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Genetic characterization and evolutionary analysis of canine parvovirus in Tangshan, China

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Abstract

Canine parvovirus (CPV) is a major enteric virus of carnivores worldwide that poses a considerable threat to dogs. In this study, we investigated the genetic variation of CPV in Tangshan, China, and the relationships between CPV disease and the vaccination status, age, and gender of dogs. Seventy-seven fecal samples from dogs in Tangshan that tested positive for CPV were obtained for analysis. Twenty-two full-length VP2 gene sequences were successfully amplified. The 22 strains included 17 CPV-2c variants, four new CPV-2a variants, and one new CPV-2b variant. Phylogenetic analysis showed that all of the CPV-2c strains clustered together and were closely related to CPV-2c strains from Asia but distantly related to CPV-2c strains from Europe. Further amino acid sequence analysis showed that, relative to CPV-2c strains from Europe, most of the CPV-2c stains in this study had A5G, F267Y, Y324I, and Q370R mutations. These findings provide a more comprehensive understanding of the variants of CPV circulating in China.

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Fig. 1
Fig. 2

Data availability

Genome sequences have been submitted to the GenBank database.

References

  1. Zhuang QY, Qiu Y, Pan ZH, Wang SC, Wang B, Wu WK, Yu JM, Yi Y, Sun FL, Wang KC (2019) Genome sequence characterization of canine parvoviruses prevalent in the Sichuan province of China. Transbound Emerg Dis 66:897–907

    Article  CAS  PubMed  Google Scholar 

  2. Mira F, Purpari G, Lorusso E, Di Bella S, Gucciardi F, Desario C, Macaluso G, Decaro N, Guercio A (2018) Introduction of Asian canine parvovirus in Europe through dog importation. Transbound Emerg Dis 65:16–21

    Article  CAS  PubMed  Google Scholar 

  3. Allison AB, Organtini LJ, Zhang S, Hafenstein SL, Holmes EC, Parrish CR (2016) Single Mutations in the VP2 300 loop region of the three-fold spike of the carnivore parvovirus capsid can determine host range. J Virol 90:753–767

    Article  CAS  PubMed  Google Scholar 

  4. Zhou P, Zeng W, Zhang X, Li S (2017) The genetic evolution of canine parvovirus—a new perspective. PLoS One 12:e0175035

    Article  PubMed  PubMed Central  Google Scholar 

  5. Chen Y, Wang J, Bi Z, Tan Y, Lv L, Zhao H, Xia X, Zhu Y, Wang Y, Qian J (2021) Molecular epidemiology and genetic evolution of canine parvovirus in East China, during 2018–2020. Infect Genet Evol 90:104780

    Article  CAS  PubMed  Google Scholar 

  6. Doan HTT, Le XTK, Do RT, Nguyen KT, Le TH (2021) Canine parvovirus type 2c in Vietnam continues to produce distinct descendants with new mutations restricted to Vietnamese variants. Arch Virol 166:1741–1749

    Article  CAS  PubMed  Google Scholar 

  7. Jiang H, Yu Y, Yang R, Zhang S, Wang D, Jiang Y, Yang W, Huang H, Shi C, Ye L, Yang G, Wang J, Wang C (2021) Detection and molecular epidemiology of canine parvovirus type 2 (CPV-2) circulating in Jilin Province, Northeast China. Comp Immunol Microbiol Infect Dis 74:101602

    Article  CAS  PubMed  Google Scholar 

  8. Li C, Tang J, Chen Z, Niu G, Liu G (2019) A divergent canine parvovirus type 2c (CPV-2c) isolate circulating in China. Infect Genet Evol 73:242–247

    Article  PubMed  Google Scholar 

  9. Mira F, Purpari G, Di Bella S, Colaianni ML, Schirò G, Chiaramonte G, Gucciardi F, Pisano P, Lastra A, Decaro N, Guercio A (2019) Spreading of canine parvovirus type 2c mutants of Asian origin in southern Italy. Transbound Emerg Dis 66:2297–2304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Parrish CR, Kawaoka Y (2005) The origins of new pandemic viruses: the acquisition of new host ranges by canine parvovirus and influenza A viruses. Annu Rev Microbiol 59:553–586

    Article  CAS  PubMed  Google Scholar 

  11. Battilani M, Balboni A, Ustulin M, Giunti M, Scagliarini A, Prosperi S (2011) Genetic complexity and multiple infections with more Parvovirus species in naturally infected cats. Vet Res 42:43

