key: cord-305763-160heazx
authors: Lai, Chih-Cheng; Wang, Jui-Hsiang; Hsueh, Po-Ren
title: Population-based seroprevalence surveys of anti-SARS-CoV-2 antibody: An up-to-date review
date: 2020-10-09
journal: Int J Infect Dis
DOI: 10.1016/j.ijid.2020.10.011
sha: 
doc_id: 305763
cord_uid: 160heazx

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), causing the 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 can be underestimated. Improved serological detection of specific antibodies against SARS-CoV-2 can help estimate the true number of infections. This article comprehensively reviewed the associated literature and provides updated information regarding the seroprevalence of the anti-SARS-CoV-2 antibody. The seroprevalence can vary according to different sites and the seroprevalence can increase with time in the longitudinal follow-up. Although healthcare workers (HCWs), especially those caring for COVID-19 patients, are considered as a high-risk group, the seroprevalence of a HCW wearing adequate personal protective equipment is thought to not be higher than other groups. With regard to sex, no statistical 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, continued seroprevalence surveillance is warranted to estimate and monitor the growing burden of COVID-19.

mild infections, and in places where qRT-PCR is unavailable. These issues can limit the understanding of the extent of SARS-CoV-2 infections and further affect the implementation of infection control and prevention policy. To solve this issue, the use of a serologic test to detect anti-SARS-CoV-2 antibody can be a better way to estimate the burden of SARS-CoV-2 infection than the PCR method, and help to understand the associated epidemiology (Lai et al., 2020c; Eckerle et al., 2020; Ko et al., 2020; . Therefore, we conducted this review to provide updated and comprehensive information about the seroprevalence of the SARS-CoV-2 antibody in different populations.

Several large population-based studies (Pollán et al., 2020; Stringhini et al., 2020; Fiore et al., 2020; Vena et al., 2020; Gallian et al., 2020; Bogogiannidou et al., 2020; Silveira et al., 2020; Amorim et al., 2020; Sood et al., 2020; Ng et al., 2020; Rosenberg et al., 2020; Havers et al., 2020; Nir et al., 2020; Sutton et al., 2020; McLaughlin et al., April 27, 2020 to May 11, 2020 households were initially selected from municipal rolls, using a two-stage random sampling stratified by province and municipality size. A total of 61,075 participants received the point-of-care test (Orient Gene Biotech COVID-19 IgG/IgM Rapid Test Cassette; Zhejiang Orient Gene Biotech, Zhejiang, China; reference GCCOV-402a), and among them, 51,958 further received a chemiluminescent microparticle immunoassay for the qualitative detection of IgG against SARS-CoV-2 nucleoprotein (SARS-CoV-2 IgG for use with ARCHITECT; Abbott Laboratories, Abbott Park, IL, USA; reference 06R8620). The seroprevalence was found to be 5.0% (95% CI, ) by the point-of-care test and 4.6% (95% CI, 4.3-5.0) by immunoassay, with a specificity-sensitivity range of 3.7% (95% CI, 3.3-4.0; both tests positive) to 6.2% (95% CI, 5.8-6.6; either test positive) (Pollán et al., 2020) . A study in Switzerland reported the preliminary results of the surveillance of 2,766 participants from 1,339 households, with a demographic distribution similar to that of the canton of Geneva between April 6 and May 9, 2020 (Stringhini et al., 2020) . In this study, 12 weekly seroprevalence surveys, using a commercially available enzyme-linked immunosorbent assay (ELISA) (Euroimmun;

