Population-based seroprevalence surveys of anti-SARS-CoV-2 antibody: An up-to-date review

Chih-Cheng Lai, Jui-Hsiang Wang, Po-Ren Hsueh, Chih-Cheng Lai, Jui-Hsiang Wang, Po-Ren Hsueh

Abstract

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the causative agent of coronavirus disease 2019 (COVID-19), has led to a global pandemic. However, the majority of currently available data are restricted to laboratory-confirmed cases for symptomatic patients, and the SARS-CoV-2 infection can manifest as an asymptomatic or mild disease. Therefore, the true extent of the burden of COVID-19 may be underestimated. Improved serological detection of specific antibodies against SARS-CoV-2 could help estimate the true numbers of infections. This article comprehensively reviews the associated literature and provides updated information regarding the seroprevalence of the anti-SARS-CoV-2 antibody. The seroprevalence can vary across different sites and the seroprevalence can increase with time during longitudinal follow-up. Although healthcare workers (HCWs), especially those caring for COVID-19 patients, are considered as a high-risk group, the seroprevalence in HCWs wearing adequate personal protective equipment is thought to be no higher than that in other groups. With regard to sex, no statistically significant difference has been found between male and female subjects. Some, but not all, studies have shown that children have a lower risk than other age groups. Finally, seroprevalence can vary according to different populations, such as pregnant women and hemodialysis patients; however, limited studies have examined these associations. Furthermore, the continued surveillance of seroprevalence is warranted to estimate and monitor the growing burden of COVID-19.

Keywords: Antibody; COVID-19; Population-based survey; SARS-CoV-2; Seroprevalence.

Copyright © 2020 The Authors. Published by Elsevier Ltd.. All rights reserved.

References

    1. Amorim Filho L., Szwarcwald C.L., Mateos S.O.G., Leon A., Medronho R.A., Veloso V.G. Seroprevalence of anti-SARS-CoV-2 among blood donors in Rio de Janeiro, Brazil. Rev Saude Publica. 2020;54:69.
    1. Arslan H., Musabak U., Ayvazoglu Soy E.H., Kurt Azap O., Sayin B., Akcay S. Incidence and immunologic analysis of coronavirus disease (COVID-19) in hemodialysis patients: a single-center experience. Exp Clin Transplant. 2020;18(3):275–283.
    1. Ashraf M.A., Keshavarz P., Hosseinpour P., Erfani A., Roshanshad A., Pourdast A. Coronavirus disease 2019 (COVID-19): a systematic review of pregnancy and the possibility of vertical transmission. J Reprod Infertil. 2020;21(3):157–168.
    1. Barbero P., Mugüerza L., Herraiz I., García Burguillo A., San Juan R., Forcén L. SARS-CoV-2 in pregnancy: characteristics and outcomes of hospitalized and non-hospitalized women due to COVID-19. J Matern Fetal Neonatal Med. 2020;(July):1–7. doi: 10.1080/14767058.2020.1793320.
    1. Bogogiannidou Z., Vontas A., Dadouli K., Kyritsi M.A., Soteriades S., Nikoulis D.J. Repeated leftover serosurvey of SARS-CoV-2 IgG antibodies, Greece, March and April 2020. Euro Surveill. 2020;25(31)
    1. Carrat F., de Lamballerie X., Rahib D., Blanche H., Lapidus N., Artaud F. Seroprevalence of SARS-CoV-2 among adults in three regions of France following the lockdown and associated risk factors: a multicohort study. medRxiv. 2020 doi: 10.1101/2020.09.16.20195693. 09.16.20195693.
    1. Chen Y., Tong X., Wang J., Huang W., Yin S., Huang R. High SARS-CoV-2 antibody prevalence among healthcare workers exposed to COVID-19 patients. J Infect. 2020;81(3):420–426.
    1. Chen H., Guo J., Wang C., Luo F., Yu X., Zhang W. Clinical characteristics and intrauterine vertical transmission potential of COVID-19 infection in nine pregnant women: a retrospective review of medical records. Lancet. 2020;395(10226):809–815.
    1. Chughtai O.R., Batool H., Khan M.D., Chughtai A.S. Frequency of COVID-19 IgG antibodies among Special Police Squad Lahore, Pakistan. J Coll Physicians Surg Pak. 2020;30:735–739.
    1. Clarke C., Prendecki M., Dhutia A., Ali M.A., Sajjad H., Shivakumar O. High prevalence of asymptomatic COVID-19 infection in hemodialysis patients detected using serologic screening. J Am Soc Nephrol. 2020;(July) doi: 10.1681/ASN.2020060827. ASN.2020060827.
