Abstract
An avian-origin canine influenza virus (CIV) has recently emerged in dogs and is spreading in China. Given that humans have frequent contact with dogs, this has prompted an increased emphasis on biosafety. In this study, we collected 693 nasal swab samples and 800 blood samples from stray dogs in animal shelters to survey canine influenza epidemiology and characterize the evolution of CIV H3N2 in Shanghai. We tested samples for canine influenza antibodies and canine influenza RNA in January–May, 2019, and the results showed that the positive rate was 17.62% by ELISA, 15.75% by microneutralization (MN) assay, and 18.51% by real time RT-PCR, respectively. We also performed phylogenetic and genomic analysis on six H3N2 CIV isolates. The H3N2 viruses which prevailed in Shanghai originated from Beijing and Jiangsu isolates. Phylogenetic analysis showed that the sequences of CIV isolates have multiple amino acid antigenic drifts, deletions, and substitutions. The time of the most recent common ancestor (TMRCA) of HA and NA was 2004 and 2005, respectively. Notably, the substitution, 146S, in hemagglutinin and the deletion in the neuraminidase (NA) stalk region we found in this study warrant attention because they have frequently been identified in human influenza viruses. The potential adaptation of this CIV H3N2 clade to mammals and its public health threat should be further evaluated.
Similar content being viewed by others
References
Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y (1992) Evolution and ecology of influenza A viruses. Microbiol Rev 56:152–179. https://doi.org/10.1007/82_2014_396
Tong S, Zhu X, Li Y, Shi M, Zhang J, Bourgeois M, Yang H, Chen X, Recuenco S, Gomez J, Chen LM, Johnson A, Tao Y, Dreyfus C, Yu W, McBride R, Carney PJ, Gilbert AT, Chang J, Guo Z, Davis CT, Paulson JC, Stevens J, Rupprecht CE, Holmes EC, Wilson IA, Donis RO (2013) New world bats harbor diverse influenza A viruses. PLoS Pathog 9:e1003657. https://doi.org/10.1371/journal.ppat.1003657
Webster RG, Shortridge KF, Kawaoka Y (1997) Influenza: interspecies transmission and emergence of new pandemics. FEMS Immunol Med Microbiol 18:275–279. https://doi.org/10.1111/j.1574-695X.1997.tb01056.x
Song D, Kang B, Lee C, Jung K, Ha G, Kang D, Park S, Park B, Oh J (2008) Transmission of avian influenza virus (H3N2) to dogs. Emerg Infect Dis 14:741–746. https://doi.org/10.3201/eid1405.071471
Li S, Shi Z, Jiao P, Zhang G, Zhong Z, Tian W, Long LP, Cai Z, Zhu X, Liao M, Wan XF (2010) Avian-origin H3N2 canine influenza A viruses in Southern China. Infect Genet Evol 10:1286–1288. https://doi.org/10.1016/j.meegid.2010.08.010
Lyu Y, Song S, Zhou L, Bing G, Wang Q, Sun H, Chen M, Hu J, Wang M, Sun H, Pu J, Xia Z, Liu J, Sun Y (2019) Canine influenza virus A(H3N2) clade with antigenic variation, china, 2016–2017. Emerg Infect Dis 25:161–165. https://doi.org/10.3201/eid2501.171878
Su S, Chen Y, Zhao FR, Chen JD, Xie JX, Chen ZM, Huang Z, Hu YM, Zhang MZ, Tan LK, Zhang GH, Li SJ (2013) Avian-origin H3N2 canine influenza virus circulating in farmed dogs in Guangdong, China. Infect Genet Evol 19:251–256. https://doi.org/10.1016/j.meegid.2012.11.018
Teng Q, Zhang X, Xu D, Zhou J, Dai X, Chen Z, Li Z (2013) Characterization of an H3N2 canine influenza virus isolated from Tibetan mastiffs in China. Vet Microbiol 162:345–352. https://doi.org/10.1016/j.vetmic.2012.10.006
Sun Y, Sun S, Ma J, Tan Y, Du L, Shen Y, Mu Q, Pu J, Lin D, Liu J (2013) Identification and characterization of avian-origin H3N2 canine influenza viruses in northern China during 2009–2010. Virology 435:301–307. https://doi.org/10.1016/j.virol.2012.09.037
Lin Y, Zhao Y, Zeng X, Lu C, Liu Y (2012) Genetic and pathobiologic characterization of H3N2 canine influenza viruses isolated in the Jiangsu Province of China in 2009–2010. Vet Microbiol 158:247–258. https://doi.org/10.1016/j.vetmic.2012.02.016
Pulit-Penaloza JA, Simpson N, Yang H, Creager HM, Maines TR (2017) Assessment of molecular, antigenic, and pathological features of canine influenza a(h3n2) viruses that emerged in the united states. J Infect Dis 216(supp_4):S499–S507
Rowe T, Abernathy RA, Hu-Primmer J, Thompson WW, Lu X, Lim W et al (1999) Detection of antibody to avian influenza a (h5n1) virus in human serum by using a combination of serologic assays. J Clin Microbiol 37(4):937–943
Sun Y, Shen Y, Zhang X, Wang Q, Liu L, Han X et al (2014) A serological survey of canine h3n2, pandemic h1n1/09 and human seasonal h3n2 influenza viruses in dogs in china. Vet Microbiol 168(1):193–196
Sun Y, Shen Y, Zhang X, Wang Q, Liu L, Han X, Jiang B, Wang R, Sun H, Pu J, Lin D, Xia Z, Liu J (2014) A serological survey of canine H3N2, pandemic H1N1/09 and human seasonal H3N2 influenza viruses in dogs in China. Vet Microbiol 168:193–196. https://doi.org/10.1016/j.vetmic.2013.10.012
OIE (World Organization for Animal Health (2015) Manual of diagnostic tests and vaccines for terrestrial animals. https://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/2.03.04_AI.pdf.
