{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,8]],"date-time":"2026-09-08T14:26:06Z","timestamp":1788877566619,"version":"build-2803163510"},"reference-count":112,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2024,6,13]],"date-time":"2024-06-13T00:00:00Z","timestamp":1718236800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"the Ministry of Education and Science, Bulgaria","award":["K\u041f-06-H73\/7-05.12.2023"],"award-info":[{"award-number":["K\u041f-06-H73\/7-05.12.2023"]}]},{"name":"the Ministry of Education and Science, Bulgaria","award":["K\u041f-06-H43\/5-30.11.2020"],"award-info":[{"award-number":["K\u041f-06-H43\/5-30.11.2020"]}]},{"name":"the Ministry of Education and Science, Bulgaria","award":["K\u041f-06-H43\/1-27.11.2020"],"award-info":[{"award-number":["K\u041f-06-H43\/1-27.11.2020"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>This study aimed to determine the incidence and etiological, seasonal, and genetic characteristics of respiratory viral coinfections involving severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Between October 2020 and January 2024, nasopharyngeal samples were collected from 2277 SARS-CoV-2-positive patients. Two multiplex approaches were used to detect and sequence SARS-CoV-2, influenza A\/B viruses, and other seasonal respiratory viruses: multiplex real-time polymerase chain reaction (PCR) and multiplex next-generation sequencing. Coinfections of SARS-CoV-2 with other respiratory viruses were detected in 164 (7.2%) patients. The most common co-infecting virus was respiratory syncytial virus (RSV) (38 cases, 1.7%), followed by bocavirus (BoV) (1.2%) and rhinovirus (RV) (1.1%). Patients \u2264 16 years of age had the highest rate (15%) of mixed infections. Whole-genome sequencing produced 19 complete genomes of seasonal respiratory viral co-pathogens, which were subjected to phylogenetic and amino acid analyses. The detected influenza viruses were classified into the genetic groups 6B.1A.5a.2a and 6B.1A.5a.2a.1 for A(H1N1)pdm09, 3C.2a1b.2a.2a.1 and 3C.2a.2b for A(H3N2), and V1A.3a.2 for the B\/Victoria lineage. The RSV-B sequences belonged to the genetic group GB5.0.5a, with HAdV-C belonging to type 1, BoV to genotype VP1, and PIV3 to lineage 1a(i). Multiple amino acid substitutions were identified, including at the antibody-binding sites. This study provides insights into respiratory viral coinfections involving SARS-CoV-2 and reinforces the importance of genetic characterization of co-pathogens in the development of therapeutic and preventive strategies.<\/jats:p>","DOI":"10.3390\/v16060958","type":"journal-article","created":{"date-parts":[[2024,6,14]],"date-time":"2024-06-14T10:42:34Z","timestamp":1718361754000},"page":"958","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Epidemiological and Genetic Characteristics of Respiratory Viral Coinfections with Different Variants of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2)"],"prefix":"10.3390","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4543-6831","authenticated-orcid":false,"given":"Ivelina","family":"Trifonova","sequence":"first","affiliation":[{"name":"Department of Virology, National Centre of Infectious and Parasitic Diseases, 1233 Sofia, Bulgaria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3188-2283","authenticated-orcid":false,"given":"Neli","family":"Korsun","sequence":"additional","affiliation":[{"name":"Department of Virology, National Centre of Infectious and Parasitic Diseases, 1233 Sofia, Bulgaria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Iveta","family":"Madzharova","sequence":"additional","affiliation":[{"name":"Department of Virology, National Centre of Infectious and Parasitic Diseases, 1233 Sofia, Bulgaria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3186-1124","authenticated-orcid":false,"given":"Ivailo","family":"Alexiev","sequence":"additional","affiliation":[{"name":"Department of Virology, National Centre of Infectious and Parasitic Diseases, 1233 Sofia, Bulgaria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2616-894X","authenticated-orcid":false,"given":"Ivan","family":"Ivanov","sequence":"additional","affiliation":[{"name":"Department of Microbiology, National Centre of Infectious and Parasitic Diseases, 1504 Sofia, Bulgaria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Viktoria","family":"Levterova","sequence":"additional","affiliation":[{"name":"Department of Microbiology, National Centre of Infectious and Parasitic Diseases, 1504 Sofia, Bulgaria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8563-5520","authenticated-orcid":false,"given":"Lyubomira","family":"Grigorova","sequence":"additional","affiliation":[{"name":"Department of Virology, National Centre of Infectious and Parasitic Diseases, 1233 Sofia, Bulgaria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9924-8553","authenticated-orcid":false,"given":"Ivan","family":"Stoikov","sequence":"additional","affiliation":[{"name":"Department of Microbiology, National