Molecular Epidemiology of Human Metapneumovirus in East Japan before and after COVID-19, 2017–2022
Human metapneumovirus (hMPV) is genetically classified into two major subgroups, A and B, based on attachment glycoprotein (G protein) gene sequences. The A2 subgroup is further separated into three subdivisions, A2a, A2b (A2b1), and A2c (A2b2). Subgroup A2c viruses carrying 180- or 111-nucleotide d...
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| Published in | Japanese Journal of Infectious Diseases Vol. 77; no. 3; pp. 137 - 143 |
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| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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Japan
National Institute of Infectious Diseases
31.05.2024
Japan Science and Technology Agency |
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| Online Access | Get full text |
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| Abstract | Human metapneumovirus (hMPV) is genetically classified into two major subgroups, A and B, based on attachment glycoprotein (G protein) gene sequences. The A2 subgroup is further separated into three subdivisions, A2a, A2b (A2b1), and A2c (A2b2). Subgroup A2c viruses carrying 180- or 111-nucleotide duplications in the G gene (A2c 180nt-dup or A2c 111nt-dup ) have been reported in Japan and Spain. The coronavirus disease 2019 (COVID-19) pandemic disrupted the epidemiological kinetics of other respiratory viruses, including hMPV. In this study, we analyzed the sequences of hMPV isolates in Tokyo and Fukushima obtained from 2017 to 2022, i.e., before and after the COVID-19 pandemic. Subgroup A hMPV strains were detected from 2017 to 2019, and most cases were A2c 111nt-dup, suggesting ongoing transmission of this clade, consistent with global transmission dynamics. Subgroup B viruses, but not subgroup A viruses, were detected in 2022 after the COVID-19 peak. Phylogenetic analysis showed that the subgroup B viruses were closely related to strains detected in Yokohama from 2013 to 2016, and strains detected in Fukushima in 2019, suggesting the reappearance of local endemic viruses in East Japan. |
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| AbstractList | Human metapneumovirus (hMPV) is genetically classified into two major subgroups, A and B, based on attachment glycoprotein (G protein) gene sequences. The A2 subgroup is further separated into three subdivisions, A2a, A2b (A2b1), and A2c (A2b2). Subgroup A2c viruses carrying 180- or 111-nucleotide duplications in the G gene (A2c 180nt-dup or A2c 111nt-dup ) have been reported in Japan and Spain. The coronavirus disease 2019 (COVID-19) pandemic disrupted the epidemiological kinetics of other respiratory viruses, including hMPV. In this study, we analyzed the sequences of hMPV isolates in Tokyo and Fukushima obtained from 2017 to 2022, i.e., before and after the COVID-19 pandemic. Subgroup A hMPV strains were detected from 2017 to 2019, and most cases were A2c 111nt-dup, suggesting ongoing transmission of this clade, consistent with global transmission dynamics. Subgroup B viruses, but not subgroup A viruses, were detected in 2022 after the COVID-19 peak. Phylogenetic analysis showed that the subgroup B viruses were closely related to strains detected in Yokohama from 2013 to 2016, and strains detected in Fukushima in 2019, suggesting the reappearance of local endemic viruses in East Japan. Human metapneumovirus (hMPV) is genetically classified into two major subgroups, A and B, based on attachment glycoprotein (G protein) gene sequences. The A2 subgroup is further separated into three subdivisions, A2a, A2b (A2b1), and A2c (A2b2). Subgroup A2c viruses carrying 180- or 111-nucleotide duplications in the G gene (A2c or A2c ) have been reported in Japan and Spain. The coronavirus disease 2019 (COVID-19) pandemic