Next Article in Journal
Durability of Immune Response to ChAdOx1-nCoV-19 Vaccine in Solid Cancer Patients Undergoing Anticancer Treatment
Previous Article in Journal
Determinants of COVID-19 Vaccination Intention among Health Care Workers in France: A Qualitative Study
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Estimated Infection and Vaccine Induced SARS-CoV-2 Seroprevalence in Israel among Adults, January 2020–July 2021

1
Israel Center for Disease Control, Ministry of Health, Gertner Institute, Chaim Sheba Medical Center, Tel-Hashomer 52621, Israel
2
Department of Epidemiology and Preventive Medicine, Sackler Faculty of Medicine, Tel-Aviv University, Tel-Aviv 69978, Israel
3
School of Public Health, University of Haifa, Haifa 3498838, Israel
4
Central Virology Laboratory, Public Health Services, Ministry of Health, Chaim Sheba Medical Center, Tel Hashomer 52621, Israel
*
Author to whom correspondence should be addressed.
Vaccines 2022, 10(10), 1663; https://doi.org/10.3390/vaccines10101663
Submission received: 19 September 2022 / Revised: 2 October 2022 / Accepted: 3 October 2022 / Published: 5 October 2022
(This article belongs to the Section COVID-19 Vaccines and Vaccination)

Abstract

:
Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) emerged in Israel in February 2020 and spread from then. In December 2020, the FDA approved an emergency use authorization of the Pfizer-BioNTech vaccine, and on 20 December, an immunization campaign began among adults in Israel. We characterized seropositivity for IgG anti-spike antibodies against SARS-CoV-2 between January 2020 and July 2021, before and after the introduction of the vaccine in Israel among adults. We tested 9520 serum samples, collected between January 2020 and July 2021. Between January and August 2020, seropositivity rates were lower than 5.0%; this rate increased from September 2020 (6.3%) to April 2021 (84.9%) and reached 79.1% in July 2021. Between January and December 2020, low socio-economic rank was an independent, significant correlate for seropositivity. Between January and July 2021, the 40.00–64.99-year-old age group, Jews and others, and residents of the Northern district were significantly more likely to be seropositive. Our findings indicate a slow, non-significant increase in the seropositivity rate to SARS-CoV-2 between January and December 2020. Following the introduction of the Pfizer-BioNTech vaccine in Israel, a significant increase in seropositivity was observed from January until April 2021, with stable rates thereafter, up to July 2021.

1. Introduction

Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) was first diagnosed in December 2019 in Wuhan, China, and from January 2020 the virus spread to other provinces in China [1]. From February 2020, SARS-CoV-2 spread worldwide, and on 21 February, Israel confirmed the first case of COVID-19. Since then, the virus has spread throughout the country [1].
Non-pharmaceutical preventive measures were applied in Israel to control the spread of the virus, including social distancing, education institute closures, face masks, and limitations on traveling in and out of the country. These measures demonstrated high effectiveness in reducing morbidity [2], though a long-term solution was required.
On December 11, 2020, Pfizer received an Emergency Use Authorization (EUA) for the BNT162b2 mRNA vaccine (Pfizer-BioNTech), and the immunization campaign began in Israel on 20 December. Of 6,480,700 citizens aged 16 years and older in Israel [3], by 31 July 2021, 5,616,678 (86.7%) were administered with the first dose, 5,253,773 (81.1%) with the second dose, and 15,272 (0.2%) with the third dose (booster) [4].
Since December 2020, several variants have emerged and have been classified as variants of concern (VOCs) by the World Health Organization (WHO): Alpha (B.1.1.7, first observed in the United Kingdom, Date of Designation (DoD): December 2020); Beta (B.1.351, first observed in South Africa, DoD: December 2020); Gamma (P.1, first observed in Brazil, DoD: January 2021), and Delta (B.1.617.2, first observed in India, DoD: May 2021) [5]. These variants contain various mutations on the spike protein, are highly transmissible, and demonstrated a degree of escape from protective antibody induced by natural infection or, to a lesser degree, after immunization [6].
Sero-surveys conducted around the world and in Israel mostly examined the seroprevalence against SARS-CoV-2 only over a short period. Information on the dynamics of SARS-CoV-2 seropositivity is required to provide insights on the population exposure to the virus in the pre-vaccination era, and the effect of the immunization on the population.
The objectives of the study were to estimate the seropositivity rate to anti-SARS-CoV-2 antibodies due to infection between January and December 2020 and due to infection and vaccination between January and July 2021 in Israel, and to identify associated risk factors for seropositivity in these periods.