Centre of Infectious and Parasitic Diseases, 1504 Sofia, Bulgaria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7447-7627","authenticated-orcid":false,"given":"Dean","family":"Donchev","sequence":"additional","affiliation":[{"name":"Department of Microbiology, National Centre of Infectious and Parasitic Diseases, 1504 Sofia, Bulgaria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7878-3995","authenticated-orcid":false,"given":"Iva","family":"Christova","sequence":"additional","affiliation":[{"name":"Department of Virology, National Centre of Infectious and Parasitic Diseases, 1233 Sofia, Bulgaria"},{"name":"Department of Microbiology, National Centre of Infectious and Parasitic Diseases, 1504 Sofia, Bulgaria"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,6,13]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Li, P., Zhang, Y., Shen, W., Shi, S., and Zhao, Z. (2022). dbGSRV: A manually curated database of genetic susceptibility to respiratory virus. PLoS ONE, 17.","DOI":"10.1371\/journal.pone.0262373"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1324","DOI":"10.3201\/eid2606.200299","article-title":"Co-infection with SARS-CoV-2 and Influenza A Virus in Patient with Pneumonia, China","volume":"26","author":"Wu","year":"2020","journal-title":"Emerg. Infect. Dis."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"e84","DOI":"10.1016\/S0140-6736(20)31052-7","article-title":"SARS-CoV-2 and influenza virus co-infection","volume":"395","author":"Bodro","year":"2020","journal-title":"Lancet"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Maltezou, H.C., Papanikolopoulou, A., Vassiliu, S., Theodoridou, K., Nikolopoulou, G., and Sipsas, N.V. (2023). COVID-19 and Respiratory Virus Co-Infections: A Systematic Review of the Literature. Viruses, 15.","DOI":"10.3390\/v15040865"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"899","DOI":"10.1001\/jama.2021.14131","article-title":"Influenza\u2019s Unprecedented Low Profile During COVID-19 Pandemic Leaves Experts Wondering What This Flu Season Has in Store","volume":"326","author":"Rubin","year":"2021","journal-title":"JAMA"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1001","DOI":"10.1038\/s41467-021-21157-9","article-title":"Impact of the COVID-19 nonpharmaceutical interventions on influenza and other respiratory viral infections in New Zealand","volume":"12","author":"Huang","year":"2021","journal-title":"Nat. Commun."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"102262","DOI":"10.1016\/j.tmaid.2022.102262","article-title":"COVID-19 and Influenza coinfection: The rise of \u00d4micron and H3N2 in Brazil\u20142022","volume":"46","author":"Fujita","year":"2022","journal-title":"Travel. Med. Infect. Dis."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Principi, N., Autore, G., Ramundo, G., and Esposito, S. (2023). Epidemiology of Respiratory Infections during the COVID-19 Pandemic. Viruses, 15.","DOI":"10.3390\/v15051160"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"6078","DOI":"10.1016\/j.vaccine.2020.07.058","article-title":"Influenza immunization and COVID-19","volume":"38","author":"Maltezou","year":"2020","journal-title":"Vaccine"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Khasawneh, A.I., Himsawi, N.M., Abu-Raideh, J.A., Sammour, A., Abu Safieh, H., Obeidat, A., Azab, M., Tarifi, A.A., Al Khawaldeh, A., and Al-Momani, H. (2023). Prevalence of SARS-CoV-2 and other respiratory pathogens among a Jordanian subpopulation during Delta-to-Omicron transition: Winter 2021\/2022. PLoS ONE, 18.","DOI":"10.1371\/journal.pone.0283804"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"e0187321","DOI":"10.1128\/jvi.01873-21","article-title":"Coinfection with SARS-CoV-2 and Influenza A Virus Increases Disease Severity and Impairs Neutralizing Antibody and CD4+ T Cell Responses","volume":"96","author":"Kim","year":"2022","journal-title":"J. Virol."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Bordi, L., Vulcano, A., Sberna, G., Nonis, M., Giacomini, P., Maggi, F., Fontana, C., and Lalle, E. (2023). Co-Circulation of SARS-CoV-2 and Other Respiratory Pathogens in Upper and Lower Respiratory Tracts during Influenza Season 2022\u20132023 in Lazio Region. Microorganisms, 11.","DOI":"10.3390\/microorganisms11092239"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1016\/j.jinf.2020.05.046","article-title":"Co-infections in people with COVID-19: A systematic review and meta-analysis","volume":"81","author":"Lansbury","year":"2020","journal-title":"J. Infect."