.fi/en/web/thlfi-en/-/study-by-thl-and-welfare-and-the-city-of-helsinki-antibodies-elicited-by-coronavirus-infection-persist-for-at-least-four-months
  96. Finnish Institute for Health and Welfare (THL). THL’s study: Majority of people who have had a coronavirus infection retain antibodies for over six months. Helsinki: THL; 2020. Available from: https://thl.fi/en/web/thlfi-en/-/thl-s-study-majority-of-people-who-have-had-a-coronavirus-infection-retain-antibodies-for-over-six-months
  97. Mutevedzi PC, Kawonga M, Kwatra G, Moultrie A, Baillie V, Mabena N, et al. Estimated SARS-CoV-2 infection rate and fatality risk in Gauteng Province, South Africa: a population-based seroepidemiological survey. Int J Epidemiol. 2022;51(2):404-17.  https://doi.org/10.1093/ije/dyab217  PMID: 34718591 
  98. Cherif I, Kharroubi G, Chaabane S, Yazidi R, Dellagi M, Snoussi MA, et al. COVID-19 in Tunisia (North Africa): Seroprevalence of SARS-CoV-2 in the general population of the capital city Tunis. Diagnostics (Basel). 2022;12(4):971.  https://doi.org/10.3390/diagnostics12040971  PMID: 35454019 
  99. Royo-Cebrecos C, Vilanova D, López J, Arroyo V, Pons M, Francisco G, et al. Mass SARS-CoV-2 serological screening, a population-based study in the Principality of Andorra. Lancet Reg Health Eur. 2021;5:100119.  https://doi.org/10.1016/j.lanepe.2021.100119  PMID: 34557824 
  100. Fogh K, Strange JE, Scharff BFSS, Eriksen ARR, Hasselbalch RB, Bundgaard H, et al. Testing Denmark: a Danish nationwide surveillance study of COVID-19. Microbiol Spectr. 2021;9(3):e0133021.  https://doi.org/10.1128/Spectrum.01330-21  PMID: 34908473 
  101. Sood N, Pernet O, Lam CN, Klipp A, Kotha R, Kovacs A, et al. Seroprevalence of antibodies specific to receptor binding domain of SARS-CoV-2 and vaccination coverage among adults in Los Angeles County, April 2021: The LA pandemic surveillance cohort study. JAMA Netw Open. 2022;5(1):e2144258.  https://doi.org/10.1001/jamanetworkopen.2021.44258  PMID: 35050360 
  102. Matias WR, Fulcher IR, Sauer SM, Nolan CP, Guillaume Y, Zhu J, et al. Disparities in SARS-CoV-2 exposure: evidence from a citywide seroprevalence study in Holyoke, Massachusetts, USA. medRxiv; 2021.10.13.21264975 .  https://doi.org/10.1101/2021.10.13.21264975 
  103. Giuliano AR, Pilon-Thomas S, Schell MJ, Abrahamsen M, Islam JY, Isaacs-Soriano K, et al. SARS-CoV-2 period seroprevalence and related factors, Hillsborough County, Florida, USA, October 2020-March 2021. Emerg Infect Dis. 2022;28(3):556-63.  https://doi.org/10.3201/eid2803.211495  PMID: 35081021 
  104. Ministerio de Sanidad (MISAN). Estudio ENE-COVID: Informe final estudio nacional de sero-epidemiología de la infección por SARS-CoV-2 en España. [ENE-COVID study: Final report of the national sero-epidemiological study of SARS-CoV-2 infection in Spain]. Madrid: MISAN; 2020. Spanish. Available from: https://portalcne.isciii.es/enecovid19/informes/informe_final.pdf
  105. Ministerio de Sanidad (MISAN). Estudio ENE-COVID: cuarta ronda estudio nacional de sero-epidemiología de la infección por SARS-CoV-2 en España. [ENE-COVID study: fourth round national study of sero-epidemiology of SARS-CoV-2 infection in Spain]. Madrid: MISAN; 2020. Spanish. Available from: https://www.sanidad.gob.es/gabinetePrensa/notaPrensa/pdf/15.12151220163348113.pdf
  106. Blankenberger J, Kaufmann M, Albanese E, Amati R, Anker D, Camerini AL, et al. Is living in a household with children associated with SARS-CoV-2 seropositivity in adults? Results from the Swiss national seroprevalence study Corona Immunitas. BMC Med. 2022;20(1):233.  https://doi.org/10.1186/s12916-022-02431-z  PMID: 35725472 
  107. Dupraz J, Butty A, Duperrex O, Estoppey S, Faivre V, Thabard J, et al. Prevalence of SARS-CoV-2 in household members and other close contacts of COVID-19 cases: a serologic study in canton of Vaud, Switzerland. Open Forum Infect Dis. 2021;8(7):ofab149.  https://doi.org/10.1093/ofid/ofab149  PMID: 34307723 