Lübeck, Germany #EI 2606-9601 G) targeting the S1 domain of the spike protein of SARS-CoV-2 (sera diluted 1:101), were processed on a EuroLabWorkstation ELISA (Euroimmun) (SEROCoV-POP study). The results estimated the seroprevalence to be J o u r n a l P r e -p r o o f 7 4.8% (95% CI, 2.4-8.0; n = 341) in the first week, 8.5% (95% CI, n = 469) in the second week, 10.9% (95% CI, 7.9-14.4; n = 577) in the third week, 6.6% (95% CI, 4.3-9.4; n = 604) in the fourth week, and 10.8% (95% CI, 8.2-13.9; n = 775) in the fifth week (Stringhini et al., 2020) . In Denmark, a total of 20,640 blood donations were given by 17-69-year-old donors from April 6 to May 3, 2020, which were then subjected to a plasma or whole blood lateral flow test according to the manufacturer's recommendations (IgM/IgG Antibody to SARS-CoV-2 lateral flow test; Livzon Diagnostics Inc., Zhuhai, Guangdong, China) (Erikstrup et al et al., 2020) . The overall unadjusted seroprevalence was 2.0% (95% CI, 1.8-2.2), and after adjusting for assay sensitivity and specificity (including their CI), the overall seroprevalence was 1.9% (95% CI, 0.8-2.3) (Erikstrup et al et al., 2020) . In Italy, 390 blood donors in the Lodi Red Zone were recruited, from March 18 to April 6, 2020, for a study that utilized the SARS-CoV-2 microneutralization assay (Percivalle et al., 2020) . A total of 91 (23%) participants were positive for SARS-CoV-2 specific neutralizing antibodies (≥ 1:10),

while 299 (77%) tested negative (< 1:10). Contrastingly, the seroprevalence was only 0.99% (n = 9) among 904 healthy blood donors in the Apulia region, South-Eastern Italy (Fiore et al., 2020) . Recently, one large series including 3609 adult volunteer s from five administrative departments of the Liguria and Lombardia regions showed the seroprevalence was 11.0% (n = 389 ) (Vena et al., 2020) . In France, 998 samples J o u r n a l P r e -p r o o f collected from blood donors during the last week of March or the first week of April 2020 were tested for neutralizing antibodies against SARS-CoV-2, and the overall seroprevalence was found to be low (2.7%, n = 27) (Gallian et al., 2020) . By contrast, one more updated surveillance conducted between May 4 and June 23, 2020 in France showed the higher adjusted estimates of seroprevalence (positive anti-SARS-CoV-2 ELISA IgG result against the spike protein of SARS-CoV-2) were 10.0% (95% CI, 9.1-10.9) and 9.0% (95% CI, 7.7-10.2) in the Ile-de-France or Grand Est, respectivelytwo regions with high rates of COVID-19 and 3.1% (95% CI, 2.4-3.7) in the Nouvelle-Aquitainethe region with a low rate of COVID-19 (Carrat et al., 2020) . Moreover, they noted that confinement is associated with a higher seroprevalence, but a lower seroprevalence was observed in smokers compared to non-smokers (Carrat et al., 2020) .

During the early stage in Greece, the positive rate of anti-SARS-CoV-2 IgG was only 0.36% (24) among 6,586 serum samples, and the crude prevalence was 0.24% (5/2075) and 0.42% (19/4,511) in March and April, respectively (Bogogiannidou et al., 2020) .

In Brazil, three rounds of probability sample household surveys in the state of Rio Grande do Sul were carried out in nine large municipalities using the Wondfo lateral flow point-of-care test for IgM and IgG against SARS-CoV-2 (https://en.wondfo.com.cn/product/wondfo-sars-cov-2-antibody-test-lateral-flowmethod-2/). The seroprevalence was estimated to be 0.048% (2/4,151; 95% CI = 0.006-J o u r n a l P r e -p r o o f 9 0.174) on 11-13 April, 2020 (round 1), 0.135% (6/4,460; 95% CI = 0.049-0.293) on 25-27 April, 2020 (round 2), and 0.222% (10/4,500; 95% CI = 0.107-0.408) on 9-11

May, 2020 (round 3) (Silveira et al., 2020) . Furthermore, a significant upward trend was observed throughout the surveys (Silveira et al., 2020 (Sood et al., 2020) .