disrupted the epidemiological kinetics of other respiratory viruses, including hMPV. In this study, we analyzed the sequences of hMPV isolates in Tokyo and Fukushima obtained from 2017 to 2022, i.e., before and after the COVID-19 pandemic. Subgroup A hMPV strains were detected from 2017 to 2019, and most cases were A2c , suggesting ongoing transmission of this clade, consistent with global transmission dynamics. Subgroup B viruses, but not subgroup A viruses, were detected in 2022 after the COVID-19 peak. Phylogenetic analysis showed that the subgroup B viruses were closely related to strains detected in Yokohama from 2013 to 2016, and strains detected in Fukushima in 2019, suggesting the reappearance of local endemic viruses in East Japan. Human metapneumovirus (hMPV) is genetically classified into two major subgroups, A and B, based on attachment glycoprotein (G protein) gene sequences. The A2 subgroup is further separated into three subdivisions, A2a, A2b (A2b1), and A2c (A2b2). Subgroup A2c viruses carrying 180- or 111-nucleotide duplications in the G gene (A2c 180nt-dup or A2c 111nt-dup ) have been reported in Japan and Spain. The coronavirus disease 2019 (COVID-19) pandemic disrupted the epidemiological kinetics of other respiratory viruses, including hMPV. In this study, we analyzed the sequences of hMPV isolates in Tokyo and Fukushima obtained from 2017 to 2022, i.e., before and after the COVID-19 pandemic. Subgroup A hMPV strains were detected from 2017 to 2019, and most cases were A2c 111nt-dup, suggesting ongoing transmission of this clade, consistent with global transmission dynamics. Subgroup B viruses, but not subgroup A viruses, were detected in 2022 after the COVID-19 peak. Phylogenetic analysis showed that the subgroup B viruses were closely related to strains detected in Yokohama from 2013 to 2016, and strains detected in Fukushima in 2019, suggesting the reappearance of local endemic viruses in East Japan.Human metapneumovirus (hMPV) is genetically classified into two major subgroups, A and B, based on attachment glycoprotein (G protein) gene sequences. The A2 subgroup is further separated into three subdivisions, A2a, A2b (A2b1), and A2c (A2b2). Subgroup A2c viruses carrying 180- or 111-nucleotide duplications in the G gene (A2c 180nt-dup or A2c 111nt-dup ) have been reported in Japan and Spain. The coronavirus disease 2019 (COVID-19) pandemic disrupted the epidemiological kinetics of other respiratory viruses, including hMPV. In this study, we analyzed the sequences of hMPV isolates in Tokyo and Fukushima obtained from 2017 to 2022, i.e., before and after the COVID-19 pandemic. Subgroup A hMPV strains were detected from 2017 to 2019, and most cases were A2c 111nt-dup, suggesting ongoing transmission of this clade, consistent with global transmission dynamics. Subgroup B viruses, but not subgroup A viruses, were detected in 2022 after the COVID-19 peak. Phylogenetic analysis showed that the subgroup B viruses were closely related to strains detected in Yokohama from 2013 to 2016, and strains detected in Fukushima in 2019, suggesting the reappearance of local endemic viruses in East Japan. |
| ArticleNumber | JJID.2023.350 |
| Author | Suwa, Reiko Kawase, Miyuki Takeda, Makoto Suzuki, Shigeo Hosoya, Mitsuaki Nao, Naganori Kume, Yohei Shirato, Kazuya Hashimoto, Koichi Norito, Sakurako Sugimoto, Satoko Ono, Takashi Sato, Masatoki Chishiki, Mina Sakuma, Hiroko Okabe, Hisao |
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| Cites_doi | 10.1016/j.jcv.2020.104590 10.1111/1348-0421.12543 10.1016/j.virs.2022.08.007 10.1371/journal.pcbi.1007046 10.3201/eid1004.030393 10.1056/NEJMoa025472 10.1093/infdis/jis309 10.1371/journal.pone.0215822 10.1128/mra.01027-21 10.1128/spectrum.01920-23 10.1371/journal.pone.0017427 10.3390/microorganisms8091280 10.1016/j.virol.2017.11.012 10.1128/mra.00411-22 10.1111/irv.12995 10.1016/j.jiac.2022.03.001 10.1038/s41598-020-70090-2 10.3201/eid2701.201043 10.1016/j.jcv.2016.06.006 10.1128/mbio.02280-22 10.1111/1348-0421.12542 10.7883/yoken.JJID.2019.124 10.3390/pathogens11070754 10.2217/fmb-2016-0211 10.3389/fmicb.2017.00402 10.1038/89098 10.1016/j.jinf.2023.05.004 |