    1. Crovetto F., Crispi F., Llurba E., Figueras F., Gómez-Roig M.D., Gratacós E. Seroprevalence and presentation of SARS-CoV-2 in pregnancy. Lancet. 2020;(August) doi: 10.1016/S0140-6736(20)31714-1. S0140-6736(20)31714-1.
    1. Dingens A.S., Crawford K.H., Adler A., Steele S.L., Lacombe K., Eguia R. Seroprevalence of SARS-CoV-2 among children visiting a hospital during the initial Seattle outbreak. medRxiv. 2020;(May) doi: 10.1101/2020.05.26.20114124. 2020.05.26.20114124.
    1. Eckerle I., Meyer B. SARS-CoV-2 seroprevalence in COVID-19 hotspots. Lancet. 2020;396(10250):514–515.
    1. Erikstrup C., Hother C.E., Pedersen O.B.V., Mølbak K., Skov R.L., Holm D.K. Estimation of SARS-CoV-2 infection fatality rate by real-time antibody screening of blood donors. Clin Infect Dis. 2020;(June) doi: 10.1093/cid/ciaa849. ciaa849.
    1. Fiore J.R., Centra M., De Carlo A., Granato T., Rosa A., Sarno M. Results from a survey in healthy blood donors in South Eastern Italy indicate that we are far away from herd immunity to SARS-CoV-2. J Med Virol. 2020;(August) doi: 10.1002/jmv.26425. 10.1002/jmv.26425.
    1. Flannery D.D., Gouma S., Dhudasia M.B., Mukhopadhyay S., Pfeifer M.R., Woodford E.C. SARS-CoV-2 seroprevalence among parturient women. Sci Immuonl. 2020;5(49) doi: 10.1126/sciimmunol.abd5709. eabd5709.
    1. Freeman B., Lester S., Mills L., Rasheed M.A.U., Moye S., Abiona O. Validation of a SARS-CoV-2 spike protein ELISA for use in contact investigations and serosurveillance. bioRxiv. 2020;(April) doi: 10.1101/2020.04.24.057323. 2020.04.24.057323.
    1. Gallian P., Pastorino B., Morel P., Chiaroni J., Ninove L., de Lamballerie X. Lower prevalence of antibodies neutralizing SARS-CoV-2 in group O French blood donors. Antiviral Res. 2020;181:104880. doi: 10.1016/j.antiviral.2020.104880.
    1. Grant J.J., Wilmore S.M.S., McCann N.S., Donnelly O., Lai R.W.L., Kinsella M.J. Seroprevalence of SARS-CoV-2 antibodies in healthcare workers at a London NHS Trust. Infect Control Hosp Epidemiol. 2020;(August):1–3. doi: 10.1017/ice.2020.402.
    1. Havers F.P., Reed C., Lim T., Montgomery J.M., Klena J.D., Hall A.J. Seroprevalence of antibodies to SARS-CoV-2 in 10 sites in the United States, March 23–May 12, 2020. JAMA Intern Med. 2020;(July) doi: 10.1001/jamainternmed.2020.4130.
    1. Houlihan C.F., Vora N., Byrne T., Lewer D., Kelly G., Heaney J. Pandemic peak SARS-CoV-2 infection and seroconversion rates in London frontline health-care workers. Lancet. 2020;396(10246):e6–e7.
    1. Huang C., Wang Y., Li X., Ren L., Zhao J., Hu Y. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395(10223):497–506.
    1. Hunter E., Price D.A., Murphy E., van der Loeff I.S., Baker K.F., Lendrem D. First experience of COVID-19 screening of health-care workers in England. Lancet. 2020;395(10234):e77–e78.
    1. Hunter B.R., Dbeibo L., Weaver C., Beeler C., Saysana M., Zimmerman M. Seroprevalence of SARS-CoV-2 antibodies among healthcare workers with differing levels of COVID-19 patient exposure. Infect Control Hosp Epidemiol. 2020;(August):1–7. doi: 10.1017/ice.2020.390.
    1. Keeley A.J., Evans C., Colton H., Ankcorn M., Cope A., State A. Roll-out of SARS-CoV-2 testing for healthcare workers at a large NHS Foundation Trust in the United Kingdom, March 2020. Euro Surveill. 2020;25(14):2000433.