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1111\/irv.12853","article-title":"Viral epidemiology and SARS-CoV-2 co-infections with other respiratory viruses during the first COVID-19 wave in Paris. France","volume":"15","author":"Bouzid","year":"2021","journal-title":"Influenza Other Respir. Viruses"},{"key":"ref_15","first-page":"e36215","article-title":"Incidence of SARS-CoV-2 Co-infections During the Second Wave in Sub-Himalayan Region. India","volume":"15","author":"Gupta","year":"2023","journal-title":"Cureus"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1699","DOI":"10.1002\/jmv.25953","article-title":"Coinfection in SARS-CoV-2 infected patients: Where are influenza virus and rhinovirus\/enterovirus?","volume":"92","author":"Nowak","year":"2020","journal-title":"J. Med. Virol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1186\/s41479-021-00083-w","article-title":"The role of co-infections and secondary infections in patients with COVID-19","volume":"13","author":"Feldman","year":"2021","journal-title":"Pneumonia"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1016\/j.jped.2022.03.003","article-title":"Rhinovirus as the main co-circulating virus during the COVID-19 pandemic in children","volume":"98","author":"Varela","year":"2022","journal-title":"J. Pediatr."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Di Lorenzo, A., Campogiani, L., Iannetta, M., Iannazzo, R., Imeneo, A., Alessio, G., D\u2019Aquila, V., Massa, B., Fato, I., and Rindi, L.V. (2023). The Impact of Viral and Bacterial Co-Infections and Home Antibiotic Treatment in SARS-CoV-2 Hospitalized Patients at the Policlinico Tor Vergata Hospital. Rome. Italy. Antibiotics, 12.","DOI":"10.3390\/antibiotics12091348"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Trifonova, I., Christova, I., Madzharova, I., Angelova, S., Voleva, S., Yordanova, R., Tcherveniakova, T., Krumova, S., and Korsun, N. (2022). Clinical significance and role of coinfections with respiratory pathogens among individuals with confirmed severe acute respiratory syndrome coronavirus-2 infection. Front. Public Health, 10.","DOI":"10.3389\/fpubh.2022.959319"},{"key":"ref_21","unstructured":"Sheehan, N.P., Leonelli, S., and Botta, F. (2023). From Collection to Analysis: A Comparison of GISAID and the COVID-19 Data Portal. bioRxiv."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"282","DOI":"10.1016\/j.ijid.2020.11.190","article-title":"Evolution and genetic diversity of SARS-CoV-2 in Africa using whole genome sequences","volume":"103","author":"Motayo","year":"2021","journal-title":"Int. J. Infect. Dis."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Yu, C.Y., Wong, S.Y., Liew, N.W.C., Joseph, N., Zakaria, Z., Nurulfiza, I., Soe, H.J., Kairon, R., Amin-Nordin, S., and Chee, H.Y. (2022). Whole genome sequencing analysis of SARS-CoV-2 from Malaysia: From alpha to Omicron. Front. Med., 9.","DOI":"10.3389\/fmed.2022.1001022"},{"key":"ref_24","unstructured":"Public Health England (2024, June 10). SARS-CoV-2 Variants of Concern and Variants under Investigation in England, Available online: https:\/\/assets.publishing.service.gov.uk\/government\/uploads\/system\/uploads\/attachment_data\/file\/984274\/Variants_of_Concern_VOC_Technical_Briefing_10_England.pdf."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"e056636","DOI":"10.1136\/bmjopen-2021-056636","article-title":"Growth, reproduction numbers and factors affecting the spread of SARS-CoV-2 novel variants of concern in the UK from October 2020 to July 2021: A modelling analysis","volume":"11","author":"Ward","year":"2021","journal-title":"BMJ Open"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"e2391","DOI":"10.1002\/rmv.2391","article-title":"Update on the omicron sub-variants BA.4 and BA.5","volume":"33","author":"Tallei","year":"2023","journal-title":"Rev. Med. Virol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"E127","DOI":"10.1503\/cmaj.1096034","article-title":"What to know about Omicron XBB.1.5","volume":"195","author":"Vogel","year":"2023","journal-title":"CMAJ"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1016\/j.cell.2022.12.018","article-title":"Alarming antibody evasion properties of rising SARS-CoV-2 BQ and XBB subvariants","volume":"186","author":"Wang","year":"2023","journal-title":"Cell"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1074","DOI":"10.1136\/bmj.p1074","article-title":"What do we know about the Arcturus XBB.1.16 subvariant?","volume":"381","author":"Looi","year":"2023","journal-title":"BMJ"},{"key":"ref_30","first-page":"e939580","article-title":"Editorial: The XBB.1.5 (\u2018Kraken\u2019) Subvariant of Omicron SARS-CoV-2 and its Rapid Global Spread","volume":"29","author":"Parums","year":"2023","journal-title":"Med. Sci. Monit."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1007\/s00705-023-05717-6","article-title":"A multiplex-NGS approach to identifying respiratory RNA viruses during the COVID-19 pandemic","volume":"168","author":"Ramos","year":"2023","journal-title":"Arch. Virol."