2. Materials and Methods

Sampling: Residual sera samples of adults aged 16 years and older were obtained from the Israel National Sera Bank (INSB) established in 1997 in the Israel Center for Disease Control. The samples were collected from individuals who performed routine or diagnostic blood tests between January 2020 and July 2021 in the following laboratories: the Soroka laboratory of the Clalit Health Maintenance Organization (HMO) (non-hospitalized patients) in the south of Israel, the Haifa and Western Galilee laboratory of the Clalit HMO in northern Israel, the Jerusalem Clalit HMO in Central Israel, the Mayanei Hayeshua Medical Center in Bnei-Brak, and the National Blood Service (NBS) of the Medical Emergency Services in Israel (Magen David Adom) in central Israel. The samples were collected throughout the period, aliquoted and stored at a temperature of −80 °C. For each sample, the retrieved data were age, gender, district of residence (North, Haifa, Central, Tel Aviv, Jerusalem, South, and Judea and Samaria), birth country (Israel vs. other), population group (Jews and others, and Arabs), and socio-economic rank. The data on socio-economic rank were based on city of residence, and an index published by the Central Bureau of Statistics that ranks the authorities in Israel based on a wide range of variables and ranges between 1 (the lowest) and 10 (the highest) [7]. Other than these details, the samples are anonymized. Further details regarding the sera collection and the INSB representativeness were described previously [8].
Ethics: Sera sample collection is approved by the legal department of the Israeli Ministry of Health.
Laboratory methods: The samples were tested for SARS-CoV-2-specific IgG antibodies using an in-house Enzyme-Linked Immunosorbent Assay (ELISA) based on the Receptor-Binding Domain (RBD) of the Spike protein [9]. Using a sample cut-off of 1.1, a lower value was defined as negative, and equal or higher value was defined as positive. The test sensitivity and specificity were 88% and 98%, respectively [9]. The samples were tested in the Central Virology Laboratory of the Ministry of Health, located in Sheba Medical Center.
Data analysis: Seropositivity rates were calculated by dividing the number of positive samples to SARS-CoV-2 IgG antibodies by the number of tested samples, and 95% confidence intervals (CI) were calculated. Across the study period, we defined two periods according to the vaccine introduction in Israel. The first period was between January and December 2020, before the vaccine was available, and the second period was between January and July 2021, after the introduction of the vaccine. For each period, seropositivity rates were calculated according to demographic characteristics, and univariable and multivariable analyses were applied, to further evaluate the association between demographic characteristics and seropositivity. Unadjusted and adjusted odds ratio (OR) and 95% confidence intervals (CI) were calculated, accordingly.
Statistical significance was determined at a level of p-value < 0.05. The statistical analyses were performed using the SAS Enterprise Guide software (version 7.12, SAS Institute Inc., Cary, NC, USA). Trends in seropositivity rates were expressed using the monthly percent change (MPC) calculated by Joinpoint software (Joinpoint Regression Program, Version 4.9.0.0, March 2021; Statistical Research and Applications Branch, National Cancer Institute. Calverton, MD, USA).

3. Results

Between January 2020 and July 2021, 9520 sera bank samples of Israeli 16+ year olds were collected. Table 1 shows the demographic characteristics of the total study population by period.
Figure 1 demonstrates seropositivity rates between January 2020 and July 2021 by month.
Between January and August 2020, the seropositivity rate was lower than 5.0%, and increased from September (6.3%; 95%CI: 4.4–8.8%) to January 2021 (19.1%; 95%CI: 15.7–22.8%), though fluctuations were observed. In February, the seropositivity rate increased (64.9%; 95%CI: 60.5–69.0%), reached 84.9% (95%CI: 81.4–87.9%) in April, and was stabilized in July (79.1%; 95%CI: 75.4–82.5%). Further analysis performed using Jointpoint to appraise the trends in seropositivity found one breakpoint in March 2021, dividing this study period into two; between January 2020 and March 2021, where a significant increase was observed (MPC = 48.1%; p-value < 0.001), and between March and July 2021, where stability was observed (MPC = −1.05%; p-value = 0.779) (Figure 1).
Table 2 presents seropositivity rates by demographic characteristics between January and December 2020 (period 1; N = 6042), and January and July 2021 (period 2; N = 3478).
The univariable and multivariable analyses for the association between demographic characteristics and SARS-CoV-2 seropositivity between January and December 2020 are presented in Table 3.
In the multivariable analysis, we have shown that low socio-economic rank was an independent risk factor for seropositivity (OR = 2.49; 95%CI: 1.64–3.80), and residents of the southern district were less likely to be seropositive than residents of the central district (OR = 0.44; 95%CI: 0.22–0.87).
The univariable and multivariable analyses for the association between SARS-CoV-2 seropositivity and demographic characteristics between January and July 2021 are presented in Table 4.
In the multivariable analysis, the 40.00–64.99-year-old age group (OR = 1.36; 95%CI: 1.13–1.64, compared to 16.00–39.99), Jews and others (OR = 1.49; 95%CI: 1.19–1.86, compared to Arabs) and residents of the Northern district (OR = 1.55; 95%CI: 1.09–2.20 compared to Central district) were significantly more likely to be seropositive to SARS-CoV-2.