    1. Kluytmans-van den Bergh M.F.Q., Buiting A.G.M., Pas S.D., Bentvelsen R.G., van den Bijllaardt W., van Oudheusden A.J.G. Prevalence and clinical presentation of health care workers with symptoms of Coronavirus Disease 2019 in 2 Dutch hospitals during an early phase of the pandemic. JAMA Netw Open. 2020;3(5)
    1. Ko J.H., Joo E.J., Kim S.H., Kim Y.J., Huh K., Cho S.Y. Clinical application of rapid diagnostic test kit for SARS-CoV-2 antibodies into the field of patient care. J Microbiol Immunol Infect. 2020;(July) doi: 10.1016/j.jmii.2020.07.003. S1684-1182(20)30160-30162.
    1. Korth J., Wilde B., Dolff S., Anastasiou O.E., Krawczyk A., Jahn M. 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.2020.104437.
    1. Lai C.C., Shih T.P., Ko W.C., Tang H.J., Hsueh P.R. Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and coronavirus disease-2019 (COVID-19): the epidemic and the challenges. Int J Antimicrob Agents. 2020;55(3):105924.
    1. Lai C.C., Wang C.Y., Wang Y.H., Hsueh S.C., Ko W.C., Hsueh P.R. Global epidemiology of coronavirus disease 2019 (COVID-19): disease incidence, daily cumulative index, mortality, and their association with country healthcare resources and economic status. Int J Antimicrob Agents. 2020;55(4):105946.
    1. Lai C.C., Wang C.Y., Ko W.C., Hsueh P.R. In vitro diagnostics of coronavirus disease 2019: technologies and application. J Microbiol Immunol Infect. 2020;(June) doi: 10.1016/j.jmii.2020.05.016. S1684-1182(20)30140-30147.
    1. Lai C.C., Ko W.C., Lee P.I., Jean S.S., Hsueh P.R. Extra-respiratory manifestations of COVID-19. Int J Antimicrob Agents. 2020;56(2)
    1. Lai C.C., Liu Y.H., Wang C.Y., Wang Y.H., Hsueh S.C., Yen M.Y. Asymptomatic carrier state, acute respiratory disease, and pneumonia due to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2): facts and myths. J Microbiol Immunol Infect. 2020;53:404–412.
    1. Lai X., Wang M., Qin C., Tan L., Ran L., Chen D. Coronavirus disease 2019 (COVID-2019) infection among health care workers and implications for prevention measures in a tertiary hospital in Wuhan, China. JAMA Netw Open. 2020;3(5)
    1. Lee E., Mohd Esa N.Y., Wee T.M., Soo C.I. Bonuses and pitfalls of a paperless drive-through screening and COVID-19: a field report. J Microbiol Immunol Infect. 2020;(May) doi: 10.1016/j.jmii.2020.05.011. S1684-1182(20)30125-0.
    1. Lee P.I., Hu Y.L., Chen P.Y., Huang Y.C., Hsueh P.R. Are children less susceptible to COVID-19? J Microbiol Immunol Infect. 2020;53(3):371–372.
    1. Li C.W., Syue L.S., Tsai Y.S., Li M.C., Lo C.L., Tsai C.S. Anosmia and olfactory tract neuropathy in a case of COVID-19. J Microbiol Immunol Infect. 2020;(June) doi: 10.1016/j.jmii.2020.05.017. S1684-1182(20)30144-4.
    1. Li Q., Guan X., Wu P., Wang X., Zhou L., Tong Y. Early transmission dynamics in Wuhan, China, of novel coronavirus-infected pneumonia. N Engl J Med. 2020;382(13):1199–1207.
    1. Liu A., Li Y., Peng J., Huang Y., Xu D. Antibody responses against SARS-CoV-2 in COVID-19 patients. J Med Virol. 2020;(June) doi: 10.1002/jmv.26241. 10.1002/jmv.26241.
    1. Martin C., Montesinos I., Dauby N., Gilles C., Dahma H., Van Den Wijngaert S. Dynamic of SARS-CoV-2 RT-PCR positivity and seroprevalence among high-risk health care workers and hospital staff. J Hosp Infect. 2020;106(1):102–106.
    1. McLaughlin C.C., Doll M.K., Morrison K.T., McLaughlin W.L., O’Connor T., Sholukh A.M. High community SARS-CoV-2 antibody seroprevalence in a Ski Resort Community, Blaine County, Idaho, US. Preliminary Results. medRxiv. 2020;(July) doi: 10.1101/2020.07.19.20157198. 2020.07.19.20157198.
    1. Moscola J., Sembajwe G., Jarrett M., Farber B., Chang T., McGinn T. Northwell health COVID-19 research consortium. Prevalence of SARS-CoV-2 antibodies in health care personnel in the New York City area. JAMA. 2020;6(August) doi: 10.1001/jama.2020.14765.