  108. Canto E Castro L, Pereira AHG, Ribeiro R, Alves C, Veloso L, Vicente V, et al. Prevalence of SARS-CoV-2 antibodies after first 6 months of COVID-19 pandemic, Portugal. Emerg Infect Dis. 2021;27(11):2878-81.  https://doi.org/10.3201/eid2711.210636  PMID: 34437830 
  109. Reyes-Vega MF, Soto-Cabezas MG, Cárdenas F, Martel KS, Valle A, Valverde J, et al. SARS-CoV-2 prevalence associated to low socioeconomic status and overcrowding in an LMIC megacity: A population-based seroepidemiological survey in Lima, Peru. EClinicalMedicine. 2021;34:100801.  https://doi.org/10.1016/j.eclinm.2021.100801  PMID: 33817611 
  110. Isho B, Abe KT, Zuo M, Jamal AJ, Rathod B, Wang JH, et al. Persistence of serum and saliva antibody responses to SARS-CoV-2 spike antigens in COVID-19 patients. Sci Immunol. 2020;5(52):eabe5511.  https://doi.org/10.1126/sciimmunol.abe5511  PMID: 33033173 
  111. Hoballah A, El Haidari R, Siblany G, Abdel Sater F, Mansour S, Hassan H, et al. SARS-CoV-2 antibody seroprevalence in Lebanon: findings from the first nationwide serosurvey. BMC Infect Dis. 2022;22(1):42.  https://doi.org/10.1186/s12879-022-07031-z  PMID: 35012464 
  112. Silveira MF, Mesenburg M, Dellagostin OA, Oliveira NR, Maia MAC, Santos FDS, et al. Time-dependent decay of detectable antibodies against SARS-CoV-2: a comparison of ELISA with two batches of a lateral-flow test. Rochester, NY: Social Science Research Network; 2021. Report No.: ID 3757411.  https://doi.org/10.2139/ssrn.3757411  https://doi.org/10.2139/ssrn.3757411 
  113. Mahajan S, Srinivasan R, Redlich CA, Huston SK, Anastasio KM, Cashman L, et al. Seroprevalence of SARS-CoV-2-specific IgG antibodies among adults living in Connecticut: post-infection prevalence (PIP) study. Am J Med. 2021;134(4):526-534.e11.  https://doi.org/10.1016/j.amjmed.2020.09.024  PMID: 33130124 
  114. Sharma N, Sharma P, Basu S, Bakshi R, Gupta E, Agarwal R, et al. Second wave of the COVID-19 pandemic in Delhi, India: high seroprevalence not a deterrent? Cureus. 2021;13(10):e19000.  https://doi.org/10.7759/cureus.19000  PMID: 34853742 
  115. Sharma P, Basu S, Mishra S, Gupta E, Agarwal R, Kale P, et al. SARS-CoV-2 seroprevalence in Delhi, India, during - September-October 2021 – a population-based seroepidemiological study. Cureus. 2022;14(7):e27428.  https://doi.org/10.7759/cureus.27428  PMID: 36051724 
  116. Abdul-Raheem R, Moosa S, Waheed F, Aboobakuru M, Ahmed IN, Rafeeg FN, et al. A sero-epidemiological study after two waves of the COVID-19 epidemic. Asian Pac J Allergy Immunol. 2021."https://pubmed.ncbi.nlm.nih.gov/34953474" PMID: 34953474 
  117. Cito F, Amato L, Di Giuseppe A, Danzetta ML, Iannetti S, Petrini A, et al. A COVID-19 Hotspot Area: Activities and Epidemiological Findings. Microorganisms. 2020;8(11):1711.  https://doi.org/10.3390/microorganisms8111711  PMID: 33142840 
  118. Espenhain L, Tribler S, Sværke Jørgensen C, Holm Hansen C, Wolff Sönksen U, Ethelberg S. Prevalence of SARS-CoV-2 antibodies in Denmark: nationwide, population-based seroepidemiological study. Eur J Epidemiol. 2021;36(7):715-25.  https://doi.org/10.1007/s10654-021-00796-8  PMID: 34420152 
  119. Statens Serum Institut (SSI). Covid-19: Den Nationale Prævalensundersøgelse. Resultaterne fra 4. runde af antistofundersøgelse med 50.000 udtrukne borgere, uge 9-12, 2021. [Covid-19: The national prevalence survey. The results of the 4th round of antibody testing with 50,000 selected citizens, week 9-12, 2021]. Copenhagen: SSI; 2021. Danish. Available from: https://files.ssi.dk/praevalensundersoegelse_runde4
  120. Statens Serum Institut (SSI). Covid-19: Den Nationale Prævalensundersøgelse Resultaterne fra 5. runde af prævalensundersøgelsen med 75.000 udtrukne borgere, uge 19-23, 2021. [Covid-19: The national prevalence survey. The results of the 5th round of the prevalence survey with 75,000 selected citizens, week 19-23, 2021]. Copenhagen: SSI; 2021. Danish. Available from: https://files.ssi.dk/praevalensundersoegelse_runde5
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