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| References | 10. Pinana M, Vila J, Gimferrer L, et al. Novel human metapneumovirus with a 180-nucleotide duplication in the G gene. Future Microbiol. 2017;12:565-571. 12. Saikusa M, Nao N, Kawakami C, et al. Predominant detection of the subgroup A2b human metapneumovirus strain with a 111-nucleotide duplication in the G gene in Yokohama City, Japan in 2018. Jpn J Infect Dis. 2019;72:350-352. 3. Widmer K, Zhu Y, Williams JV, et al. Rates of hospitalizations for respiratory syncytial virus, human metapneumovirus, and influenza virus in older adults. J Infect Dis. 2012;206:56-62. 13. Pinana M, Gonzalez-Sanchez A, Andres C, et al. The emergence, impact, and evolution of human metapneumovirus variants from 2014 to 2021 in Spain. J Infect. 2023;87:103-110. 22. Kakizaki M, Kume Y, Suwa R, et al. Thirteen nearly complete genome sequences of human bocavirus 1 isolated from pediatric inpatients in Fukushima, Japan. Microbiol Resour Announc. 2022;11:e0102721. 20. Takayama I, Semba S, Yokono K, et al. Clinical evaluation of fully automated molecular diagnostic system "Simprova" for influenza virus, respiratory syncytial virus, and human metapneumovirus. Sci Rep. 2020;10:13496. 21. Sugimoto S, Kume Y, Suwa R, et al. Ten nearly complete genome sequences of human orthorubulavirus 4 isolated from pediatric inpatients in Fukushima, Japan. Microbiol Resour Announc. 2022;11:e0041122. 1. van den Hoogen BG, de Jong JC, Groen J, et al. A newly discovered human pneumovirus isolated from young children with respiratory tract disease. Nat Med. 2001;7:719-724. 7. Nao N, Saikusa M, Sato K, et al. Recent molecular evolution of human metapneumovirus (HMPV): subdivision of HMPV A2b strains. Microorganisms. 2020;8:1280. 14. Zhao H, Feng Q, Feng Z, et al. Clinical characteristics and molecular epidemiology of human metapneumovirus in children with acute lower respiratory tract infections in China, 2017 to 2019: a multicentre prospective observational study. Virol Sin. 2022;37:874-882. 8. Saikusa M, Kawakami C, Nao N, et al. 180-nucleotide duplication in the G gene of human metapneumovirus A2b subgroup strains circulating in Yokohama City, Japan, since 2014. Front Microbiol. 2017;8:402. 5. Gaunt ER, Jansen RR, Poovorawan Y, et al. Molecular epidemiology and evolution of human respiratory syncytial virus and human metapneumovirus. PLoS One. 2011;6:e17427. 2. Williams J V, Harris PA, Tollefson SJ, et al. Human metapneumovirus and lower respiratory tract disease in otherwise healthy infants and children. N Engl J Med. 2004;350:443-450. 27. Xie Z, Xu J, Ren Y, et al. Emerging human metapneumovirus gene duplication variants in patients with severe acute respiratory infection, China, 2017–2019. Emerg Infect Dis. 2021;27:275-277. 17. Suwa R, Kume Y, Kawase M, et al. Practical validation of United States Centers for Disease Control and Prevention assays for the detection of human respiratory syncytial virus in pediatric inpatients in Japan. Pathogens. 2022;11:754. 23. Kawase M, Suwa R, Sugimoto S, et al. Evidence of the simultaneous replications of active viruses in specimens positive for multiple respiratory viruses. Microbiol Spectr. 2024;12:e0192023. 18. Kume Y, Hashimoto K, Chishiki M, et al. Changes in virus detection in hospitalized children before and after the severe acute respiratory syndrome coronavirus 2 pandemic. Influenza Other Respir Viruses. 2022;16:837-841. 