4. Discussion

The aim of the present survey was to characterize and to describe the dynamics of the seropositivity rate to SARS-CoV-2 before and after the introduction of the vaccine in Israel. The results showed that the seropositivity rate to SARS-CoV-2 increased slowly between January and December 2020 due to exposure to the virus; however, following the implementation of the vaccine program in Israel, a significant increase was observed until April 2021, stabilizing thereafter.
We have shown that between January and December 2020, seropositivity rates were between 0.4% (March 2020) and 10.2% (October 2020). During the same year, higher seropositivity rates were observed in New York City (May–July 2020; 18+ years; 23.6% [10] and June–October 2020; 18+ years; 24.3% [11]), Saudi-Arabia (May–July 2020; 18+ years; 19.3%) [12], Ireland (June–July 2020; 18+ years; 12.6%) [13], and Mexico (August–November 2020; 20–39 (27.9%), 40–59 (27.8%) and 60+ (18.6%) years) [14]. Similar rates were observed in Ethiopia (June–July 2020; 15+ years, 3.2%) [15], England (April–September 2020; 18–65 years; 5.9%) [16], Amsterdam, the Netherlands (June and October 2020; 18–70 years, 9.4%) [17], Germany (May–June 2020; 18+ years; 11.3%) [10], and the United States (July 2020 (3.5%), December 2020 (11.5%); 16+ years) [18]. In Australia, between April and June 2020, the seropositivity rate among 20 year olds and above was lower than 1% [19].
The seropositivity rates observed in our study between January and December 2020 corresponded with the extent of the actual exposure of the Israeli population to SARS-CoV-2, and reflects the three COVID-19 waves. The first COVID-19 wave, observed between March and April 2020, was reflected by an increase from 0.4% to 1.2% in seropositivity, respectively; the second, between September and October 2020, was reflected by an increase from 6.3% to 10.2% in seropositivity, respectively; and the third wave started in December 2020 (8.1%) until February 2021 (64.9%). The seropositivity rate is a reliable measure for exposure to SARS-CoV-2 in comparison to the number of confirmed COVID-19 cases reported, affected by the number of PCR tests performed and the testing policy, which changed rapidly throughout the outbreak period. It should be taken into account that the accuracy of the seropositivity obtained using ELISA is high, with 88% sensitivity and 98% specificity, but not perfect [9]. Indeed, we have interestingly shown that in January and February 2020, seropositivity rates were 2.0% and 1.2%, respectively, though officially, the first confirmed case (an imported one) was recorded only by the end of February. A potential explanation may be false positive results as the specificity of the test is 98% [9]; thus, 2% percent false positives are expected.
We have shown that SARS-CoV-2 infection-induced seroprevalence between January and December 2020 was independently associated with low socio-economic rank. Similar findings were also observed in the United States [10,20], in Mexico [14], in a study performed in Colombia among children [21], and in a previous sero-epidemiological survey we conducted among children between January 2020 and March 2021 in Israel [22]. SARS-CoV-2 is transmitted from person to person by exposure to infected respiratory fluids. As the number of contacts increase, the odds for infection become higher, and in a densely populated country such as Israel, high exposure to SARS-CoV-2 should be expected.
According to our data, by December 2020, 8.1% of those aged 16 years and above were exposed to SARS-CoV-2, while based on the national repository of PCR tests, 3.6% were confirmed as infected with SARS-CoV-2 [1]. Using these data, for every confirmed case in Israel, the number of SARS-CoV-2 seropositive cases was 2.2. Similar ratios were observed in the US in July 2020 (3.1) and in May 2021 (2.1) [18], as well as in a previous study we performed among children aged <16 years in Israel, where a ratio of 2.3 was demonstrated in December 2020 [22]. The disparity observed between these rates may be explained by asymptomatic infections, which were not tested and were not confirmed by PCR. Another explanation is the changing PCR test policy in Israel during the outbreak, which may have underestimated the number of those confirmed with SARS-CoV-2.