Phipps LP, Essen SC, Brown IH (2004) Genetic subtyping of influenza a viruses using rt-pcr with a single set of primers based on conserved sequences within the ha2 coding region. J Virol Methods 122(1):119–122
Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR (2001) Universal primer set for the full-length amplification of all influenza a viruses. Arch Virol 146(12):2275–2289
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214. https://doi.org/10.1186/1471-2148-7-214
Stadler T, Kühnert D, Bonhoeffer S, Drummond AJ (2013) Birth–death skyline plot reveals temporal changes of epidemic spread in HIV and hepatitis C virus (HCV). Proc Natl Acad Sci 110(1):228–233
Helfrich P, Rieb E, Abrami G, Lucking A, Mehler A (2018 TreeAnnotator: versatile visual annotation of hierarchical text relations. Lrec 2018: edition of the language resources and evaluation conference. https://doi.org/10.1128/JVI.03395-14.
Rambaut A, Lam TT, Max Carvalho L, Pybus OG (2016) Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol 2:vew007
Zhu H, Hughes J, Murcia PR (2015) Origins and evolutionary dynamics of H3N2 canine influenza virus. J Virol 89:5406–5418
Lee IW, Kim YI, Lim GJ, Kwon HI, Si YJ, Park SJ et al (2018) Comparison of the virulence and transmissibility of canine h3n2 influenza viruses and characterization of their canine adaptation factors. Emerg Microb Infect 7(1):17
Connor RJ, Kawaoka Y, Webster RG, Paulson JC (1994) Receptor specificity in human, avian, and equine h2 and h3 influenza virus isolates. Virology 205(1):17–23
Su S, Li HT, Zhao FR, Chen JD, Xie JX, Chen ZM et al (2013) Avian-origin h3n2 canine influenza virus circulating in farmed dogs in guangdong, china. Infect Genet Evol 14:444–449
Lee C, Song D, Kang B, Kang D, Yoo J, Jung K et al (2009) A serological survey of avian origin canine h3n2 influenza virus in dogs in korea. Vet Microbiol 137(3–4):359–362
Voorhees IEH, Glaser AL, Kathy TK, Sandra N, Dalziel BD, Dubovi EJ et al (2017) Spread of canine influenza a(h3n2) virus, united states. Emerg Infect Dis 23(12):1950–1957
Lyu Y, Song S, Zhou L, Bing G, Wang Q, Sun H, Chen M, Hu J, Wang M, Sun H, Pu J, Sun Y (2019) Canine influenza virus a(h3n2) clade with antigenic variation, china, 2016–2017. Emerg Infect Dis 25(1):161–165. https://doi.org/10.3201/eid2501.171878
Lin D, Sun S, Du L, Ma J, Fan L, Pu J, Sun Y, Zhao J, Sun H, Liu J (2012) Natural and experimental infection of dogs with pandemic H1N1/2009 influenza virus. J General Virol 93:119–123. https://doi.org/10.1099/vir.0.037358-0
Matrosovich M, Zhou N, Kawaoka Y, Webster R (1999) The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties. J Virol 73:1146–1155. https://doi.org/10.0000/PMID9882316
Acknowledgements
This work was supported by a grant from Shanghai Agricultural Applied Technology Development Program, China (Grant NO. G20190303) and Shanghai Outstanding Agricultural Academic Leaders Plan.
Author information
Authors and Affiliations
Contributions
HJZ and JW conceived and designed the study. HXS, FFG, HBJ, DQY, JL, XCY, and XL performed the experiments. HXS and FFG analyzed the data. HXS and FFG wrote the manuscript, and all authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
All individual participants approve to submit and declare no conflict of interests.
Ethics approval
This study was conducted according to animal welfare guidelines of the World Organization for Animal Health and approved by Shanghai Municipal Commission of Agriculture (Permit number: 2013 [19]).
Additional information
Edited by William Dundon.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Shen, HX., Ge, FF., Li, X. et al. Epidemiological survey and genetic evolution of H3N2 subtype influenza viruses from stray dogs in Shanghai, China. Virus Genes 56, 329–338 (2020). https://doi.org/10.1007/s11262-020-01748-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11262-020-01748-2