16. Kume Y, Hashimoto K, Shirato K, et al. Epidemiological and clinical characteristics of infections with seasonal human coronavirus and respiratory syncytial virus in hospitalized children immediately before the coronavirus disease 2019 pandemic. J Infect Chemother. 2022;28:859-865. 6. van den Hoogen BG, Herfst S, Sprong L, et al. Antigenic and genetic variability of human metapneumoviruses. Emerg Infect Dis. 2004;10:658-666. 26. Miura S, Tamura K, Tao Q, et al. A new method for inferring timetrees from temporally sampled molecular sequences. PLoS Comput Biol. 2020;16:e1007046. 28. Pinana M, Vila J, Maldonado C, et al. Insights into immune evasion of human metapneumovirus: novel 180- and 111-nucleotide duplications within viral G gene throughout 2014–2017 seasons in Barcelona, Spain. J Clin Virol. 2020;132:104590. 9. Saikusa M, Nao N, Kawakami C, et al. A novel 111-nucleotide duplication in the G gene of human metapneumovirus. Microbiol Immunol. 2017;61:507-512. 11. Groen K, van Nieuwkoop S, Meijer A, et al. Emergence and potential extinction of genetic lineages of human metapneumovirus between 2005 and 2021. mBio. 2023;14:e0228022. 4. Scheuerman O, Barkai G, Mandelboim M, et al. Human metapneumovirus (hMPV) infection in immunocompromised children. J Clin Virol. 2016;83:12-16. 24. Nao N, Sato K, Yamagishi J, et al. Consensus and variations in cell line specificity among human metapneumovirus strains. PLoS One. 2019;14:e0215822. 15. Kume Y, Hashimoto K, Chishiki M, et al. Changes in virus detection in hospitalized children before and after the severe acute respiratory syndrome coronavirus 2 pandemic. Influenza Other Respir Viruses. 2022;16:837-841. 25. Sato K, Watanabe O, Ohmiya S, et al. Efficient isolation of human metapneumovirus using MNT-1, a human malignant melanoma cell line with early and distinct cytopathic effects. Microbiol Immunol. 2017;61:497-506. 19. Shirato K, Kawase M, Matsuyama S. Wild-type human coronaviruses prefer cell-surface TMPRSS2 to endosomal cathepsins for cell entry. Virology. 2018;517:9-15. 22 23 24 25 26 27 28 10 11 12 13 14 15 16 17 18 19 1 2 3 4 5 6 7 8 9 20 21 |
| References_xml | – reference: 20. Takayama I, Semba S, Yokono K, et al. Clinical evaluation of fully automated molecular diagnostic system "Simprova" for influenza virus, respiratory syncytial virus, and human metapneumovirus. Sci Rep. 2020;10:13496. – reference: 3. Widmer K, Zhu Y, Williams JV, et al. Rates of hospitalizations for respiratory syncytial virus, human metapneumovirus, and influenza virus in older adults. J Infect Dis. 2012;206:56-62. – reference: 15. Kume Y, Hashimoto K, Chishiki M, et al. Changes in virus detection in hospitalized children before and after the severe acute respiratory syndrome coronavirus 2 pandemic. Influenza Other Respir Viruses. 2022;16:837-841. – reference: 5. Gaunt ER, Jansen RR, Poovorawan Y, et al. Molecular epidemiology and evolution of human respiratory syncytial virus and human metapneumovirus. PLoS One. 2011;6:e17427. – reference: 28. Pinana M, Vila J, Maldonado C, et al. Insights into immune evasion of human metapneumovirus: novel 180- and 111-nucleotide duplications within viral G gene throughout 2014–2017 seasons in Barcelona, Spain. J Clin Virol. 2020;132:104590. – reference: 16. Kume Y, Hashimoto K, Shirato K, et al. Epidemiological and clinical characteristics of infections with seasonal human coronavirus and respiratory syncytial virus in hospitalized children immediately before the coronavirus disease 2019 pandemic. J Infect Chemother. 2022;28:859-865. – reference: 8. Saikusa M, Kawakami C, Nao N, et al. 180-nucleotide duplication in the G gene of human metapneumovirus A2b subgroup strains circulating in Yokohama City, Japan, since 2014. Front Microbiol. 