On December 20, 2020, a wide, aggressive campaign was launched in Israel, aiming to vaccinate the entire 16-year-old and above population against SARS-CoV-2 within a short time period, and by February 2021, 51.3% of the 16-year-old and above population were vaccinated in Israel [4]. We have shown that, in parallel to the introduction of the vaccine in Israel, the seropositivity rate increased significantly by April 2021 and remained constant at 80% until July 2021. Lower seropositivity rates were demonstrated in Los Angeles, California (April 2021; 18+ years; 72.2%) [23], Western Romania (March–June 2021; 18+ years; 45.6%) [24], and in the United States (May 2021; 18+ years; 20.2%) [18]. The seropositivity rates observed after the introduction of the vaccine in Israel reflect the cumulative effect of infection but also of vaccination, which was responsible for the significant increase in seropositivity rates, as the incidence of COVID-19 in those months in Israel was low. The third COVID-19 wave in Israel occurred between December 2020 and March 2021, and the fourth began in June 2021 and continued until October 2021. The parallelization of seropositivity and COVID-19 waves in Israel was impossible, since we could not differentiate between those who were vaccinated and those who were infected, and the rate of those who were infected in these waves was most probably negligible in comparison to the high vaccine acceptance in Israel.
After the introduction of the vaccine, we have shown a significant difference in seropositivity rate by ethnicity as Jews and others were more likely than Arabs to be seropositive. Differences in COVID-19 vaccination according to ethnicity were also demonstrated in the UK [25] and the USA [18,26]. This finding may be explained by the low COVID-19 vaccination rates among the Arab population in Israel, as was previously reported [27,28]. We have also demonstrated that residents of the Northern district were more likely to be seropositive. Geographical differences in seropositivity rates were also observed in the US [20], in Peru [29], and in a previous study we performed among children younger than 16 years [22]. In addition, the 40.00–64.99-year-old age group was more likely than the 16.00–39.99- and 65+-year-old groups to be seropositive. The high odds ratios for seropositivity in these population groups may reflect higher vaccination rates but may also reflect higher exposure to the virus. Since we were not able to differentiate the origin of anti-SARS-CoV-2 antibodies, robust conclusions cannot be drawn.
Future invasions of new variants of concern (VOCs) may cause breakthrough infections and reinfections, leading to difficulty in controlling a new COVID-19 wave. Strategies to mitigate the influence of VOCs in specific populations should be developed accordingly. Using a mathematical model performed to characterize the population-level impact of SARS-CoV-2 variants, it has been shown that the combination of high transmissibility and partial immune/vaccine escape increases not just the total size of the epidemic but also the number of primary infections in susceptible hosts, who are more likely to suffer severe illness or death [30].
The benefits of the study were the systematic, continuous, representative sample collection, the long study period, which reflected three COVID-19 waves in Israel, and the large sample size.
The disadvantages of the study were as follows. 1. The seropositivity rate to SARS-CoV-2 may have been overestimated, since the sample was based on five different laboratories, which perform routine blood tests obtained from patients, mostly with medical backgrounds and may be vulnerable to infection with SARS-CoV-2. 2. We were unable to link the serological result with the national repository of SARS-CoV-2 PCR test results, since the INSB sera samples are anonymous. 3. The inability to differentiate between exposure due to infection or vaccination. 4. Vaccination with SARS-CoV-2 was provided in Israel in an age-descending order with priorities to population groups who were at higher risk, such as the older population and healthcare workers. This gradation was not taken into account in the analysis. 5. Treatment with immunosuppressive medications, such as biologic disease-modifying anti-rheumatic drugs (bDMARDs), can reduce vaccine effectiveness; thus, a lack of drug anamnesis may be considered a major bias.

