Changes in the pathogenic spectrum of acute respiratory tract infections during the COVID-19 epidemic in Beijing, China: A large-scale active surveillance study
Authors: Mei Dong, Ming Luo, Aihua Li, Hui Xie, Cheng Gong, Juan Du, Xinrui Wang, Maozhong Li, Xue Wang, Yiting Wang, Haiyan Zhang, Xiaoxing Yang, Wei Cai, Hongjun Li, Wenzeng Zhang, Lijun Ren, Qing-Bin Lu, Fang Huang
Journal: Journal of Infection (2021)

•The positive rate of pathogens decreased from 32.6% before the COVID-19 to 10.97% during the COVID-19.•Among all the pathogens, only seasonal HCoV positive rate increased, especially in children.•The decrease of the positive rate was closely relating to public health measures against COVID-19. Poole and colleagues demonstrated the impact of coronavirus disease 2019 (COVID-19) pandemic on the epidemiology of general respiratory viruses.1Poole S. Brendish N.J. Clark T.W. SARS-CoV-2 has displaced other seasonal respiratory viruses: results from a prospective cohort study.J Infect. Dec 2020; 81 (PubMed PMID: 33207254. Pubmed Central PMCID: PMC7666810. Epub 2020/11/19): 966-972Abstract Full Text Full Text PDF PubMed Scopus (55) Google Scholar The prevalence of non-SARS-CoV-2 viruses during the COVID-19 epidemic has not been wildly reported in China. We conducted to analyze the surveillance data of respiratory pathogens to explore the impact of public health measures against COVID-19 on the prevalence of non-SARS-CoV-2 pathogens in China. Among 41,630 acute respiratory tract infections (ARTIs) between 01/02/2015 and 31/01/2021 in 35 hospitals from the Respiratory Pathogen Surveillance System (detailed in Supplemental materials), 37,490 (25,658 adults and 11,832 children) occurred before the COVID-19 epidemic (01/02/2015–31/01/2020), and 4140 (3379 adults and 761 children) occurred during the COVID-19 epidemic (01/02/2020–31/01/2021) (Fig. 1A-B). All 41,630 cases were tested for 11 respiratory tract pathogens and 13,630 (32.74%, 95% CI 32.29% to 33.19%) had at least one positive result. Before the COVID-19 epidemic, the most common pathogen among the positive cases was influenza virus (IFV), followed by mycoplasma pneumoniae (MP), human parainfluenza virus (HPIV), human rhinovirus (HRV), enterovirus (EV), respiratory syncytial virus (RSV), seasonal human coronavirus (HCoV), human metapneumovirus (HMPV), human adenovirus (HAdV), human bocavirus (HBoV) and chlamydia pneumoniae (CP), which changed to seasonal HCoV, followed by HRV, HPIV, IFV, RSV, EV, HBoV, HMPV, MP, HAdV and CP during the COVID-19 epidemic (Fig. 1C-F and Table S1-S3). SARS-CoV-2 was not detected. For children, the top five pathogens were MP, IFV, HPIV, EV and RSV before the COVID-19 epidemic, changing to HPIV, seasonal HCoV, HRV, RSV and IFV. For adults, the top five pathogens were IFV, MP, HRV, HPIV and seasonal HCoV before the COVID-19 epidemic, changing to seansonal HCoV, HRV, IFV HPIV and EV. All the other pathogens had distinct increases in proportions except for IFV. Before the COVID-19 epidemic, 12,058 (32.16%, 95% CI 31.69% to 32.64%) were positive for at least one pathogen, which significantly dropped to 10.97% (95% CI 10.03% to 11.96%) during the COVID-19 epidemic (P<0.001, Fig. 2A and Table S4). The positive rates of the top five pathogens were IFV (9.22%), MP (6.77%), HPIV (4.14%), HRV (3.29%) and EV (2.94%) before the COVID-19 epidemic and seasonal HCoV (2.42%), HRV (2.17%), HPIV (1.71%), IFV (1.50%) and RSV (1.23%) during the COVID-19 epidemic. A similar trend was observed in children (from 41.92% to 20.76%, P<0.001) and in adults (from 27.66% to 8.76%, P<0.001). Among all the pathogens, only seasonal HCoV had 20.74% increase in the positive rate, from 2.00% to 2.42% (P = 0.073). The other 10 pathogens had significant decreases in their positive rates (all P<0.05). IFV had the largest difference (−7.72%, 95% CI −8.19% to −7.25%) in the positive rate decreasing by 83.75% (Fig. 2B). In children, a significant increase in seasonal HCoV was observed from 1.74% to 3.29% (P = 0.002, Fig. 2A,C and Table S5). The positive rates of the top five pathogens were MP (9.37%), IFV (7.43%), HPIV (6.94%), EV (5.09%) and RSV (4.28%) before the COVID-19 epidemic and HPIV (5.26%), seasonal HCoV (3.29%), HRV (3.29%), RSV (3.15%) and IFV (1.97%) during the COVID-19 epidemic. The other nine pathogens showed decreased positive rates but significant for IFV, MP, EV, HMPV and HAdV (Fig. 2C). In adults, seasonal HCoV slightly increased during the COVID-19 epidemic (P = 0.710, Fig. 2A and Table S6). The positive rates of the other nine pathogens significantly decreased except for RSV. The positive rates of the top