2017;8:402. – reference: 2. Williams J V, Harris PA, Tollefson SJ, et al. Human metapneumovirus and lower respiratory tract disease in otherwise healthy infants and children. N Engl J Med. 2004;350:443-450. – reference: 13. Pinana M, Gonzalez-Sanchez A, Andres C, et al. The emergence, impact, and evolution of human metapneumovirus variants from 2014 to 2021 in Spain. J Infect. 2023;87:103-110. – reference: 17. Suwa R, Kume Y, Kawase M, et al. Practical validation of United States Centers for Disease Control and Prevention assays for the detection of human respiratory syncytial virus in pediatric inpatients in Japan. Pathogens. 2022;11:754. – reference: 25. Sato K, Watanabe O, Ohmiya S, et al. Efficient isolation of human metapneumovirus using MNT-1, a human malignant melanoma cell line with early and distinct cytopathic effects. Microbiol Immunol. 2017;61:497-506. – reference: 6. van den Hoogen BG, Herfst S, Sprong L, et al. Antigenic and genetic variability of human metapneumoviruses. Emerg Infect Dis. 2004;10:658-666. – reference: 23. Kawase M, Suwa R, Sugimoto S, et al. Evidence of the simultaneous replications of active viruses in specimens positive for multiple respiratory viruses. Microbiol Spectr. 2024;12:e0192023. – reference: 12. Saikusa M, Nao N, Kawakami C, et al. Predominant detection of the subgroup A2b human metapneumovirus strain with a 111-nucleotide duplication in the G gene in Yokohama City, Japan in 2018. Jpn J Infect Dis. 2019;72:350-352. – reference: 10. Pinana M, Vila J, Gimferrer L, et al. Novel human metapneumovirus with a 180-nucleotide duplication in the G gene. Future Microbiol. 2017;12:565-571. – reference: 7. Nao N, Saikusa M, Sato K, et al. Recent molecular evolution of human metapneumovirus (HMPV): subdivision of HMPV A2b strains. Microorganisms. 2020;8:1280. – reference: 22. Kakizaki M, Kume Y, Suwa R, et al. Thirteen nearly complete genome sequences of human bocavirus 1 isolated from pediatric inpatients in Fukushima, Japan. Microbiol Resour Announc. 2022;11:e0102721. – reference: 21. Sugimoto S, Kume Y, Suwa R, et al. Ten nearly complete genome sequences of human orthorubulavirus 4 isolated from pediatric inpatients in Fukushima, Japan. 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Consensus and variations in cell line specificity among human metapneumovirus strains. PLoS One. 2019;14:e0215822. – reference: 19. Shirato K, Kawase M, Matsuyama S. Wild-type human coronaviruses prefer cell-surface TMPRSS2 to endosomal cathepsins for cell entry. Virology. 2018;517:9-15. – reference: 9. Saikusa M, Nao N, Kawakami C, et al. A novel 111-nucleotide duplication in the G gene of human metapneumovirus. Microbiol Immunol. 2017;61:507-512. – reference: 11. Groen K, van Nieuwkoop S, Meijer A, et al. Emergence and potential extinction of genetic lineages of human metapneumovirus between 2005 and 2021. mBio. 2023;14:e0228022. – reference: 1. van den Hoogen BG, de Jong JC, Groen J, et al. A newly discovered human pneumovirus isolated from young children with respiratory tract disease. Nat Med. 2001;7:719-724. – reference: 26. Miura S, Tamura K, Tao Q, et al. A new method for inferring timetrees from temporally sampled molecular sequences. 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| SubjectTerms | Child Child, Preschool Coronaviruses COVID-19 COVID-19 - epidemiology COVID-19 - transmission COVID-19 - virology Disease transmission Epidemiology Gene sequencing Glycoproteins human metapneumovirus Humans Infant Japan - epidemiology Metapneumovirus - classification Metapneumovirus - genetics Metapneumovirus - isolation & purification Molecular Epidemiology Nucleotides Pandemics Paramyxoviridae Infections - epidemiology Paramyxoviridae Infections - virology phylogenetic analysis Phylogeny SARS-CoV-2 - classification SARS-CoV-2 - genetics Subdivisions subgroup Subgroups Viral diseases Viruses |
| Title | Molecular Epidemiology of Human Metapneumovirus in East Japan before and after COVID-19, 2017–2022 |
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