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Tsibane, T., Ekiert, D.C., Krause, J.C., Martinez, O., Crowe, J.E., Wilson, I.A., and Basler, C.F. (2012). Influenza human monoclonal antibody 1F1 interacts with three major antigenic sites and residues mediating human receptor specificity in H1N1 viruses. PLoS Pathog., 8.","DOI":"10.1371\/journal.ppat.1003067"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/j.virol.2009.06.028","article-title":"The hemagglutinin structure of an avian H1N1 influenza A virus","volume":"392","author":"Lin","year":"2009","journal-title":"Virology"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/j.ijid.2020.10.040","article-title":"Co-infection of SARS-CoV-2 with other respiratory viruses and performance of lower respiratory tract samples for the diagnosis of COVID-19","volume":"102","author":"Burrel","year":"2021","journal-title":"Int. J. Infect. Dis."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Morales-Jad\u00e1n, D., Muslin, C., Viteri-D\u00e1vila, C., Coronel, B., Castro-Rodr\u00edguez, B., Vallejo-Janeta, A.P., Henr\u00edquez-Trujillo, A.R., Garcia-Bereguiain, M.A., and Rivera-Olivero, I.A. (2023). Coinfection of SARS-CoV-2 with other respiratory pathogens in outpatients from Ecuador. Front. Public Health, 11.","DOI":"10.3389\/fpubh.2023.1264632"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"e13131","DOI":"10.1111\/irv.13131","article-title":"Viral co-infection with human respiratory syncytial virus in suspected acute and severe respiratory tract infections during COVID-19 pandemic in Yaound\u00e9, Cameroon, 2020\u20132021","volume":"17","author":"Monamele","year":"2023","journal-title":"Influenza Other Respir. Viruses"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Pucarelli-Lebreiro, G., Venceslau, M.T., Cordeiro, C.C., Maciel, F.Q., Anachoreta, T.D., de Abreu, T.F., Frota, A.C.C., Casti\u00f1eiras, T.M.P.P., da Costa, A.M., and Lopes, A.C.D.L. (2022). Clinical Manifestations and Complications of Children with COVID-19 Compared to Other Respiratory Viral Infections: A Cohort Inpatient Study from Rio de Janeiro, Brazil. Front. Pediatr., 10.","DOI":"10.3389\/fped.2022.934648"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Nunziata, F., Salomone, S., Catzola, A., Poeta, M., Pagano, F., Punzi, L., Lo Vecchio, A., Guarino, A., and Bruzzese, E. (2023). Clinical Presentation and Severity of SARS-CoV-2 Infection Compared to Respiratory Syncytial Virus and Other Viral Respiratory Infections in Children Less than Two Years of Age. Viruses, 15.","DOI":"10.3390\/v15030717"},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Samal, J., Agarwal, R., Soni, A., Pandey, A., Thapar, S., and Gupta, E. (2022). Co-infection of SARS-CoV-2 with other respiratory pathogens in patients with liver disease. Access Microbiol., 4.","DOI":"10.1099\/acmi.0.000456"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"6781","DOI":"10.2147\/IDR.S435143","article-title":"High Prevalence of Respiratory Co-Infections and Risk Factors in COVID-19 Patients at Hospital Admission During an Epidemic Peak in China","volume":"16","author":"Zhu","year":"2023","journal-title":"Infect. Drug Resist."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"143","DOI":"10.5144\/0256-4947.2023.143","article-title":"Impact of non-pharmaceutical interventions on circulating respiratory viruses during the COVID-19 pandemic in Turkey","volume":"43","author":"Gozalan","year":"2023","journal-title":"Ann. Saudi Med."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"ofab618","DOI":"10.1093\/ofid\/ofab618","article-title":"Circulation of Non-SARS-CoV-2 Respiratory Pathogens and Coinfection with SARS-CoV-2 Amid the COVID-19 Pandemic","volume":"9","author":"Uhteg","year":"2021","journal-title":"Open Forum Infect. Dis."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Zeng, Z., Guan, W., Liu, Y., Lin, Z., Liang, W., Liang, J., Chen, B., Wu, T., Wang, Y., and Yang, C. (2022). Different Circulation Pattern of Multiple Respiratory Viruses in Southern China During the COVID-19 Pandemic. Front. Microbiol., 12.","DOI":"10.3389\/fmicb.2021.801946"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"e28489","DOI":"10.1002\/jmv.28489","article-title":"Low prevalence of influenza viruses and predominance of A(H3N2) virus with respect to SARS-CoV-2 during the 2021\u20132022 season in Bulgaria","volume":"95","author":"Korsun","year":"2023","journal-title":"J. Med. Virol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1070","DOI":"10.1016\/j.ajic.2022.05.009","article-title":"Viral transmissibility of SARS-CoV-2 accelerates in the winter, similarly to influenza epidemics","volume":"50","author":"Inaida","year":"2022","journal-title":"Am. J. Infect. Control"},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Nichols, G.L., Gillingham, E.L., Macintyre, H.L., Vardoulakis, S., Hajat, S., Sarran, C.E., Amankwaah, D., and Phalkey, R. (2021). Coronavirus seasonality, respiratory infections and weather. BMC Infect. Dis., 21.","DOI":"10.1186\/s12879-021-06785-2"},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Korsun, N., Trifonova, I., Madzharova, I., Alexiev, I., Uzunova, I., Ivanov, I., Velikov, P., Tcherveniakova, T., and Christova, I. (2024). Resurgence of respiratory syncytial virus with dominance of RSV-B during the 2022\u20132023 season. Front. Microbiol., 15.","DOI":"10.3389\/fmicb.2024.1376389"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"631.e1","DOI":"10.1016\/j.cmi.2020.05.042","article-title":"Dynamics and predisposition of respiratory viral co-infections in children and adults","volume":"27","author":"Mandelia","year":"2021","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1991","DOI":"10.1007\/s00431-021-03947-x","article-title":"Viral co-infections among SARS-CoV-2-infected children and infected adult household contacts","volume":"180","author":"Pigny","year":"2021","journal-title":"Eur. J. Pediatr."