five pathogens were IFV (10.04%), MP (5.57%), HRV (2.89%), HPIV (2.85%) and seasonal HCoV (2.12%) before the COVID-19 epidemic and seasonal HCoV (2.22%), HRV (1.92%), IFV (1.39%), HPIV (0.92%) and EV (0.89%) during the COVID-19 epidemic. IFV had the largest difference in the positive rate, followed by MP and HPIV (Fig. 2D). After on 24/01/2020 in Beijing, the overall positive rates of all pathogens changed according to the implementation of different levels of PHER (Fig. 2E-P). The positive rates sharply decreased due to the outbreak of COVID-19 in the Xinfadi Market and in Shunyi District, Beijing. These results indicated the prevalence of pathogens was closely related to public health measures against COVID-19. Four groups were classified according to the dynamic trend of the positive rate of each pathogen. The positive rates of seasonal HCoV and HPIV were lower in the early stage of the COVID-19 epidemic and increased in the late stage, even exceeding the previous peak. For HRV, EV and HBoV, the positive rates returned to their previous levels in the late stage of the COVID-19 epidemic. The positive rates decreased to lower levels and remained until January 2021 for IFV, MP, HMPV, HAdV and CP. IFV was only detected in February and March 2020. COVID-19 had a relatively smaller effect on the positive rate of RSV compared to other pathogens. Public health measures against COVID-19 and people's daily behavior changed potentially affected the prevalence of other respiratory pathogens.2Zhang N. Jia W. Lei H. Wang P. Zhao P. Guo Y. et al.Effects of human behaviour changes during the COVID-19 pandemic on influenza spread in Hong Kong.Clin Infect Dis. 2020 Dec 4; (PubMed PMID: 33277643. Pubmed Central PMCID: PMC7799278. Epub 2020/12/06)Google Scholar, 3Soo R.J.J. Chiew C.J. Ma S. Pung R. Lee V. Decreased Influenza Incidence under COVID-19 Control Measures, Singapore.Emerg Infect Dis. Aug 2020; 26 (PubMed PMID: 32339092. Pubmed Central PMCID: PMC7392467. Epub 2020/04/28): 1933-1935Crossref PubMed Scopus (225) Google Scholar, 4Kuitunen I. Artama M. Makela L. Backman K. Heiskanen-Kosma T. Renko M. 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Disappearance of summer influenza in the Okinawa prefecture during the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic.Respir Investig. Jan 2021; 59 (PubMed PMID: 33246913. Pubmed Central PMCID: PMC7667393. Epub 2020/11/29): 149-152Crossref PubMed Scopus (18) Google Scholar The decrease of IFV is closely related to influenza vaccination as well as the public health measures. More influenza vaccinations may have effectively reduced the spread of IFV. The COVID-19 epidemic and the corresponding protective measures have changed people's medical behavior, with significant decreases in non-COVID-19 inpatient and outpatient visits. Seasonal HCoV became the first pathogen in ARTIs during the COVID-19 epidemic. Anton et al. reported that the detection rates of HCoV and HPIV increased after the H1N1 epidemic in Catalonia, Spain.7Anton A. Marcos M.A. Torner N. Isanta R. Camps M. 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J Med Virol. Feb 2011; 83 (PubMed PMID: 21181925. Pubmed Central PMCID: PMC7166607. Epub 2010/12/25): 291-297Crossref PubMed Scopus (43) Google Scholar Therefore, the incidence of seasonal HCoV may have peaked in 2020/2021, which may have been higher without no public measures for COVID-19. This suggests that we need to further strengthen the monitoring of HCoV in the future to prevent a co-epidemic of seasonal HCoV and SARS-CoV-2, especially when control measures for COVID-19 become normalized. In general, public health measures against COVID-19 substantially reduced the prevalence of other respiratory pathogens. IFV decreased from the first to the fourth during the COVID-19 epidemic. Seasonal HCoV, which became the first pathogen of ARTIs, should be strengthened to control to prevent co-circulation with SARS-CoV-2. These findings indicated the additional benefits of the public health measures implemented for COVID-19 in reducing the spread of other respiratory diseases. Notes The study was supported by the National Major Science and Technology Project for Control and Prevention of Major Infectious Diseases in China (2017ZX10103004). We thank all participants, including study volunteers enrolled in the study. We thank the staff of the 35 sentinel hospitals composed the Respiratory Pathogen Surveillance System in Beijing, who enrolled the study participants and the staff members of all district-level CDCs for their assistance on respiratory pathogen surveillance. Download .docx (.04 MB) Help with docx files