    1. Naranbhai V., Chang C.C., Beltran W.F.G., Miller T.E., Astudillo M.G., Villalba J.A. High seroprevalence of anti-SARS-CoV-2 antibodies in Chelsea, Massachusetts. J Infect Dis. 2020;(September) doi: 10.1093/infdis/jiaa579. jiaa579.
    1. Ng D., Goldgof G., Shy B., Levine A., Balcerek J., Bapat S.P. SARS-CoV-2 seroprevalence and neutralizing activity in donor and patient blood from the San Francisco Bay Area. medRxiv. 2020;(May) doi: 10.1101/2020.05.19.20107482. 2020.05.19.20107482.
    1. Nir Menachemi, Constantin T. Yiannoutsos, Brian E. Dixon, Thomas J. Duszynski, William F. Fadel, Kara K. Wools-Kaloustian. Population point prevalence of SARS-CoV-2 infection based on a statewide random sample-Indiana, April 25–29, 2020. MMWR Morb Mortal Wkly Rep. 2020;69(29):960–964.
    1. Noh J.Y., Seo Y.B., Yoon J.G., Seong H., Hyun H., Lee J. Seroprevalence of anti-SARS-CoV-2 antibodies among outpatients in southwestern Seoul, Korea. J Korean Med Sci. 2020;35:e311. doi: 10.3346/jkms.2020.35.e311.
    1. Pallett S.J.C., Rayment M., Patel A., Fitzgerald-Smith S.A.M., Denny S.J., Charani E. 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;(July) doi: 10.1016/S2213-2600(20)30315-5. S2213-2600(20)30315-5.
    1. Percivalle E., Cambiè G., Cassaniti I., Nepita E.V., Maserati R., Ferrari A. Prevalence of SARS-CoV-2 specific neutralising antibodies in blood donors from the Lodi Red Zone in Lombardy, Italy, as at 06 April 2020. Euro Surveill. 2020;25(24):2001031. doi: 10.2807/1560-7917.ES.2020.25.24.2001031.
    1. Plebani M., Padoan A., Fedeli U., Schievano E., Vecchiato E., Lippi G. SARS-CoV-2 serosurvey in health care workers of the Veneto Region. Clin Chem Lab Med. 2020;(August) doi: 10.1515/cclm-2020-1236. /j/cclm.ahead-of-print/cclm-2020-1236/cclm-2020-1236.xml.
    1. Pollán M., Pérez-Gómez B., Pastor-Barriuso R., Oteo J., Hernán M.A., Pérez-Olmeda M. Prevalence of SARS-CoV-2 in Spain (ENE-COVID): a nationwide, population-based seroepidemiological study. Lancet. 2020;396(10250):535–544.
    1. Rosenberg E.S., Tesoriero J.M., Rosenthal E.M., Chung R., Barranco M.A., Styer L.M. Cumulative incidence and diagnosis of SARS-CoV-2 infection in New York. Ann Epidemiol. 2020;48:23–29. doi: 10.1016/j.annepidem.2020.06.004.
    1. Sahin D., Tanacan A., Erol S.A., Anuk A.T., Eyi E.G.Y., Ozgu-Erdinc A.S. A pandemic center’s experience of managing pregnant women with COVID-19 infection in Turkey: a prospective cohort study. Int J Gynaecol Obstet. 2020;(July) doi: 10.1002/ijgo.13318.
    1. Sam I.C., Chong Y.M., Tan C.W., Chan Y.F. Low post-pandemic wave SARS-CoV-2 seroprevalence in Kuala Lumpur and Selangor, Malaysia. J Med Virol. 2020;(August) doi: 10.1002/jmv.26426. 10.1002/jmv.26426.
    1. Schmid M.B., Fontijn J., Ochsenbein-Kölble N., Berger C., Bassler D. COVID-19 in pregnant women. Lancet Infect Dis. 2020;20(6):653.
    1. Self W.H., Tenforde M.W., Stubblefield W.B., Feldstein L.R., Steingrub J.S., Shapiro N.I. Seroprevalence of SARS-CoV-2 among frontline health care personnel in a multistate hospital network -13 academic medical centers, April–June 2020. MMWR Morb Mortal Wkly Rep. 2020;69(September (35)):1221–1226. doi: 10.15585/mmwr.mm6935e2.
    1. Sheng W.H., Ko W.C., Huang Y.C., Hsueh P.R. SARS-CoV-2 and COVID-19. J Microbiol Immunol Infect. 2020;53(3):363–364.
    1. Silveira M.F., Barros A.J.D., Horta B.L., Pellanda L.C., Victora G.D., Dellagostin O.A. Population-based surveys of antibodies against SARS-CoV-2 in Southern Brazil. Nat Med. 2020;26(8):1196–1199.