5. Conclusions

Our study results indicate a slight increase in the seropositivity rate to SARS-CoV-2 due to exposure to the virus, but a significant increase following the introduction of the vaccine in Israel. The challenges introduced during the global pandemic and the new emerging VOCs that appeared stress the importance of population-based seroprevalence studies, which provide an estimate of the extent of population protection against future waves, as well as the proportion of those who should be targeted for vaccination. The challenges increase in parallel to the implementation of a “living with COVID-19” strategy, which includes removing most restrictions.

Author Contributions

Conceptualization, R.B., L.K.-B., V.I., E.M., Y.L. and D.C.; Methodology, R.B. and V.I.; Software, R.B.; Validation, R.B. and V.I.; Formal analysis, R.B.; Investigation, R.B. and V.I.; Resources, R.B., L.K.-B., V.I. and E.M.; Data Curation, R.B., L.K.-B., V.I., E.M., Y.L. and D.C.; Writing—R.B., L.K.-B. and V.I.; Writing—Review and Editing, R.B., L.K.-B., V.I. and E.M.; Visualization, R.B.; Supervision, R.B. and V.I.; Project Administration, R.B. and V.I.; Funding Acquisition, None. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We would like to thank Rita Lokshin for her assistance in sample collection and separation in the Israel Center for Disease Control. We also would like to thank Kamalia Raguimov from Soroka University Medical Center; Ann But from Haifa and Western Galilee HMO Laboratory; Mohammed Elmraanih and Rasha Mansour from Schneider Children’s Medical Center; Rutty Hofrichter from Mayanei Hayeshua Medical Center, and Mohammed A. Odeh from Jerusalem HMO Laboratory for sample collection. We also would like to thank Tal Levin, Yara Knaaneh, Shiri Katz Likvornik, Ravit Koren, and Osnat Halpern for performing the technical laboratory work.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. COVID-19 Coronavirus Pandemic. Available online: https://www.worldometers.info/coronavirus/ (accessed on 19 September 2022).
  2. Chu, D.K.; Akl, E.A.; Duda, S.; Solo, K.; Yaacoub, S.; Schünemann, H.J. Physical distancing, face masks, and eye protection to prevent person-to-person transmission of SARS-CoV-2 and COVID-19: A systematic review and meta-analysis. Lancet 2020, 395, 1973–1987. [Google Scholar] [CrossRef]
  3. The Israel Central Bureau of Statistics. Population, by Population Group, Religion, Age and Sex, District and Sub-District. Available online: https://www.cbs.gov.il/he/Pages/search/yearly.aspx (accessed on 19 September 2022).
  4. Coronavirius in Israel. Available online: https://datadashboard.health.gov.il/COVID-19/general (accessed on 19 September 2022).
  5. World Health Organization. Tracking SARS-CoV-2 Variants. Available online: https://www.who.int/activities/tracking-SARS-CoV-2-variants (accessed on 19 September 2022).
  6. Cevik, M.; Grubaugh, N.D.; Iwasaki, A.; Openshaw, P. COVID-19 vaccines: Keeping pace with SARS-CoV-2 variants. Cell 2021, 184, 5077–5081. [Google Scholar] [CrossRef]
  7. Characterization and Classification of Local Authorities by the Socio-Economic Level of the Population in 2017. Local Councils and Municipalities—Rank, Cluster Membership, Population, Variable Values, Standardized Values and Ranking for the Variables Used in the Computation of the Index. Available online: https://www.cbs.gov.il/he/publications/DocLib/2021/socio_eco17_1832/h_print.pdf (accessed on 19 September 2022).
  8. Bassal, R.; Cohen, D.; Green, M.S.; Keinan-Boker, L. The Israel National Sera Bank: Methods, Representativeness, and Challenges. Int. J. Environ. Res. Public Health 2021, 18, 2280. [Google Scholar] [CrossRef] [PubMed]
  9. Indenbaum, V.; Koren, R.; Katz-Likvornik, S.; Yitzchaki, M.; Halpern, O.; Regev-Yochay, G.; Cohen, C.; Biber, A.; Feferman, T.; Cohen Saban, N.; et al. Testing IgG antibodies against the RBD of SARS-CoV-2 is sufficient and necessary for COVID-19 diagnosis. PLoS ONE 2020, 15, e0241164. [Google Scholar] [CrossRef] [PubMed]