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1007\/s10096-020-04038-9","article-title":"Children were less frequently infected with SARS-CoV-2 than adults during 2020 COVID-19 pandemic in Warsaw, Poland","volume":"40","author":"Kuchar","year":"2021","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1205","DOI":"10.1038\/s41591-020-0962-9","article-title":"Eggo RM. Age-dependent effects in the transmission and control of COVID-19 epidemics","volume":"26","author":"Davies","year":"2020","journal-title":"Nat. Med."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"e13","DOI":"10.1016\/j.jinf.2022.08.025","article-title":"Are SARS-CoV-2 viral loads in children lower than in adults?","volume":"86","author":"Bayhan","year":"2023","journal-title":"J. Infect."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1007\/s12098-020-03322-y","article-title":"Pathophysiology of COVID-19: Why Children Fare Better than Adults?","volume":"87","author":"Dhochak","year":"2020","journal-title":"Indian J. Pediatr."},{"key":"ref_54","unstructured":"Manti, S., Licari, A., Montagna, L., Votto, M., Leonardi, S., Brambilla, I., Castagnoli, R., Foiadelli, T., Marseglia, G.L., and Cardinale, F. (2020). SARS-CoV-2 infection in pediatric population. Acta Biomed., 91."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"e2019006","DOI":"10.4084\/mjhid.2019.006","article-title":"Respiratory Viral Infections in Children and Adolescents with Hematological Malignancies","volume":"11","author":"Han","year":"2019","journal-title":"Mediterr. J. Hematol. Infect. Dis."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Trapani, S., Caporizzi, A., Ricci, S., and Indolfi, G. (2023). Human Bocavirus in Childhood: A True Respiratory Pathogen or a \u201cPassenger\u201d Virus? A Comprehensive Review. Microorganisms, 11.","DOI":"10.3390\/microorganisms11051243"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"05040","DOI":"10.7189\/jogh.12.05040","article-title":"The role of respiratory co-infection with influenza or respiratory syncytial virus in the clinical severity of COVID-19 patients: A systematic review and meta-analysis","volume":"12","author":"Cong","year":"2022","journal-title":"J. Glob. Health"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"2947","DOI":"10.1002\/jmv.26817","article-title":"Co-infection of influenza A virus and SARS-CoV-2: A retrospective cohort study","volume":"93","author":"Cheng","year":"2021","journal-title":"J. Med. Virol."},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Gautam, S., Malhotra, B., Sharma, P., Bhomia, N., Deeba, F., Sharma, H., and Parsoya, D. (2023). Co-infection of respiratory pathogens in SARS-CoV-2 positive patients at North West India, Rajasthan. Indian J. Med. Microbiol., 44.","DOI":"10.1016\/j.ijmmb.2023.100371"},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Deng, Z., Li, C., Wang, Y., Wu, F., Liang, C., Deng, W., and Wang, Y. (2023). Targeted next-generation sequencing for pulmonary infection diagnosis in patients unsuitable for bronchoalveolar lavage. Front. Med., 10.","DOI":"10.3389\/fmed.2023.1321515"},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Guo, W., Cui, X., Wang, Q., Wei, Y., Guo, Y., Zhang, T., and Zhan, J. (2022). Clinical evaluation of metagenomic next-generation sequencing for detecting pathogens in bronchoalveolar lavage fluid collected from children with community-acquired pneumonia. Front. Med., 9.","DOI":"10.3389\/fmed.2022.952636"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1017\/ice.2021.495","article-title":"Respiratory virus coinfections with severe acute respiratory coronavirus virus 2 (SARS-CoV-2) continue to be rare one year into the coronavirus disease 2019 (COVID-19) pandemic in Alberta, Canada (June 2020\u2013May 2021)","volume":"44","author":"Kanji","year":"2023","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"3934","DOI":"10.1038\/s41598-021-83642-x","article-title":"Respiratory viral co-infections among SARS-CoV-2 cases confirmed by virome capture sequencing","volume":"11","author":"Kim","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Sahajpal, N.S., Mondal, A.K., Njau, A., Petty, Z., Chen, J., Ananth, S., Ahluwalia, P., Williams, C., Ross, T.M., and Chaubey, A. (2021). High-Throughput Next-Generation Sequencing Respiratory Viral Panel: A Diagnostic and Epidemiologic Tool for SARS-CoV-2 and Other Viruses. Viruses, 13.","DOI":"10.3390\/v13102063"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"19274","DOI":"10.1038\/s41598-022-23422-3","article-title":"Capturing SARS-CoV-2 from patient samples with low viral abundance: A comparative analysis","volume":"12","author":"Kornobis","year":"2022","journal-title":"Sci. Rep."