In San Francisco Bay Area, the seroprevalence was tested using the Architect SARS166

CoV-2 anti-nucleocapsid protein IgG and was found to be only 0.1% in 1,000 blood donors in March 2020 (Ng et al., 2020 J o u r n a l P r e -p r o o f 2020) (Havers et al., 2020) . In Indiana, the seroprevalence among 3,658 randomly selected noninstitutional participants was 1.01% (n = 38) between April 25 and 29, 2020 (Nir et al., 2020) . In Oregon, the overall seropositivity was 1.0% (n = 9) among 897 participants from 19 facilities participating in the Influenza-like Illness Surveillance

Network (Sutton et al., 2020) . In Blaine County, 208 out of 917 adult residents had positive anti-SARS-CoV-2 IgG and the overall seroprevalence was 22.7% between May 4 and 9 (McLaughlin et al., 2020). The highest seroprevalence was found to be 31.5% among 200 asymptomatic residents in Chelsea, Massachusetts (Naranbhai et al., 2020) .

In China, a serological survey was conducted in seven cities,

including Hubei Province (Wuhan, Honghu, and Jingzhou), Guangdong Province (Guangzhou and Foshan), Sichuan Province (Chengdu), and Chongqing between March 9, 2020 and April 10, 2020, and a validated serological test for the presence of antibodies (IgM or IgG) against SARS-CoV-2 was tested in a total of 17,368 individuals. For 10,499 individuals in the community setting, the seropositivity ranged from 0.6% among 9,442 community residents in Chengdu, Sichuan, and 1.4% among factory workers in Guangzhou, Guangdong, to 3.2% among 219 HCWs relatives, and 3.8% among 346 hotel staff members in Wuhan, Hubei . Moreover, seropositivity progressively decreased in other cities as the distance to the epicenter J o u r n a l P r e -p r o o f increased . In Pakistan, 24 (15.6%) of 154 asymptomatic young policemen had positive anti-SARS-CoV-2 IgG in high-risk areas of Lahore (Chughtai et al., 2020) and 21.4% to 37.7% of 380 healthy blood donor in Karachi (Younas et al., 2020) . In Malaysia, the seropositivity of anti-SARS-CoV-2 IgG was 0.6% (2/327) and 0.4% (1/261) based on the collected serum samples for non-respiratory-respiratory infections during the pandemic and post-pandemic period, respectively . In Seoul, Korea, the seroprevalence was only 0.07% based on the surveillance of 1500 residual sample from outpatients of two university hospital (Noh et al., 2020) .

In summary, the seroprevalence ranges from < 0.1% to more than 20% in the different regions and can increase with time (Table 1) . Regular monitoring of the seroprevalence in each site should be indicated to establish the epidemiology of COVID-19.

Nosocomial transmission of SARS-CoV-2 is common within hospitals and COVID-19 is a threat for HCWs, especially those without appropriate personal protective equipment (PPE) (Houlihan et al., 2020; Hunter et al., 2020; Kluytmans et al., 2020; Lai et al., 2020; Keeley et al., 2020; Wei et al., 2020) . One population-based study demonstrated that the positive rate of anti-SARS-CoV-2 IgG or IgM in the J o u r n a l P r e -p r o o f hospital settings was 2.5% (170/6919), which was higher than that reported in the community setting (0.8%, 81/10,449) . In this study , the positive rate was highest for HCWs in Wuhan, Hubei (3.8%, 27/714). Many studies had evaluated the seroprevalence among HCWs (Steensels et al., 2020; Martin et al., 2020; Korth et al., 2020; Stubblefield et al., 2020; Pallett et al., 2020; Grant et al., 2020; Hunter et al., 2020; Self et al., 2020; Moscola et al., 2020; Plebani et al., 2020 HCWs who regularly had direct contact with units housing adult COVID-19 patients in the month prior to undergoing testing with the validated enzyme-linked immunosorbent assay against the extracellular domain of the SARS-CoV-2 spike protein (Stubblefield et al., 2020) . Overall, 19 (7.6%) healthcare personnel tested positive for SARS-CoV-2 antibodies, and seropositivity was more common among those who were reported to generally not be wearing PPE for all encounters, versus those who were reported to be always wearing PPE (15.8% versus 4.3%) (P = 0.07) (Stubblefield et al., 2020) . In

China, 105 HCWs exposed to four laboratory-confirmed COVID-19 patients received testing with an enzyme immunoassay (EIA), as well as a microneutralization assay to assess the seroprevalence on day 14 th of quarantine, in which, 17.14% (n = 18) of HCWs were seropositive . A higher risk of seroconversion was found for .