  10. Pathela, P.; Crawley, A.; Weiss, D.; Maldin, B.; Cornell, J.; Purdin, J.; Schumacher, P.K.; Marovich, S.; Li, J.; Daskalakis, D. Seroprevalence of Severe Acute Respiratory Syndrome Coronavirus 2 Following the Largest Initial Epidemic Wave in the United States: Findings From New York City, 13 May to 21 July 2020. J. Infect. Dis. 2021, 224, 196–206. [Google Scholar] [CrossRef]
  11. Parrott, J.C.; Maleki, A.N.; Vassor, V.E.; Osahan, S.; Hsin, Y.; Sanderson, M.; Fernandez, S.; Levanon Seligson, A.; Hughes, S.; Wu, J.; 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, 188–195. [Google Scholar] [CrossRef]
  12. Mahallawi, W.H.; Al-Zalabani, A.H. The seroprevalence of SARS-CoV-2 IgG antibodies among asymptomatic blood donors in Saudi Arabia. Saudi J. Biol. Sci. 2021, 28, 1697–1701. [Google Scholar] [CrossRef]
  13. O’Callaghan, M.E.; Ryan, E.; Walsh, C.; Hayes, P.; Casey, M.; O’Dwyer, P.; Culhane, A.; Duncan, J.W.; Harrold, P.; Healy, J.; et al. SARS-CoV-2 infection in general practice in Ireland: A seroprevalence study. BJGP Open 2021, 5, bjgpo.2021.0038. [Google Scholar] [CrossRef]
  14. Basto-Abreu, A.; Carnalla, M.; Torres-Ibarra, L.; Romero-Martínez, M.; Martínez-Barnetche, J.; López-Martínez, I.; Aparicio-Antonio, R.; Shamah-Levy, T.; Alpuche-Aranda, C.; Rivera, J.A.; et al. Nationally representative SARS-CoV-2 antibody prevalence estimates after the first epidemic wave in Mexico. Nat. Commun. 2022, 13, 589. [Google Scholar] [CrossRef]
  15. Shaweno, T.; Abdulhamid, I.; Bezabih, L.; Teshome, D.; Derese, B.; Tafesse, H.; Shaweno, D. Seroprevalence of SARS-CoV-2 antibody among individuals aged above 15 years and residing in congregate settings in Dire Dawa city administration, Ethiopia. Trop. Med. Health 2021, 49, 55. [Google Scholar] [CrossRef]
  16. Coltart, C.E.M.; Wells, D.; Sutherland, E.; Fowler, A. National cross-sectional survey of 1.14 million NHS staff SARS-CoV-2 serology tests: A comparison of NHS staff with regional community seroconversion rates. BMJ Open 2021, 11, e049703. [Google Scholar] [CrossRef] [PubMed]
  17. Coyer, L.; Boyd, A.; Schinkel, J.; Agyemang, C.; Galenkamp, H.; Koopman, A.D.M.; Leenstra, T.; Moll van Charante, E.P.; van den Born, B.H.; Lok, A.; et al. SARS-CoV-2 antibody prevalence and correlates of six ethnic groups living in Amsterdam, the Netherlands: A population-based cross-sectional study, June–October 2020. BMJ Open 2022, 12, e052752. [Google Scholar] [CrossRef] [PubMed]
  18. Jones, J.M.; Stone, M.; Sulaeman, H.; Fink, R.V.; Dave, H.; Levy, M.E.; Di Germanio, C.; Green, V.; Notari, E.; Saa, P.; et al. Estimated US Infection- and Vaccine-Induced SARS-CoV-2 Seroprevalence Based on Blood Donations, July 2020–May 2021. JAMA 2021, 326, 1400–1409. [Google Scholar] [CrossRef]
  19. Gidding, H.F.; Machalek, D.A.; Hendry, A.J.; Quinn, H.E.; Vette, K.; Beard, F.H.; Shilling, H.S.; Hirani, R.; Gosbell, I.B.; Irving, D.O.; et al. Seroprevalence of SARS-CoV-2-specific antibodies in Sydney after the first epidemic wave of 2020. Med. J. Aust. 2021, 214, 179–185. [Google Scholar] [CrossRef]
  20. Li, Z.; Lewis, B.; Berney, K.; Hallisey, E.; Williams, A.M.; Whiteman, A.; Rivera-González, L.O.; Clarke, K.E.N.; Clayton, H.; Tincher, T.; et al. Social vulnerability and rurality associated with higher Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) infection-induced seroprevalence: A nationwide blood donor study—United States, July 2020–June 2021. Clin. Infect. Dis. 2022, 75, e133–e143. [Google Scholar] [CrossRef]
  21. Garay, E.; Serrano-Coll, H.; Rivero, R.; Gastelbondo, B.; Faccini-Martínez, Á.; Berrocal, J.; Pérez, A.; Badillo, M.; Martínez-Bravo, C.; Botero, Y.; et al. SARS-CoV-2 in eight municipalities of the Colombian tropics: High immunity, clinical and sociodemographic outcomes. Trans. R. Soc. Trop. Med. Hyg. 2021, 116, 139–147. [Google Scholar] [CrossRef] [PubMed]
  22. Indenbaum, V.; Lustig, Y.; Mendelson, E.; Hershkovitz, Y.; Glatman-Freedman, A.; Keinan-Boker, L.; Bassal, R. Under-diagnosis of SARS-CoV-2 infections among children aged 0–15 years, a nationwide seroprevalence study, Israel, January 2020 to March 2021. Euro Surveill. Bull. Eur. Mal. Transm. 2021, 26, 2101040. [Google Scholar] [CrossRef]
  23. Sood, N.; Pernet, O.; Lam, C.N.; Klipp, A.; Kotha, R.; Kovacs, A.; Hu, H. 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, e2144258. [Google Scholar] [CrossRef]