},{"key":"ref_66","doi-asserted-by":"crossref","unstructured":"Chatterjee, S., Bhattacharya, M., Nag, S., Dhama, K., and Chakraborty, C. (2023). A Detailed Overview of SARS-CoV-2 Omicron: Its Sub-Variants, Mutations and Pathophysiology, Clinical Characteristics, Immunological Landscape, Immune Escape, and Therapies. Viruses, 15.","DOI":"10.3390\/v15010167"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"5","DOI":"10.58395\/68gqp351","article-title":"Dynamic of SARS-CoV-2 spread in Bulgaria, 2020\u20132022","volume":"51","author":"Madzharova","year":"2023","journal-title":"Probl. Infect. Parasit. Dis."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"921","DOI":"10.1016\/j.ijid.2022.07.060","article-title":"Metagenomic next-generation sequencing for accurate diagnosis and management of lower respiratory tract infections","volume":"122","author":"Liang","year":"2022","journal-title":"Int. J. Infect. Dis."},{"key":"ref_69","doi-asserted-by":"crossref","unstructured":"Zheng, Y., Qiu, X., Wang, T., and Zhang, J. (2021). The Diagnostic Value of Metagenomic Next-Generation Sequencing in Lower Respiratory Tract Infection. Front. Cell Infect. Microbiol., 11.","DOI":"10.3389\/fcimb.2021.694756"},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Trombetta, C.M., Kistner, O., Montomoli, E., Viviani, S., and Marchi, S. (2022). Influenza Viruses and Vaccines: The Role of Vaccine Effectiveness Studies for Evaluation of the Benefits of Influenza Vaccines. Vaccines, 10.","DOI":"10.3390\/vaccines10050714"},{"key":"ref_71","doi-asserted-by":"crossref","unstructured":"Fratty, I.S., Jurkowicz, M., Zuckerman, N., Nemet, I., Atari, N., Kliker, L., Gur-Arie, L., Rosenberg, A., Glatman-Freedman, A., and Lustig, Y. (2024). Influenza vaccine compatibility among hospitalized patients during and after the COVID-19 pandemic. Front. Microbiol., 14.","DOI":"10.3389\/fmicb.2023.1296179"},{"key":"ref_72","doi-asserted-by":"crossref","unstructured":"Igarashi, M., Ito, K., Yoshida, R., Tomabechi, D., Kida, H., and Takada, A. (2010). Predicting the antigenic structure of the pandemic (H1N1) 2009 influenza virus hemagglutinin. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0008553"},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Zolotarova, O., Budzanivska, I., Leibenko, L., Radchenko, L., and Mironenko, A. (2019). Antigenic Site Variation in the Hemagglutinin of Pandemic Influenza A(H1N1)pdm09 Viruses between 2009\u20132017 in Ukraine. Pathogens, 8.","DOI":"10.3390\/pathogens8040194"},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Dempsey, R., Tamburrino, G., Schewe, K.E., Crowe, J., Nuccitelli, A., and Dibben, O. (2022). Haemagglutinin substitutions N125D, D127E, D222G and R223Q improve replicative fitness and vaccine effectiveness of an A\/H1N1pdm09 live attenuated influenza vaccine virus by enhancing \u03b1-2,6 receptor binding. PLoS Pathog., 18.","DOI":"10.1371\/journal.ppat.1010585"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"4504","DOI":"10.1128\/JVI.00057-15","article-title":"Influenza hemagglutinin (HA) stem region mutations that stabilize or destabilize the structure of multiple HA subtypes","volume":"89","author":"Galloway","year":"2015","journal-title":"J. Virol."},{"key":"ref_76","unstructured":"World Health Organization (2023). Influenza Virus Characterization Summary Report, Europe, December 2023 (No. WHO\/EURO: 2023 6189 45954 68789), World Health Organization, Regional Office for Europe."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"ofad577","DOI":"10.1093\/ofid\/ofad577","article-title":"Evolution of Influenza A(H3N2) Viruses in 2 Consecutive Seasons of Genomic Surveillance, 2021\u20132023","volume":"10","author":"Fall","year":"2023","journal-title":"Open Forum Infect. Dis."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"110897","DOI":"10.1016\/j.celrep.2022.110897","article-title":"Antigenic and virological properties of an H3N2 variant that continues to dominate the 2021\u20132022 Northern Hemisphere influenza season","volume":"39","author":"Bolton","year":"2022","journal-title":"Cell Rep."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"12274","DOI":"10.1128\/JVI.76.23.12274-12280.2002","article-title":"Antibody epitopes on the neuraminidase of a recent H3N2 influenza virus (A\/Memphis\/31\/98)","volume":"76","author":"Gulati","year":"2002","journal-title":"J. Virol."