Trends in Respiratory Virus Infections During the COVID-19 Pandemic in Singapore, 2020 | Global Health | JAMA Network Open | JAMA Network
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Figure 1.  Numbers of Respiratory Virus Tests and Positive Tests for Different Viruses in 2019 and 2020
Numbers of Respiratory Virus Tests and Positive Tests for Different Viruses in 2019 and 2020

Blue bars indicate weekly numbers of multiplex tests performed, and colored lines indicate positive tests for different viruses per calendar week in 2019 and 2020. Influenza (flu) seasons are denoted by vertical lines according to Singapore Health Hub.4 AdV indicates adenovirus; EV/RV, enterovirus/rhinovirus (combined test); hCoV, common cold coronaviruses HKU1, NL63, 229E, and OC43; MPV, human metapneumovirus; PIV 1-4, parainfluenza viruses 1-4; and RSV, respiratory syncytial virus.

Figure 2.  Percentage of Positive Tests for Different Respiratory Viruses in 2019 and in 2020
Percentage of Positive Tests for Different Respiratory Viruses in 2019 and in 2020

AdV indicates adenovirus; EV/RV, enterovirus/rhinovirus (combined test); flu A/B, influenza virus A/B; hCoV, common cold coronaviruses HKU1, NL63, 229E, and OC43; MPV, human metapneumovirus; PIV 1-4, parainfluenza viruses 1-4; and RSV, respiratory syncytial virus.

1.
Cowling  BJ, Ali  ST, Ng  TWY,  et al.  Impact assessment of non-pharmaceutical interventions against coronavirus disease 2019 and influenza in Hong Kong: an observational study.   Lancet Public Health. 2020;5(5):e279-e288. doi:10.1016/S2468-2667(20)30090-6 PubMedGoogle ScholarCrossref
2.
Fricke  LM, Glöckner  S, Dreier  M, Lange  B.  Impact of non-pharmaceutical interventions targeted at COVID-19 pandemic on influenza burden—a systematic review.   J Infect. 2021;82(1):1-35. doi:10.1016/j.jinf.2020.11.039 PubMedGoogle ScholarCrossref
3.
Partridge  E, McCleery  E, Cheema  R,  et al.  Evaluation of seasonal respiratory virus activity before and after the statewide COVID-19 shelter-in-place order in Northern California.   JAMA Netw Open. 2021;4(1):e2035281. doi:10.1001/jamanetworkopen.2020.35281 PubMedGoogle Scholar
4.
Health Hub. Influenza. Accessed November 4, 2020. https://www.healthhub.sg/a-z/diseases-and-conditions/103/topics_influenza
5.
Hale  T, Atav  T, Hallas  L, Kira  B, Phillips  T, Petherick  A,  et al. Coronavirus government response tracker. Accessed January 4, 2021. https://www.bsg.ox.ac.uk/research/research-projects/coronavirus-government-response-tracker
6.
Kutter  JS, Spronken  MI, Fraaij  PL, Fouchier  RAM, Herfst  S.  Transmission routes of respiratory viruses among humans.   Curr Opin Virol. 2018;28:142-151. doi:10.1016/j.coviro.2018.01.001 PubMedGoogle ScholarCrossref
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    Research Letter
    Infectious Diseases
    June 28, 2021

    Trends in Respiratory Virus Infections During the COVID-19 Pandemic in Singapore, 2020

    Author Affiliations
    • 1Department of Microbiology, Singapore General Hospital, Singapore
    • 2Infectious Disease Service, Department of Paediatric Medicine, KK Women’s and Children’s Hospital, Singapore
    • 3Lee Kong Chian School of Medicine, Nanyang Technological University, Singapore
    • 4Duke–National University of Singapore Graduate Medical School, Singapore
    • 5Yong Loo Lin School of Medicine, National University of Singapore, Singapore
    • 6Department of Pathology and Laboratory Medicine, KK Women’s and Children’s Hospital, Singapore
    • 7Department of Molecular Pathology, Singapore General Hospital, Singapore
    • 8Genome Institute of Singapore, Agency for Science, Technology, and Research (A*STAR), Singapore
    JAMA Netw Open. 2021;4(6):e2115973. doi:10.1001/jamanetworkopen.2021.15973
    Introduction