Based on the above findings (Table 2) , HCWs are at high risk of acquiring SARS-CoV-2 infection, and adequate PPE could help protect them from the COVID-19 infection.

In the UK, a multicenter investigation showed that the seroprevalence was 10.6% and 44.7% among 405 asymptomatic and 1,299 symptomatic HCWs (Pallett et al., 2020) .

In another investigation in the UK, an overall seropositivity rate of 31.6% among HCW was found, which was highest among staff working in a clinical environment with direct patient contact (34.7%) and lowest among those working in nonclinical environments without patient contact (22.6%) (Grant et al., 2020) . In contrast, one study in the US showed that employees with heavy COVID-19 exposure had antibody prevalence similar to those with limited or no exposure and suggested that PPE use seems effective in the prevention of COVID-19 infection in healthcare workers (Hunter et al., 2020) .

Another study showed the similar findings that seroprevalence was lower among personnel who reported always wearing a face covering while caring for patients (6%), compared with those who did not (9%) (Self et al., 2020) . In the largest cohorts enrolling 40,329 HCWs at New York City, the overall seroprevalence was 13.7% (n = 5,523); however, only 9.0% (n = 3,077) among 34,251 without PCR testing were 

Several population-based studies (Pollán et al., 2020; 13 Stringhini et al., 2020; , Amorim et al., 2020; Sood et al., 2020; Rosenberg et al., 2020) have demonstrated differences in seroprevalence rates among male and female subjects. In New York, the weighted seroprevalence rate of males was 14.8% (95% CI, 13.8-15.8), which was numerically higher than that of females (13.3%; 95% CI, 12.4-14.2) ( Rosenberg et al., 2020) . In Switzerland, the rate of positive SARS-CoV-2 serology tests among males was 9.0% (118/1312), which was higher than that among females, at 6.9% (101/1454) (Erikstrup et al., 2020) . In Los Angeles, the unweighted portion of the population positive for IgM or IgG among males was 5.18% (95% CI, 3.10-8.07), which was numerically higher than that among females (3.31%; 95% CI, 1.94-5.24) (Sood et al., 2020) . In Brazil, males had a higher seroprevalence, after adjustment, than females (4.1% vs 3.5%, respectively), but the difference was not statistically significant (OR, (Pollán et al., 2020) . In the US, there was no clear association between seroprevalence by sex across sites (Havers et al., 2020) . Overall, these findings indicated that the seroprevalence between males and females is not significantly different.

Three population-based studies (Pollán et al., 2020; Stringhini et al., 2020; Havers et al., 2020; Sutton et al., 2020 ) demonstrated a lower seroprevalence among children.

Compared to subjects aged 20-49 years, children aged 5-9 years had a significantly lower seroprevalence of 0.8% (1/123) (relative risk, 0.32; 95% CI, 0.13-0.63) in a Swiss surveillance study (SEROCoV-POP) (Stringhini et al., 2020) . In Spain, the ENE-COVID study showed that the seroprevalence of subjects aged 0-19 years was 3.4%

using the point-of-care test, and 3.8% by immunoassay, which were lower than those reported for any other age group (4.4-6.0% using the point-of-care test, and 4.5-5.0% by immunoassay) (Pollán et al., 2020) . In the United States, the seroprevalence of subjects aged 0-18 years ranged from 0.7% (95% CI, 0-2.5) in Western Washington State to 5.8% (95% CI, 0-14.3) in Minneapolis-St Paul-St Cloud metro area (Minnesota) (Havers et al., 2020) . Moreover, the seroprevalence of this age group was numerically lower than that of other age groups in Western Washington State, New York, Louisiana, Missouri, and Connecticut (Havers et al., 2020) .