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"149","DOI":"10.4103\/lungindia.lungindia_66_24","article-title":"Influenza vaccination: A case for removal of B\/Yamagata from the quadrivalent vaccine","volume":"41","author":"Koul","year":"2024","journal-title":"Lung India"},{"key":"ref_81","doi-asserted-by":"crossref","unstructured":"Vajo, Z., and Torzsa, P. (2022). Extinction of the Influenza B Yamagata Line during the COVID Pandemic-Implications for Vaccine Composition. Viruses, 14.","DOI":"10.3390\/v14081745"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1343","DOI":"10.1126\/science.1222908","article-title":"Highly conserved protective epitopes on influenza B viruses","volume":"337","author":"Dreyfus","year":"2012","journal-title":"Science"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"6421","DOI":"10.1021\/jm100621s","article-title":"Structural and functional basis of resistance to neuraminidase inhibitors of influenza B viruses","volume":"53","author":"Oakley","year":"2010","journal-title":"J. Med. Chem."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"e01673-18","DOI":"10.1128\/JVI.01673-18","article-title":"Antibody Responses toward the Major Antigenic Sites of Influenza B Virus Hemagglutinin in Mice, Ferrets, and Humans","volume":"93","author":"Sun","year":"2019","journal-title":"J. Virol."},{"key":"ref_85","first-page":"83","article-title":"Structure and function of respiratory syncytial virus surface glycoproteins","volume":"372","author":"McLellan","year":"2013","journal-title":"Curr. Top. Microbiol. Immunol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1080\/14760584.2020.1711053","article-title":"Progress in the development of virus-like particle vaccines against respiratory viruses","volume":"19","author":"Quan","year":"2020","journal-title":"Expert Rev. Vaccines"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"2380","DOI":"10.3201\/eid2911.230836","article-title":"Genomic Sequencing Surveillance to Identify Respiratory Syncytial Virus Mutations, Arizona, USA","volume":"29","author":"Holland","year":"2023","journal-title":"Emerg. Infect. Dis."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"101337","DOI":"10.1016\/j.coviro.2023.101337","article-title":"Structural basis for respiratory syncytial virus and human metapneumovirus neutralization","volume":"61","author":"Miller","year":"2023","journal-title":"Curr. Opin. Virol."},{"key":"ref_89","doi-asserted-by":"crossref","unstructured":"Esposito, S., Abu-Raya, B., Bonanni, P., Cahn-Sellem, F., Flanagan, K.L., Martinon Torres, F., Mejias, A., Nadel, S., Safadi, M.A.P., and Simon, A. (2021). Coadministration of Anti-Viral Monoclonal Antibodies with Routine Pediatric Vaccines and Implications for Nirsevimab Use: A White Paper. Front. Immunol., 12.","DOI":"10.3389\/fimmu.2021.708939"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1016\/j.virol.2018.03.002","article-title":"Hexon and fiber of adenovirus type 14 and 55 are major targets of neutralizing antibody but only fiber-specific antibody contributes to cross-neutralizing activity","volume":"518","author":"Feng","year":"2018","journal-title":"Virology"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1007\/s00430-019-00645-2","article-title":"Human adenovirus binding to host cell receptors: A structural view","volume":"209","author":"Stasiak","year":"2020","journal-title":"Med. Microbiol. Immunol."},{"key":"ref_92","doi-asserted-by":"crossref","unstructured":"Wu, X., Zhang, J., Lan, W., Quan, L., Ou, J., Zhao, W., Wu, J., Woo, P.C.Y., Seto, D., and Zhang, Q. (2022). Molecular Typing and Rapid Identification of Human Adenoviruses Associated with Respiratory Diseases Using Universal PCR and Sequencing Primers for the Three Major Capsid Genes: Penton Base, Hexon, and Fiber. Front. Microbiol., 13.","DOI":"10.3389\/fmicb.2022.911694"},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"1289","DOI":"10.1056\/NEJM197206152862403","article-title":"Fatal pneumonia associated with adenovirus type 7 in three military trainees","volume":"286","author":"Dudding","year":"1972","journal-title":"N. Engl. J. Med."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"105","DOI":"10.7883\/yoken.67.105","article-title":"Impact of human adenovirus serotype 7 in hospitalized children with severe fatal pneumonia in the Philippines","volume":"67","author":"Yamamoto","year":"2014","journal-title":"Jpn. J. Infect. Dis."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"746","DOI":"10.1128\/JCM.02517-14","article-title":"Human adenovirus type 7 infection associated with severe and fatal acute lower respiratory illness and nosocomial transmission","volume":"53","author":"Cui","year":"2015","journal-title":"J. Clin. Microbiol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"e4392","DOI":"10.1093\/cid\/ciaa1149","article-title":"Role of Human Bocavirus Respiratory Tract Infection in Hematopoietic Cell Transplant Recipients","volume":"73","author":"Ogimi","year":"2021","journal-title":"Clin. Infect. Dis."