    The COVID-19 pandemic brought unprecedented challenges to the world. Many jurisdictions implemented control measures, such as border closures, lockdowns, school and business closures, travel restrictions, mask wearing, and social distancing. This was associated with changes in the prevalence of other respiratory viruses, predominantly influenza viruses1,2 but others as well.3

    Singapore represents a unique setting that is credited with having a successful COVID-19 response. It went through different response phases, from prelockdown (pandemic level 3) to a full lockdown (known as circuit breaker), followed by a phased reopening, during which schools and businesses reopened but social distancing measures and universal mask wearing remained in place (eTable in the Supplement). Our aim in this study was to assess the associated changes in respiratory virus prevalence in 2020 compared with the prepandemic year 2019.

    Methods

    In this cross-sectional study, data from respiratory virus multiplex polymerase chain reaction tests from 3 major public hospitals in Singapore for 2019 and 2020 were compiled (eMethods in the Supplement). This included hospital A, a women’s and children’s hospital (800 beds); hospital B, offering pediatric and adult services (1200 beds); and hospital C, with adult services (1700 beds). Weekly numbers of tests and positive results for each virus were collated. Institutional review board application and informed consent were not required under SingHealth institutional rules. We followed the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) reporting guideline. A 1-tailed t test (with significance set at P = .05) was used to compare means. Data were compiled using Excel 2013 (Microsoft) and analyzed using R version 3.6.2 (R Project for Statistical Computing).

    Results

    The full data set comprised 42 558 test results, 19 898 (46.8%) from 2019 and 22 660 (53.2%) from 2020. During 2019, influenza A/B, enterovirus/rhinovirus, and respiratory syncytial virus (RSV) were most commonly detected (Figure 1).4 A peak of influenza activity occurred during December 2019 to January 2020 (prepeak, week 33 to 45, 2019: mean [SD], 12.9 [2.7] cases per 100 samples; peak, week 46, 2019, to week 5, 2020: mean [SD], 29.8 [7.5] cases per 100 samples; P < .001). Enterovirus/rhinovirus activity was high starting in the second half of 2019 (week 1 to 25, 2019: mean [SD], 20.4 [2.6] cases per 100 samples; week 26 to 52, 2019: mean [SD], 25.2 [5.2] cases per 100 samples; P < .001). Adenovirus activity increased starting in approximately September 2019 (week 1 to 38, 2019: mean [SD], 4.6 [1.6] cases per 100 samples; week 39 to 52, 2019: mean [SD], 8.5 [2.5] cases per 100 samples; P < .001).

    Implementation of prelockdown measures was associated with a reduction of influenza and most other viruses (Figure 1 and Figure 2).5 However, a decrease of enterovirus/rhinovirus and adenovirus was only observed during lockdown, when movement restrictions were implemented (eg, prelockdown, enterovirus/rhinovirus, week 1-14, 2020: mean [SD], 16.1 [2.6] cases per 100 samples; lockdown, week 15-22, 2020: mean [SD], 3.9 [3.1] cases per 100 samples; P < .001). This phase saw substantial decreases across all respiratory viruses.

    During reopening, low levels of all viruses were sustained for approximately 13 weeks, but a reemergence of enterovirus/rhinovirus occurred in early September and a less pronounced rebound of adenovirus in mid-October (enterovirus/rhinovirus, week 15-36, 2020: mean [SD], 2.6 [2.4] cases per 100 samples; week 37-52, 2020: mean 27.1 [7.2] cases per 100 samples; P < .001; adenovirus, week 15-42, 2020: mean 1.3 [0.6] cases per 100 samples; week 43-52, 2020: mean 3.1 [1.0] cases per 100 samples; P < .001). Most other viruses remained at historically low levels until the end of the year, despite reopening businesses and schools (with mask wearing) and gradual resumption of activities. Small increases for RSV, parainfluenza, and metapneumovirus were seen in November and December.

    Discussion

    COVID-19 pandemic control measures in Singapore were associated with changes across a broad range of respiratory viruses; the changes were most substantial during lockdown. However, the patterns of decrease and subsequent reemergence differed between viruses and pandemic response phases.

    A decrease in influenza was already seen following relatively modest control measures, including mask-wearing recommendations among only ill or symptomatic individuals. Influenza remained nearly absent for the remainder of 2020. International travel restrictions likely contributed to this.

