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Open Access

Peer-reviewed

Research Article

Seroprevalence and SARS-CoV-2 invasion in general populations: A scoping review over the first year of the pandemic

  • Clémentine Metzger,

    Roles Data curation, Writing – original draft

    Affiliation CHRU -Nancy, INSERM, Université de Lorraine, CIC Epidémiologie clinique, F-54000, Nancy, France

    ⨯
  • Taylor Leroy,

    Roles Data curation, Resources, Writing – review & editing

    Affiliation CHRU -Nancy, INSERM, Université de Lorraine, CIC Epidémiologie clinique, F-54000, Nancy, France

    ⨯
  • Agathe Bochnakian,

    Roles Data curation, Writing – review & editing

    Affiliation CHRU -Nancy, INSERM, Université de Lorraine, CIC Epidémiologie clinique, F-54000, Nancy, France

    ⨯
  • Hélène Jeulin,

    Roles Conceptualization, Writing – review & editing

    Affiliations Université de Lorraine, CNRS, LCPME, F‐54000, Nancy, France, Laboratoire de Virologie, CHRU de Nancy Brabois, F‐54500, Nancy, France

    ⨯
  • Anne Gegout-Petit,

    Roles Conceptualization, Writing – review & editing

    Affiliation Université de Lorraine, CNRS, Inria, IECL, F-54000, Nancy, France

    ⨯
  • Karine Legrand,

    Roles Writing – review & editing

    Affiliation CHRU -Nancy, INSERM, Université de Lorraine, CIC Epidémiologie clinique, F-54000, Nancy, France

    ⨯
  • Evelyne Schvoerer,

    Roles Conceptualization, Writing – review & editing

    Affiliations Université de Lorraine, CNRS, LCPME, F‐54000, Nancy, France, Laboratoire de Virologie, CHRU de Nancy Brabois, F‐54500, Nancy, France

    ⨯
  • Francis Guillemin

    Roles Conceptualization, Resources, Supervision, Writing – review & editing

    francis.guillemin@chru-nancy.fr

    Affiliation CHRU -Nancy, INSERM, Université de Lorraine, CIC Epidémiologie clinique, F-54000, Nancy, France

    ⨯

Abstract

Since the beginning of the COVID-19 pandemic, counting infected people has underestimated asymptomatic cases. This literature scoping review assessed the seroprevalence progression in general populations worldwide over the first year of the pandemic. Seroprevalence studies were searched in PubMed, Web of Science and medRxiv databases up to early April 2021. Inclusion criteria were a general population of all ages or blood donors as a proxy. All articles were screened for the title and abstract by two readers, and data were extracted from selected articles. Discrepancies were resolved with a third reader. From 139 articles (including 6 reviews), the seroprevalence estimated in 41 countries ranged from 0 to 69%, with a heterogenous increase over time and continents, unevenly distributed among countries (differences up to 69%) and sometimes among regions within a country (up to 10%). The seroprevalence of asymptomatic cases ranged from 0% to 31.5%. Seropositivity risk factors included low income, low education, low smoking frequency, deprived area residency, high number of children, densely populated centres, and presence of a case in a household. This review of seroprevalence studies over the first year of the pandemic documented the progression of this virus across the world in time and space and the risk factors that influenced its spread.

Citation: Metzger C, Leroy T, Bochnakian A, Jeulin H, Gegout-Petit A, Legrand K, et al. (2023) Seroprevalence and SARS-CoV-2 invasion in general populations: A scoping review over the first year of the pandemic. PLoS ONE 18(4): e0269104. https://doi.org/10.1371/journal.pone.0269104

Editor: Chandrabose Selvaraj, Alagappa University, INDIA

Received: October 25, 2021; Accepted: May 13, 2022; Published: April 19, 2023

Copyright: © 2023 Metzger et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: Toutes les données pertinentes se trouvent dans le manuscrit et ses fichiers d’informations à l’appui All relevant data is in the manuscript and its supporting information files.