    1. Sood N., Simon P., Ebner P., Eichner D., Reynolds J., Bendavid E. Seroprevalence of SARS-CoV-2-specific antibodies among adults in Los Angeles County, California, on April 10–11, 2020. JAMA. 2020;323(23):2425–2427.
    1. Steensels D., Oris E., Coninx L., Nuyens D., Delforge M.L., Vermeersch P. Hospital-wide SARS-CoV-2 antibody screening in 3056 staff in a tertiary center in Belgium. JAMA. 2020;324(2):195–197.
    1. Stringhini S., Wisniak A., Piumatti G., Azman A.S., Lauer S.A., Baysson H. Seroprevalence of anti-SARS-CoV-2 IgG antibodies in Geneva, Switzerland (SEROCoV-POP): a population-based study. Lancet. 2020;396(10247):313–319.
    1. Stubblefield W.B., Talbot H.K., Feldstein L., Tenforde M.W., Rasheed M.A.U., Mills L. Seroprevalence of SARS-CoV-2 among frontline healthcare personnel during the first month of caring for COVID-19 patients-Nashville, Tennessee. Clin Infect Dis. 2020;(July) doi: 10.1093/cid/ciaa936. ciaa936.
    1. Sutton M., Cieslak P., Linder M. Notes from the field: Seroprevalence estimates of SARS-CoV-2 infection in convenience sample-Oregon, May 11–June 15, 2020. MMWR Morb Mortal Wkly Rep. 2020;69(32):1100–1101.
    1. Tang H., Tian J.B., Dong J.W., Tang X.T., Yan Z.Y., Zhao Y.Y. Serologic detection of SARS-CoV-2 infections in hemodialysis centers: a multicenter retrospective study in Wuhan, China. Am J Kidney Dis. 2020;(July) doi: 10.1053/j.ajkd.2020.06.008. S0272-6386(20)30786-1.
    1. Torres J.P., Piñera C., De La Maza V., Lagomarcino A.J., Simian D., Torres B. SARS-CoV-2 antibody prevalence in blood in a large school community subject to a Covid-19 outbreak: a cross-sectional study. Clin Infect Dis. 2020;(July) doi: 10.1093/cid/ciaa955. ciaa955.
    1. Vena A., Berruti M., Adessi A., Blumetti P., Brignole M., Colognato R. Prevalence of antibodies to SARS-CoV-2 in Italian adults and associated risk factors. J Clin Med. 2020;9:E2780. doi: 10.3390/jcm9092780.
    1. Wang D., Hu B., Hu C., Zhu F., Liu X., Zhang J. Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China. JAMA. 2020;323(11):1061–1069.
    1. Wei X.S., Wang X.R., Zhang J.C., Yang W.B., Ma W.L., Yang B.H. A cluster of health care workers with COVID-19 pneumonia caused by SARS-CoV-2. J Microbiol Immunol Infect. 2020;(April) doi: 10.1016/j.jmii.2020.04.013. S1684-1182(20)30107-30109.
    1. World Health Organization (WHO). . [Accessed 7 September 2020].
    1. Wu Y., Feng Z., Li P., Yu Q. Relationship between ABO blood group distribution and clinical characteristics in patients with COVID-19. Clin Chim Acta. 2020;509:220–223. doi: 10.1016/j.cca.2020.06.026.
    1. Xu X., Sun J., Nie S., Li H., Kong Y., Liang M. Seroprevalence of immunoglobulin M and G antibodies against SARS-CoV-2 in China. Nat Med. 2020;26:1193–1195.
    1. Yau K., Muller M.P., Lin M., Siddiqui N., Neskovic S., Shokar G. COVID-19 outbreak in an Urban hemodialysis unit. Am J Kidney Dis. 2020;(July) doi: 10.1053/j.ajkd.2020.07.001. S0272-6386(20)30811-30818.
    1. Younas A., Waheed S., Khawaja S., Imam M., Borhany M., Shamsi T. Seroprevalence of SARS-CoV-2 antibodies among healthy blood donors in Karachi, Pakistan. Transfus Apher Sci. 2020;(August):102923. doi: 10.1016/j.transci.2020.102923.
    1. Yu N., Li W., Kang Q., Xiong Z., Wang S., Lin X. Clinical features and obstetric and neonatal outcomes of pregnant patients with COVID-19 in Wuhan, China: a retrospective, single-centre, descriptive study. Lancet Infect Dis. 2020;20(5):559–564.

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