  24. Olariu, T.R.; Craciun, A.C.; Vlad, D.C.; Dumitrascu, V.; Marincu, I.; Lupu, M.A. SARS-CoV-2 Seroprevalence in Western Romania, March to June 2021. Medicina 2022, 58, 35. [Google Scholar] [CrossRef]
  25. Curtis, H.J.; Inglesby, P.; Morton, C.E.; MacKenna, B.; Green, A.; Hulme, W.; Walker, A.J.; Morley, J.; Mehrkar, A.; Bacon, S.; et al. Trends and clinical characteristics of COVID-19 vaccine recipients: A federated analysis of 57.9 million patients’ primary care records in situ using OpenSAFELY. Br. J. Gen. Pract. 2022, 72, e51–e62. [Google Scholar] [CrossRef]
  26. Pingali, C.; Meghani, M.; Razzaghi, H.; Lamias, M.J.; Weintraub, E.; Kenigsberg, T.A.; Klein, N.P.; Lewis, N.; Fireman, B.; Zerbo, O.; et al. COVID-19 Vaccination Coverage Among Insured Persons Aged ≥16 Years, by Race/Ethnicity and Other Selected Characteristics—Eight Integrated Health Care Organizations, United States, December 14, 2020–May 15, 2021. MMWR Morb. Mortal. Wkly. Rep. 2021, 70, 985–990. [Google Scholar] [CrossRef] [PubMed]
  27. Benderly, M.; Huppert, A.; Novikov, I.; Ziv, A.; Kalter-Leibovici, O. Fighting a pandemic: Sociodemographic disparities and coronavirus disease–2019 Vaccination gaps—A population study. Int. J. Epidemiol. 2022, 51, 709–717. [Google Scholar] [CrossRef] [PubMed]
  28. Gorelik, Y.; Anis, E.; Edelstein, M. Inequalities in initiation of COVID19 vaccination by age and population group in Israel—December 2020–July 2021. Lancet Reg. Health—Eur. 2022, 12, 100234. [Google Scholar] [CrossRef] [PubMed]
  29. Moreira-Soto, A.; Pachamora Diaz, J.M.; González-Auza, L.; Merino Merino, X.J.; Schwalb, A.; Drosten, C.; Gotuzzo, E.; Talledo, M.; Arévalo Ramirez, H.; Peralta Delgado, R.; et al. High SARS-CoV-2 Seroprevalence in Rural Peru, 2021: A Cross-Sectional Population-Based Study. mSphere 2021, 6, e0068521. [Google Scholar] [CrossRef]
  30. Bushman, M.; Kahn, R.; Taylor, B.P.; Lipsitch, M.; Hanage, W.P. Population impact of SARS-CoV-2 variants with enhanced transmissibility and/or partial immune escape. Cell 2021, 184, 6229–6242.e18. [Google Scholar] [CrossRef]
Figure 1. Seropositivity to SARS-CoV-2 between January 2020 and July 2021 in Israel, by month (N = 9520). * p-value < 0.05.
Figure 1. Seropositivity to SARS-CoV-2 between January 2020 and July 2021 in Israel, by month (N = 9520). * p-value < 0.05.
Vaccines 10 01663 g001
Table 1. Demographic characteristics of the total study population and by period (period 1 = January–December 2020 and period 2 = January–July 2021).
Table 1. Demographic characteristics of the total study population and by period (period 1 = January–December 2020 and period 2 = January–July 2021).
TotalPeriod 1Period 2
CategoryN%N%N%
Total9520100.06042100.03478100.0
AgeMean± Standard deviation; Minimum–Maximum45.7 ± 21.4; 16.0–103.645.8 ± 21.6; 16.0–100.645.5 ± 21.0; 16.0–103.6
Age group (years)16.00–39.99439746.2279646.3160146.0
40.00–64.99295331.0182830.3112532.4
65.00+216722.8141523.475221.6
GenderMale435345.7281946.7153444.1
Female516754.3322353.3194455.9
Birth countryIsrael715775.3447174.1268677.3
Other235224.7156325.978922.7
Population groupJews and others621570.8393670.3227971.8
Arabs256029.2166529.789528.2
DistrictJerusalem137914.586714.451214.8
North238225.1146124.292126.6
Haifa8929.45749.53189.2
Central8559.05348.93219.3
Tel Aviv9299.85519.137810.9
South255626.9171128.484524.4
Judea and Samaria5015.33315.51704.9
Socio-demographic rankHigh (6–10)309033.3196233.3112833.2
Low (1–5)620066.7392566.7227566.8
Table 2. SARS-CoV-2 seropositivity by demographic characteristics and time periods (period 1 = January–December 2020 and period 2 = January–July 2021).
Table 2. SARS-CoV-2 seropositivity by demographic characteristics and time periods (period 1 = January–December 2020 and period 2 = January–July 2021).
Period 1Period 2
CategoryTestedPositive%95%CI £TestedPositive%95%CI £
Age group (years)16.00–39.9927961164.23.4–5.01601109368.365.9–70.6
40.00–64.991828673.72.8–4.6112583574.271.6–76.8
65.00+1415664.73.6–5.975251868.965.4–72.2
GenderMale28191154.13.4–4.91534109571.469.0–73.6
Female32231344.23.5–4.91944135169.567.4–71.5