Funding: The study was funded by Metropole du Grand (https://www.grandnancy.eu/accueil/). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

The coronavirus disease outbreak, caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), was first reported in Wuhan in December 2019 and spread rapidly to other parts of the world. On April 30, 2021, COVID-19 accounted for 150,000,000 confirmed cases worldwide, more than 3,000,000 deaths and about 87,000,000 recoveries, representing the deadliest pandemic in decades [1]. To contain the spread of the virus, daily counts of laboratory-confirmed cases and deaths have been published in real time.

The emergence of this new virus has resulted in an important early warning plan, and the WHO has tried to understand its modes of transmission, severity, characteristics and risk factors for infection. This alert plan was targeted to manage this epidemic, which became a pandemic barely 2 months after its appearance [2]. The plan includes refining case referrals, reinforcing surveillance, and defining the main epidemiological characteristics of COVID-19 to help understand the spread, severity, spectrum of the disease and impact on the community and to provide guidance on the application of countermeasures such as case isolation and contact tracing. Daily counts of confirmed COVID-19 cases and deaths alone provide incomplete information on the relative abundance of epidemiological compartments of a susceptible infected, recovered or deceased population. Therefore, the WHO has recommended repeatedly carrying out seroprevalence surveys in multiple geographical settings [2].

Several serological surveys of SARS-CoV-2 have been performed, and others are ongoing since the beginning of the COVID-19 pandemic, finding variable seroprevalence in different countries, sometimes even among regions of the same country [3,4].

The purpose of this literature scoping review was to summarise and map the results of the seroprevalence studies according to the time since the onset of the pandemic and geographical region and to identify risk factors.

Methods

We performed a literature review of seroprevalence studies conducted in different populations since the onset of the pandemic up to April 10, 2021, searching PubMed, Web of Science and medRxiv databases. We searched references of citations for reviews, which allowed for additional references to be added.

Eligibility

We included original articles and reviews written in English language that reported data for the general population living in a defined geographical area. We considered a general population as a population-based sample, a described general population sample, or the inclusion of men and women of unselected categories of all ages in the population, preferably (but not exclusively) obtained by a random sampling technique from a large population (survey or database). We also included blood donors as a proxy for the general population. We excluded studies of health care workers, people attending a clinic or a hospital, a professional branch (industry, factory, farmers, university) and a particular population (students, nursing home) as well as modelling studies.

Search strategy

The strategy consisted of searching PubMed and medRxiv with “(Covid OR SARS-CoV-2) AND seroprevalence” and Web of Science with “covid AND seroprevalence”. Articles were selected by reading titles and abstracts. All article titles were first read by two readers (CM, AB), then by a third one (FG or TL), which allowed for discussion in case of discrepancies after abstract reading to obtain consensus. Full-article reading allowed for the final selection of relevant studies and data extraction.

Data extraction

Data extraction was conducted by three authors who used a standardized form. The data collected, when available, were location; selection criteria; type of population; sample size and method; seroprevalence; serological test and type of Ig antibody tested; time period of the study; presence and type of symptoms; risk factors such as age, sex, ethnicity and origin; local medical resources; and social class.

Results

Study characteristics

The search strategy yielded 742 articles from PubMed, 281 from Web of Science and 1141 from medRxiv. The selection of relevant articles, after removal of duplicates, yielded 139 articles, including 6 reviews and meta-analysis [5–10], published from January 1, 2020 to April 10, 2021 (Fig 1). Article references described in this section refer to those in Table 1. Of the 133 original studies, 31 were of blood donors. In 64 studies, the sample included all ages; in 40, it included people ≥ 18 years old; and a few studied people < age 18 years (n = 17) or 10 years (n = 12). Some studies identified co-morbidities or asymptomatic cases. The samples ranged from 194 to 10,294,728 participants.

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Fig 1. PRISMA flowchart.

https://doi.org/10.1371/journal.pone.0269104.g001

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Table 1. Characteristics of country, methods, population of seroprevalence of included studies.

https://doi.org/10.1371/journal.pone.0269104.t001

Serological status

The determination of seroprevalence in most studies involved the ELISA test, which detects IgG and IgM antibodies. Other studies used a serum epitope repertoire analysis or a plaque reduction neutralization test, and IgA antibodies were also identified. Estimated seroprevalence was 0 to 69% (Table 1). Among the 133 original studies, 13 studies investigated IgG [11–23], 8 studies IgG or IgM [24–31], two studies IgG and IgM [32,33], one study IgA or IgG [34], one study IgG only or IgG and IgM [35] and one study IgG or IgM or both simultaneously [36].

Prevalence by continent and over time

General population.

The most-represented and explored territories were Europe, with 34 studies, distributed among Italy (9), France (4), England (4), Spain (3), Germany (3), Slovenia (2), Switzerland (2), Luxembourg (1), Austria (1), Hungary (1), Denmark (1), Faroe Island (1), Greece (1), Albania (1), Sweden (1), United Kingdom (1), Georgia (1), Poland (1), and Estonia (1); the United States, with 24 studies; other Organisation for Economic Co-operation and Development (OECD) countries, with Japan (3), Canada (1), and Australia (1); and other countries, with India (12), Brazil (6), China (6), Iran (4), Argentina (1), Iraq (1), Palestine (1), Pakistan (1), Qatar (1). South Africa (1), and Sudan (1). Fig 2 represents the spread of seroprevalence estimates in each continent over the study period.

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Fig 2. Seroprevalence (%) in each continent over the observation period.

https://doi.org/10.1371/journal.pone.0269104.g002

Most studies (n = 52) estimated a seroprevalence of SARS-CoV-2 of 0 to 7%; for more than half, the seroprevalence was < 5%. England had the highest seroprevalence, estimated at 69% from July to September 2020, followed by Iraq, at 62.6% between July 2020 and February 2021.

Blood donors.

The most represented and explored territories were Europe, with 10 studies, distributed among Italy (3), France (2), Germany (1), Denmark (1), Netherlands (1), Sweden (1), and Scotland (1); the United States, with 7 studies; other OECD countries, with Canada (1), Australia (1) and Mexico (1); and other countries, with Kenya (3), Brazil (2), Saudi Arabia (2), China (1), South Africa (1), Pakistan (1), and Panama (1).

Most studies (n = 20) estimated a seroprevalence of SARS-CoV-2 of 0 to 7%; for more than half, the seroprevalence was < 5% (n = 17).

South Africa had the highest seroprevalence, estimated at 63% in January 2021, and the lowest seroprevalence was estimated in the United States, 0% in March 2020.

Symptoms.

A total of 84 articles [3,4,13,15,16,18,21,23,29,31,32,35,37–108] focused on COVID-19–related symptoms. The seroprevalence of asymptomatic cases ranged from 0% (Q1-Q3 1–3%) to 31.5% (3–7%). Only 35 articles explicitely assessed asymptomatic populations [18,19,24–26,32,45,47,53,56,59,64,66,69,75,76,78,81,83,89,90,92,93,95,98,99,102,105–114]. The symptoms most strongly associated with seropositivity were anosmia, agueusia, fever, fatigue, rhinorrhea, sore throat, breathing difficulties, flu-like symptoms, cough, dyspnoea, myalgias, headache and asthenia. Diarrhoea, muscle aches, and chest pain were also common.

Risk factors.

The most densely populated centres were the most affected by COVID-19 [8,16,20,32,40,41,48,50,53,55,56,59,71,76,78,81,86,87,88,91,92,94,95,101,102,106,115–126]. Sex was examined in 14 studies, which found mostly no significant difference (one a higher seroprevalence in men and 6 a higher seroprevalence in women).

In articles published by the end of 2020 [91,95,99,118], the age group most significantly affected was young adults aged 18–30 years. Other studies showed an increase in seroprevalence in older age groups. For children, eighteen studies [37,47,49,56,60,68,75,79,83,85,88,89,93,108,119,122,127,128] showed significantly lower seroprevalence than for adults. For articles published after late 2020, the age ranges were narrower than in articles published at the beginning of the pandemic. Since the emergence of the virus, young populations have also been found to have high seroprevalence and should not be overlooked [40,96]. The impact of social disadvantage was documented in the general population and blood donors in a comparison of seroprevalence according to income [32,47,68,104,126,129–134] or education level [18,19,20,47,48,53,57,68,82,99,130–138]. Prevalence was higher in the lowest than highest income groups (prevalence doubled [32], from 1.8% to 3.7%). The seroprevalence was two times higher with low than high education [91]. Thirteen studies showed that the risk of seropositivity increased by about 30% with a confirmed COVID-19 case in the household [23,32,36,47,55,59,68,75,79,88,92,125,136]. Ten studies showed that the risk of seropositivity increased with the number of children in the household [16,25,55,71,77,88,116,120,125,133]. The highest seroprevalence was found in the most deprived areas [59,67,68,86,92,104,126,130–133,139,140]. Finally, seven studies [18,60,68,87,93,116,141] found a decrease in SARS-CoV-2 seroprevalence associated with greater freqency of smoking.

Discussion

Published studies of seroprevalence of SARS-CoV-2 in the general population over the year after the onset of the pandemic up to early April 2021 showed estimates ranging from 0% in Palestine in the West Bank between June and July 2020 to 69% in England between July and September 2020, with different dynamics across continents.

This review purposedly focused on the first year of the pandemic to better understand the spread and dynamics from the early stages of the pandemic and to summarize identified factors for SARS-CoV-2 penetration that could further serve as a reference for adapted measures to mitigate future epidemics. Such measures include barriers, social distancing, evolving vaccines according to the molecular and biological monitoring of viruses, and preventive or early treatments to avoid severity.

Fig 2 shows that the blood donors were not fully representative of the general population. Their seroprevalence and respective peaks show variations of lower magnitude in general. Blood donors could have been an early resource for documenting the epidemic before their decrease in frequency, with population-based studies taking place later. Some continents have fewer donors than others, probably related to national heath care organisation.

The variations observed across studies, besides the true virus exposure and spread differences over space and time within countries, could be due to different sampling techniques and the use of different serological tests. Our results suggest that the number of symptomatic cases was lower than the number of actual cases, despite only few studies (n = 21) characterizing asymptomatic seropositive cases.

Most of the studies did not find or found minimal differences regarding sex. Age categories analysis did not yet reveal any conclusive results. Social disadvantage seemed to play a role, at least for the least well-off categories, but the impact of belonging to the most privileged categories, whatever the classification used, remains to be elucidated. Finally, the presence of a COVID-19 case in a household increasing the risk of the other members has been demonstrated consistently for developing antibodies.

This review had a longer study period than six previous reviews; it focused on general populations and blood donors; it covered a larger world area by including all continents as compared with Grant et al. [8], Rostami et al. [10], Chen et al. [6] and Levesque and Maybury[9], and it summarised a number of risk factors identified, mostly of a sociodemographic nature.

A limitation of this scoping review is the heterogeneity of samples with different age ranges, so seroprevalence data are not fully comparable. Potential biases in such seroprevalence observational studies also do not account for SARS-COV-2–related deaths. Also, we did not include grey literature because we did not know how to search such literature in the particular context of this pandemic with so much suspicion of non-peer–reviewed publications. A third limitation is that we did not assess the methodological quality of the studies reviewed. Finally, the results of seroprevalence studies may have been affected by the specificity and sensitivity of different serological methods used.

In conclusion, from this scoping review of seroprevalence studies over the first year of the COVID-19 pandemic, the seroprevalence of SARS-CoV-2 varied according to the study period, with lower seroprevalence at the beginning of the epidemic than between July and September 2020. This review documented the progression of this virus across the world in time and space and the risk factors that influenced its spread.

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