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/j.jiph.2020.12.007","article-title":"Human bocavirus genotypes 1, 2, and 3 circulating in pediatric patients with acute gastroenteritis in Chiang Mai, Thailand, 2012\u20132018","volume":"14","author":"Nantachit","year":"2021","journal-title":"J. Infect. Public Health"},{"key":"ref_98","doi-asserted-by":"crossref","unstructured":"Korsun, N., Angelova, S., Trifonova, I., Voleva, S., Grigorova, I., Tzotcheva, I., Mileva, S., and Perenovska, P. (2021). Prevalence and Genetic Characteristics of Human Bocaviruses Detected in Patients with Acute Respiratory Infections in Bulgaria. Int. J. Microbiol., 2021.","DOI":"10.1155\/2021\/7035081"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/j.jinf.2016.05.014","article-title":"Genetic characterization of human bocavirus among children with severe acute respiratory infection in China","volume":"73","author":"Wang","year":"2016","journal-title":"J. Infect."},{"key":"ref_100","doi-asserted-by":"crossref","unstructured":"Ljubin-Sternak, S., Slovi\u0107, A., Mija\u010d, M., Jurkovi\u0107, M., For\u010di\u0107, D., Ivkovi\u0107-Jurekovi\u0107, I., Tot, T., and Vrane\u0161, J. (2021). Prevalence and Molecular Characterization of Human Bocavirus Detected in Croatian Children with Respiratory Infection. Viruses, 13.","DOI":"10.3390\/v13091728"},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"1197","DOI":"10.1099\/jmm.0.001243","article-title":"Detection and phylogenetic analysis of Human bocavirus in children diagnosed with acute respiratory tract infection","volume":"69","author":"Abozahra","year":"2020","journal-title":"J. Med. Microbiol."},{"key":"ref_102","doi-asserted-by":"crossref","unstructured":"Principi, N., Piralla, A., Zampiero, A., Bianchini, S., Umbrello, G., Scala, A., Bosis, S., Fossali, E., Baldanti, F., and Esposito, S. (2015). Bocavirus Infection in Otherwise Healthy Children with Respiratory Disease. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0135640"},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1111\/j.1750-2659.2012.00369.x","article-title":"Human bocavirus amongst an all-ages population hospitalised with acute lower respiratory infections in Cambodia","volume":"7","author":"Arnott","year":"2013","journal-title":"Influenza Other Respir. Viruses"},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1007\/s00239-001-0064-3","article-title":"Rates of molecular evolution in RNA viruses: A quantitative phylogenetic analysis","volume":"54","author":"Jenkins","year":"2002","journal-title":"J. Mol. Evol."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"9733","DOI":"10.1128\/JVI.00694-10","article-title":"Viral mutation rates","volume":"84","author":"Nebot","year":"2010","journal-title":"J. Virol."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"118","DOI":"10.12688\/wellcomeopenres.14730.2","article-title":"UK circulating strains of human parainfluenza 3: An amplicon based next generation sequencing method and phylogenetic analysis","volume":"3","author":"Smielewska","year":"2018","journal-title":"Wellcome Open Res."},{"key":"ref_107","doi-asserted-by":"crossref","unstructured":"Shao, N., Liu, B., Xiao, Y., Wang, X., Ren, L., Dong, J., Sun, L., Zhu, Y., Zhang, T., and Yang, F. (2021). Genetic Characteristics of Human Parainfluenza Virus Types 1\u20134 from Patients with Clinical Respiratory Tract Infection in China. Front. Microbiol., 12.","DOI":"10.3389\/fmicb.2021.679246"},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"1329","DOI":"10.1128\/jvi.64.3.1329-1334.1990","article-title":"Naturally occurring human parainfluenza type 3 viruses exhibit divergence in amino acid sequence of their fusion protein neutralization epitopes and cleavage sites","volume":"64","author":"Coelingh","year":"1990","journal-title":"J. Virol."},{"key":"ref_109","doi-asserted-by":"crossref","unstructured":"He, Y., Liu, W.J., Jia, N., Richardson, S., and Huang, C. (2023). Viral respiratory infections in a rapidly changing climate: The need to prepare for the next pandemic. EBioMedicine, 93.","DOI":"10.1016\/j.ebiom.2023.104593"},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.virusres.2011.09.003","article-title":"Insights on influenza pathogenesis from the grave","volume":"162","author":"Taubenberger","year":"2011","journal-title":"Virus Res."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"507","DOI":"10.3201\/eid1803.111238","article-title":"Adenovirus-associated deaths in US military during postvaccination period, 1999\u20132010","volume":"18","author":"Potter","year":"2012","journal-title":"Emerg. Infect. Dis."},{"key":"ref_112","doi-asserted-by":"crossref","unstructured":"Carballal, G., Videla, C., Misirlian, A., Requeijo, P.V., and Aguilar Mdel, C. (2002). Adenovirus type 7 associated with severe and fatal acute lower respiratory infections in Argentine children. BMC Pediatr., 2.","DOI":"10.1186\/1471-2431-2-6"}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/16\/6\/958\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:58:09Z","timestamp":1760108289000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/16\/6\/958"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,6,13]]},"references-count":112,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2024,6]]}},"alternative-id":["v16060958"],"URL":"https:\/\/doi.org\/10.3390\/v16060958","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,6,13]]}}}