Birth countryIsrael44712024.53.9–5.22686190070.769.0–72.4
Other1563473.02.2–4.078954368.865.5–72.0
Population groupJews and others39361523.93.3–4.52279164372.170.2–73.9
Arabs1665895.44.3–6.589557364.060.8–67.2
DistrictJerusalem867546.24.7–8.051237372.868.8–76.7
North1461664.53.5–5.792169074.972.0–77.7
Haifa574152.61.5–4.331823473.668.4–78.4
Central534142.61.4–4.432124175.170.0–79.7
Tel Aviv551386.94.9–9.337824665.160.0–69.9
South1711432.51.8–3.484552261.858.4–65.1
Judea and Samaria331154.52.6–7.417013076.569.4–82.6
Socio-demographic rankHigh (6–10)1962402.01.5–2.8112885375.673.0–78.1
Low (1–5)39252035.24.5–5.92275156969.067.0–70.9
£ CI—Confidence interval.
Table 3. Univariable and multivariable analyses for the association between SARS-CoV-2 seropositivity and demographic characteristics in Israel, period 1 (January–December 2020).
Table 3. Univariable and multivariable analyses for the association between SARS-CoV-2 seropositivity and demographic characteristics in Israel, period 1 (January–December 2020).
UnivariableMultivariable
CategoryOR 95%CI £p-ValueOR 95%CI £p-Value
Agegroup (years)16.00–39.99Ref.
40.00–64.990.880.65–1.200.4099
65.00+1.130.83–1.540.4373
GenderMale0.980.76–1.260.8789
FemaleRef.
Birth countryIsrael1.531.10–2.110.01021.250.87–1.800.2242
OtherRef. Ref.
Population groupJews and othersRef. Ref.
Arabs1.411.08–1.840.01271.300.89–1.910.1771
DistrictJerusalem2.471.36–4.490.00311.060.54–2.080.8764
North1.760.98–3.160.05910.760.39–1.480.4154
Haifa1.000.48–2.080.99290.700.32–1.500.3566
CentralRef. Ref.
Tel Aviv2.751.47–5.140.00151.710.87–3.350.1175
South0.960.52–1.760.88930.440.22–0.870.0190
Judea and Samaria1.760.84–3.700.13401.050.48–2.290.9076
Socio-demographic rankHigh (6–10)Ref. Ref.
Low (1–5)2.621.86–3.69<0.00012.491.64–3.80<0.0001
OR—Odds Ratio; £ CI—Confidence interval.
Table 4. Univariable and multivariable analyses for the association between SARS-CoV-2 seropositivity and demographic characteristics in Israel, period 2 (January–July 2021).
Table 4. Univariable and multivariable analyses for the association between SARS-CoV-2 seropositivity and demographic characteristics in Israel, period 2 (January–July 2021).
UnivariableMultivariable
CategoryOR 95%CI £p-ValueOR 95%CI £p-Value
Age group (years)16.00–39.99Ref.
40.00–64.991.341.13–1.590.00081.361.13–1.640.0013
65.00+1.030.85–1.240.76531.020.82–1.250.8899
GenderMale1.100.94–1.270.2267
FemaleRef.
Birth countryIsrael1.100.92–1.300.3005
OtherRef.
Population groupJews and others1.451.23–1.71<0.00011.491.19–1.860.0005
ArabsRef.
DistrictJerusalem0.890.65–1.230.47771.150.79–1.680.4701
North0.990.74–1.330.95481.551.09–2.200.0140
Haifa0.920.65–1.320.66591.080.74–1.590.6890
CentralRef.
Tel Aviv0.620.44–0.860.00430.710.49–1.020.0601
South0.540.40–0.72<0.00010.850.60–1.200.3480
Judea and Samaria1.080.70–1.670.73291.320.82–2.110.2525
Socio-demographic rankHigh (6–10)1.401.19–1.64<0.00011.230.99–1.530.0607
Low (1–5)Ref.
OR—Odds Ratio; £ CI—Confidence interval.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Bassal, R.; Keinan-Boker, L.; Cohen, D.; Mendelson, E.; Lustig, Y.; Indenbaum, V. Estimated Infection and Vaccine Induced SARS-CoV-2 Seroprevalence in Israel among Adults, January 2020–July 2021. Vaccines 2022, 10, 1663. https://doi.org/10.3390/vaccines10101663

AMA Style

Bassal R, Keinan-Boker L, Cohen D, Mendelson E, Lustig Y, Indenbaum V. Estimated Infection and Vaccine Induced SARS-CoV-2 Seroprevalence in Israel among Adults, January 2020–July 2021. Vaccines. 2022; 10(10):1663. https://doi.org/10.3390/vaccines10101663

Chicago/Turabian Style

Bassal, Ravit, Lital Keinan-Boker, Dani Cohen, Ella Mendelson, Yaniv Lustig, and Victoria Indenbaum. 2022. "Estimated Infection and Vaccine Induced SARS-CoV-2 Seroprevalence in Israel among Adults, January 2020–July 2021" Vaccines 10, no. 10: 1663. https://doi.org/10.3390/vaccines10101663

APA Style

Bassal, R., Keinan-Boker, L., Cohen, D., Mendelson, E., Lustig, Y., & Indenbaum, V. (2022). Estimated Infection and Vaccine Induced SARS-CoV-2 Seroprevalence in Israel among Adults, January 2020–July 2021. Vaccines, 10(10), 1663. https://doi.org/10.3390/vaccines10101663

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop