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      Magnitude of asymptomatic COVID-19 cases throughout the course of infection: A systematic review and meta-analysis

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          Abstract

          Background

          Asymptomatic SARS-CoV-2 infections are responsible for potentially significant transmission of COVID-19. Worldwide, a number of studies were conducted to estimate the magnitude of asymptomatic COVID-19 cases. However, there is a need for more robust and well-designed studies to have a relevant public health intervention. Synthesis of the available studies significantly strengthens the quality of evidences for public health practice. Thus, this systematic review and meta-analysis aimed to determine the overall magnitude of asymptomatic COVID-19 cases throughout the course of infection using available evidences.

          Methods

          We followed the PRISMA checklist to present this study. Two experienced review authors (MA and DBK) were systematically searched international electronic databases for studies. We performed meta-analysis using R statistical software. The overall weighted proportion of asymptomatic COVID-19 cases throughout the course infection was computed. The pooled estimates with 95% confidence intervals were presented using forest plot. Egger’s tests were used to assess publication bias, and primary estimates were pooled using a random effects model. Furthermore, a sensitivity analysis was conducted to assure the robustness of the result.

          Results

          A total of 28 studies that satisfied the eligibility criteria were included in this systematic review and meta-analysis. Consequently, in the meta-analysis, a total of 6,071 COVID-19 cases were included. The proportion of asymptomatic infections among the included studies ranged from 1.4% to 78.3%. The findings of this meta-analysis showed that the weighted pooled proportion of asymptomatic COVID-19 cases throughout the course of infection was 25% (95%CI: 16–38). The leave-one out result also revealed that the weighted pooled average of asymptomatic SARS-CoV-2 infection was between 28% and 31.4%.

          Conclusions

          In conclusion, one-fourth of SARS-CoV-2 infections are remained asymptomatic throughout the course infection. Scale-up of testing, which targeting high risk populations is recommended to tackle the pandemic.

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          Most cited references41

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          Temporal dynamics in viral shedding and transmissibility of COVID-19

          Xi. He, Eric Lau, Peng Wu … (2020)
          We report temporal patterns of viral shedding in 94 patients with laboratory-confirmed COVID-19 and modeled COVID-19 infectiousness profiles from a separate sample of 77 infector-infectee transmission pairs. We observed the highest viral load in throat swabs at the time of symptom onset, and inferred that infectiousness peaked on or before symptom onset. We estimated that 44% (95% confidence interval, 25-69%) of secondary cases were infected during the index cases' presymptomatic stage, in settings with substantial household clustering, active case finding and quarantine outside the home. Disease control measures should be adjusted to account for probable substantial presymptomatic transmission.
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            Clinical and immunological assessment of asymptomatic SARS-CoV-2 infections

            Quan-Xin Long, Xiao-Jun Tang, Qiu-Lin Shi … (2020)
            The clinical features and immune responses of asymptomatic individuals infected with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) have not been well described. We studied 37 asymptomatic individuals in the Wanzhou District who were diagnosed with RT-PCR-confirmed SARS-CoV-2 infections but without any relevant clinical symptoms in the preceding 14 d and during hospitalization. Asymptomatic individuals were admitted to the government-designated Wanzhou People's Hospital for centralized isolation in accordance with policy1. The median duration of viral shedding in the asymptomatic group was 19 d (interquartile range (IQR), 15-26 d). The asymptomatic group had a significantly longer duration of viral shedding than the symptomatic group (log-rank P = 0.028). The virus-specific IgG levels in the asymptomatic group (median S/CO, 3.4; IQR, 1.6-10.7) were significantly lower (P = 0.005) relative to the symptomatic group (median S/CO, 20.5; IQR, 5.8-38.2) in the acute phase. Of asymptomatic individuals, 93.3% (28/30) and 81.1% (30/37) had reduction in IgG and neutralizing antibody levels, respectively, during the early convalescent phase, as compared to 96.8% (30/31) and 62.2% (23/37) of symptomatic patients. Forty percent of asymptomatic individuals became seronegative and 12.9% of the symptomatic group became negative for IgG in the early convalescent phase. In addition, asymptomatic individuals exhibited lower levels of 18 pro- and anti-inflammatory cytokines. These data suggest that asymptomatic individuals had a weaker immune response to SARS-CoV-2 infection. The reduction in IgG and neutralizing antibody levels in the early convalescent phase might have implications for immunity strategy and serological surveys.
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              Presymptomatic SARS-CoV-2 Infections and Transmission in a Skilled Nursing Facility

              Melissa M. Arons, Kelly Hatfield, Sujan Reddy … (2020)
              Abstract Background Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection can spread rapidly within skilled nursing facilities. After identification of a case of Covid-19 in a skilled nursing facility, we assessed transmission and evaluated the adequacy of symptom-based screening to identify infections in residents. Methods We conducted two serial point-prevalence surveys, 1 week apart, in which assenting residents of the facility underwent nasopharyngeal and oropharyngeal testing for SARS-CoV-2, including real-time reverse-transcriptase polymerase chain reaction (rRT-PCR), viral culture, and sequencing. Symptoms that had been present during the preceding 14 days were recorded. Asymptomatic residents who tested positive were reassessed 7 days later. Residents with SARS-CoV-2 infection were categorized as symptomatic with typical symptoms (fever, cough, or shortness of breath), symptomatic with only atypical symptoms, presymptomatic, or asymptomatic. Results Twenty-three days after the first positive test result in a resident at this skilled nursing facility, 57 of 89 residents (64%) tested positive for SARS-CoV-2. Among 76 residents who participated in point-prevalence surveys, 48 (63%) tested positive. Of these 48 residents, 27 (56%) were asymptomatic at the time of testing; 24 subsequently developed symptoms (median time to onset, 4 days). Samples from these 24 presymptomatic residents had a median rRT-PCR cycle threshold value of 23.1, and viable virus was recovered from 17 residents. As of April 3, of the 57 residents with SARS-CoV-2 infection, 11 had been hospitalized (3 in the intensive care unit) and 15 had died (mortality, 26%). Of the 34 residents whose specimens were sequenced, 27 (79%) had sequences that fit into two clusters with a difference of one nucleotide. Conclusions Rapid and widespread transmission of SARS-CoV-2 was demonstrated in this skilled nursing facility. More than half of residents with positive test results were asymptomatic at the time of testing and most likely contributed to transmission. Infection-control strategies focused solely on symptomatic residents were not sufficient to prevent transmission after SARS-CoV-2 introduction into this facility.
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                Author and article information

                Contributors
                Muluneh Alene:
                ORCID: https://orcid.org/0000-0002-1485-9014
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: MethodologyRole: SoftwareRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Leltework Yismaw: Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ValidationRole: Writing – review & editing
                Moges Agazhe Assemie:
                ORCID: https://orcid.org/0000-0003-0380-834X
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Daniel Bekele Ketema: Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SupervisionRole: ValidationRole: Writing – original draft
                Belayneh Mengist:
                ORCID: https://orcid.org/0000-0002-0363-8777
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: MethodologyRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Bekalu Kassie: Role: Data curationRole: Formal analysisRole: InvestigationRole: SupervisionRole: ValidationRole: Writing – review & editing
                Tilahun Yemanu Birhan: Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – review & editing
                Kin On Kwok: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS One
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 23 March 2021
                Publication date Collection: 2021
                Publication date PMC-release: 23 March 2021
                Volume: 16
                Issue: 3
                Electronic Location Identifier: e0249090
                Affiliations
                [1 ] Department of Public Health, Debre Markos University, Debre Markos, Ethiopia
                [2 ] Department of Midwifery, Debre Markos University, Debre Markos, Ethiopia
                [3 ] Department of Epidemiology and Biostatistics, University of Gondar, Gondar, Ethiopia
                Chinese University of Hong Kong, HONG KONG
                Author notes

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

                Author information
                https://orcid.org/0000-0002-1485-9014
                https://orcid.org/0000-0003-0380-834X
                https://orcid.org/0000-0002-0363-8777
                Article
                Publisher ID: PONE-D-20-28251
                DOI: 10.1371/journal.pone.0249090
                PMC ID: 7987199
                PubMed ID: 33755688
                SO-VID: 2c5d5cfc-a6f2-46e9-8bf8-9937562a1ea1
                Copyright © © 2021 Alene et al
                License:

                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.

                History
                Date received : 8 September 2020
                Date accepted : 11 March 2021
                Page count
                Figures: 3, Tables: 2, Pages: 11
                Funding
                The authors received no specific funding for this work.
                Categories
                Subject: Research Article
                Subject: Medicine and Health Sciences
                Subject: Medical Conditions
                Subject: Infectious Diseases
                Subject: Viral Diseases
                Subject: Covid 19
                Subject: Biology and life sciences
                Subject: Organisms
                Subject: Viruses
                Subject: RNA viruses
                Subject: Coronaviruses
                Subject: SARS coronavirus
                Subject: SARS CoV 2
                Subject: Biology and life sciences
                Subject: Microbiology
                Subject: Medical microbiology
                Subject: Microbial pathogens
                Subject: Viral pathogens
                Subject: Coronaviruses
                Subject: SARS coronavirus
                Subject: SARS CoV 2
                Subject: Medicine and health sciences
                Subject: Pathology and laboratory medicine
                Subject: Pathogens
                Subject: Microbial pathogens
                Subject: Viral pathogens
                Subject: Coronaviruses
                Subject: SARS coronavirus
                Subject: SARS CoV 2
                Subject: Biology and life sciences
                Subject: Organisms
                Subject: Viruses
                Subject: Viral pathogens
                Subject: Coronaviruses
                Subject: SARS coronavirus
                Subject: SARS CoV 2
                Subject: Medicine and Health Sciences
                Subject: Medical Conditions
                Subject: Infectious Diseases
                Subject: Respiratory Infections
                Subject: Medicine and Health Sciences
                Subject: Medical Conditions
                Subject: Respiratory Disorders
                Subject: Respiratory Infections
                Subject: Medicine and Health Sciences
                Subject: Pulmonology
                Subject: Respiratory Disorders
                Subject: Respiratory Infections
                Subject: Research and Analysis Methods
                Subject: Mathematical and Statistical Techniques
                Subject: Statistical Methods
                Subject: Metaanalysis
                Subject: Physical Sciences
                Subject: Mathematics
                Subject: Statistics
                Subject: Statistical Methods
                Subject: Metaanalysis
                Subject: Research and Analysis Methods
                Subject: Research Assessment
                Subject: Systematic Reviews
                Subject: Medicine and Health Sciences
                Subject: Diagnostic Medicine
                Subject: Virus Testing
                Subject: Research and Analysis Methods
                Subject: Database and Informatics Methods
                Subject: Database Searching
                Subject: Medicine and Health Sciences
                Subject: Epidemiology
                Subject: Pandemics
                Custom metadata
                Data Availability All relevant data are within the manuscript and its Supporting Information files.
                Outbreaks COVID-19

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