    For enterovirus/rhinovirus and adenovirus, reductions were only seen after lockdown, and these viruses rebounded earlier than others. Continued mandatory mask wearing did not appear to prevent this. These are small, hydrophilic, nonenveloped viruses that are hardier than others, and we hypothesize that greater relative propensity for contact transmission, in addition to droplet transmission, at a time of increasing social contacts during reopening may have contributed to these findings.6 The multitude of different enterovirus/rhinovirus and adenovirus types may be another factor contributing to their reemergence.

    This study has limitations. The data were obtained from routine diagnostic tests and thus depend on prevailing test requesting patterns. Changes in health care–seeking behavior during the pandemic may have influenced the trends observed.

    In conclusion, Singapore’s COVID-19 response represents a unique situation of effectively enforced populationwide interventions that resulted in a broad decrease in the transmission of respiratory viruses. With phased relaxation of measures, different viruses showed different propensities for reemergence, with most enveloped viruses remaining contained at a time of continued universal mask wearing. Further studies into these phenomena are a matter of public health importance; this should include assessing the changes into 2021, differences between adults and children, and associating changes more precisely with different pandemic control measures and their relaxation.

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    Article Information

    Accepted for Publication: May 4, 2021.

    Published: June 28, 2021. doi:10.1001/jamanetworkopen.2021.15973

    Open Access: This is an open access article distributed under the terms of the CC-BY License. © 2021 Wan WY et al. JAMA Network Open.

    Corresponding Author: Matthias Maiwald, MD, Department of Pathology and Laboratory Medicine, KK Women’s and Children’s Hospital, 100 Bukit Timah Rd, Singapore 229899, Singapore (matthias.maiwald@singhealth.com.sg).

    Author Contributions: Drs Wan and Maiwald had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

    Concept and design: Wan, Thoon, Chan, Maiwald.

    Acquisition, analysis, or interpretation of data: All authors.

    Drafting of the manuscript: Wan, Maiwald.

    Critical revision of the manuscript for important intellectual content: All authors.

    Statistical analysis: Wan, Ramasamy.

    Administrative, technical, or material support: Wan, Loo, Chan, Oon, Maiwald.

    Supervision: Oon, Maiwald.

    Conflict of Interest Disclosures: None reported.

    Additional Contributions: We thank the Department of Laboratory Medicine, National University Hospital, Singapore, for the generous provision of the respiratory virus data from the hospital.

    References
    1.
    Cowling  BJ, Ali  ST, Ng  TWY,  et al.  Impact assessment of non-pharmaceutical interventions against coronavirus disease 2019 and influenza in Hong Kong: an observational study.   Lancet Public Health. 2020;5(5):e279-e288. doi:10.1016/S2468-2667(20)30090-6 PubMedGoogle ScholarCrossref
    2.
    Fricke  LM, Glöckner  S, Dreier  M, Lange  B.  Impact of non-pharmaceutical interventions targeted at COVID-19 pandemic on influenza burden—a systematic review.   J Infect. 2021;82(1):1-35. doi:10.1016/j.jinf.2020.11.039 PubMedGoogle ScholarCrossref
    3.
    Partridge  E, McCleery  E, Cheema  R,  et al.  Evaluation of seasonal respiratory virus activity before and after the statewide COVID-19 shelter-in-place order in Northern California.   JAMA Netw Open. 2021;4(1):e2035281. doi:10.1001/jamanetworkopen.2020.35281 PubMedGoogle Scholar
    4.
    Health Hub. Influenza. Accessed November 4, 2020. https://www.healthhub.sg/a-z/diseases-and-conditions/103/topics_influenza
    5.
    Hale  T, Atav  T, Hallas  L, Kira  B, Phillips  T, Petherick  A,  et al. Coronavirus government response tracker. Accessed January 4, 2021. https://www.bsg.ox.ac.uk/research/research-projects/coronavirus-government-response-tracker
    6.
    Kutter  JS, Spronken  MI, Fraaij  PL, Fouchier  RAM, Herfst  S.  Transmission routes of respiratory viruses among humans.   Curr Opin Virol. 2018;28:142-151. doi:10.1016/j.coviro.2018.01.001 PubMedGoogle ScholarCrossref
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