In addition, a cross-section study using the novel coronavirus (2019-nCoV)

IgG/IgM Test Kit (Colloidal gold; Genrui Biotech Inc, China) was conducted 8-10 weeks after a school outbreak, and the results showed antibody positivity rates of 9.9% (95% CI: 8.2-11.8) for 1,009 students (Table 2) . Moreover, the positivity was associated with a younger age (P = 0.01), lower grade (P = 0.05), prior RT-PCR positivity (P = 0.03), and history of contact with a confirmed case (P < 0.001) (Torres et al., 2020) . In another study (Dingens et al., 2020) , the seroprevalence in children who had visited Seattle Children's Hospital during the initial Seattle outbreak was determined using Abbott SARS-CoV-2 IgG chemiluminescent microparticle immunoassay, and only 8 children were found to be seropositive, with a seroprevalence of 0.7% (Table 2) . Overall, children seem to have a lower seroprevalence than adults, which was consistent with previous epidemiological findings of laboratory-confirmed COVID-19 cases Wang et al., 2020; Huang et al., 2020; .

Pregnant women can be infected by SARS-Co-2, although data in this population are limited (Ashraf et al., 2020; Barbero et al., 2020; Sahin et al., 2020; J o u r n a l P r e -p r o o f 2020; Schmid et al., 2020; Yu et al., 2020) . Recently, 1,293 parturient women were tested using an ELISA for SARS-CoV-2 IgG and IgM antibodies to the spike receptorbinding domain antigen at two centers in Philadelphia from April 4 to June 3, 2020.

The results demonstrated that 80/1,293 (6.2%) of parturient women possessed IgG and/or IgM SARS-CoV-2-specific antibodies ( (Gallian et al., 2020) .

Patients undergoing hemodialysis are also at risk for COVID-19 transmission due to the need for frequent hospital stays, and therefore, the difficulty in maintaining physical distancing (Yau et al., 2020; Tang et al., 2020; Arslan et al., 2020) . The J o u r n a l P r e -p r o o f seroprevalence of hemodialysis patients ranged from 2.8% (16/563) to 3.6% (35/979) in a study in China (31). Another study showed the overall SARS-CoV-2 seroprevalence was 36.2% (129/356) in hemodialysis patients, and 40.3% (n =52) of them were asymptomatic or with negative PCR results (Clarke et al., 2020) .

In this review, we found no significant association between the incidence of COVID-19 cases and their associated seroprevalence (Table 1) . Even in the same country, the seroprevalence ranged from 0.1% to 12.5%, and 0.05% to 4.0% in the US and Brazil (20, (22) (23) (24) 26) , respectively. These findings may be due to the fact that anti-SARS-CoV-2 antibody seroprevalence varies according to the different study countries/regions, study populations, timing during the period of the COVID-19 pandemic, and methods used for serology tests. Therefore, the seroprevalence reported in this article can only reflect the situation of the time and place in which the surveillance investigation was performed by the specific test methods. In fact, the number of COVID-19 cases is still rapidly growing, and given the time-sensitivity, a true estimation of the epidemiology of SARS infection remains a great challenge.

Therefore, such seroprevalence surveillance should be continued and is necessary to 

The seroprevalence can vary across different regions and can increase with time in the longitudinal follow-up. Although HCWs, especially those caring for COVID-19

patients, are considered a high-risk group, their seroprevalence would not be higher than that observed in other groups if they wear adequate PPE. Regarding sex, no statistical difference was found between male and female subjects. Some studies have

shown that children have a lower risk than other age groups, while others did not.

Finally, the seroprevalence can vary according to different populations, such as in pregnant women and patients undergoing hemodialysis; however, relevant studies are limited. Therefore, further continued seroprevalence surveillance is warranted to estimate and monitor the growing burden of COVID-19.

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

No funding was required.

J o u r n a l P r e -p r o o f

No ethical approval sought.

We declare no conflict of interest.

J o u r n a l P r e -p r o o f 

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