    Article  PubMed  PubMed Central  Google Scholar 

  12. Buonavoglia C, Martella V, Pratelli A, Tempesta M, Cavalli A, Buonavoglia D, Bozzo G, Elia G, Decaro N, Carmichael L (2001) Evidence for evolution of canine parvovirus type 2 in Italy. J Gen Virol 82:3021–3025

    Article  CAS  PubMed  Google Scholar 

  13. Miranda C, Thompson G (2016) Canine parvovirus: the worldwide occurrence of antigenic variants. J Gen Virol 97:2043–2057

    Article  CAS  PubMed  Google Scholar 

  14. Truyen U, Evermann JF, Vieler E, Parrish CR (1996) Evolution of canine parvovirus involved loss and gain of feline host range. Virology 215:186–189

    Article  CAS  PubMed  Google Scholar 

  15. Kwan E, Carrai M, Lanave G, Hill J, Parry K, Kelman M, Meers J, Decaro N, Beatty JA, Martella V, Barrs VR (2021) Analysis of canine parvoviruses circulating in Australia reveals predominance of variant 2b and identifies feline parvovirus-like mutations in the capsid proteins. Transbound Emerg Dis 68:656–666

    Article  CAS  PubMed  Google Scholar 

  16. Shima FK, Omobowale TO, Adesina RD, Nottidge HO, Fagbohun OA (2020) Molecular characterisation of canine parvoviruses from clinical samples and vaccines in Nigeria. Infect Genet Evol 85:104553

    Article  CAS  PubMed  Google Scholar 

  17. Hoelzer K, Shackelton LA, Parrish CR, Holmes EC (2008) Phylogenetic analysis reveals the emergence, evolution and dispersal of carnivore parvoviruses. J Gen Virol 89:2280–2289

    Article  CAS  PubMed  Google Scholar 

  18. Zhao Y, Lin Y, Zeng X, Lu C, Hou J (2013) Genotyping and pathobiologic characterization of canine parvovirus circulating in Nanjing, China. Virol J 10:272

    Article  PubMed  PubMed Central  Google Scholar 

  19. Zhao H, Wang J, Jiang Y, Cheng Y, Lin P, Zhu H, Han G, Yi L, Zhang S, Guo L, Cheng S (2017) Typing of canine parvovirus strains circulating in North-East China. Transbound Emerg Dis 64:495–503

    Article  CAS  PubMed  Google Scholar 

  20. Chen B, Zhang X, Zhu J, Liao L, Bao E (2021) Molecular epidemiological survey of canine parvovirus circulating in China from 2014 to 2019. Pathogens 10:588

    Article  PubMed  PubMed Central  Google Scholar 

  21. Hao X, He Y, Wang C, Xiao W, Liu R, Xiao X, Zhou P, Li S (2020) The increasing prevalence of CPV-2c in domestic dogs in China. PeerJ 8:e9869

    Article  PubMed  PubMed Central  Google Scholar 

  22. Qi S, Zhao J, Guo D, Sun D (2020) A mini-review on the epidemiology of canine parvovirus in China. Front Vet Sci 7:5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Wang X, Li C, Guo D, Wang X, Wei S, Geng Y, Wang E, Wang Z, Zhao X, Su M, Liu Q, Zhang S, Feng L, Sun D (2016) Co-circulation of canine coronavirus I and IIa/b with high prevalence and genetic diversity in Heilongjiang province, Northeast China. PLoS One 11:e0146975

    Article  PubMed  PubMed Central  Google Scholar 

  24. Kosakovsky Pond SL, Frost SD (2005) Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22:1208–1222

    Article  PubMed  Google Scholar 

  25. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL (2012) Detecting individual sites subject to episodic diversifying selection. PLoS Genet 8:e1002764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Kosakovsky Pond SL, Scheffler K (2013) FUBAR: a fast, unconstrained bayesian approximation for inferring selection. Mol Biol Evol 30:1196–1205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Moon BY, Jang J, Kim SH, Kim YH, Lee HK, So B, Park CK, Lee KK (2020) Genetic characterization of canine parvovirus type 2c from domestic dogs in Korea. Transbound Emerg Dis 67:1645–1653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Cavalli A, Desario C, Kusi I, Mari V, Lorusso E, Cirone F, Kumbe I, Colaianni ML, Buonavoglia D, Decaro N (2014) Detection and genetic characterization of Canine parvovirus and Canine coronavirus strains circulating in district of Tirana in Albania. J Vet Diagn Investig 26:563–566

    Article  Google Scholar 

  29. Geng Y, Guo D, Li C, Wang E, Wei S, Wang Z, Yao S, Zhao X, Su M, Wang X, Wang J, Wu R, Feng L, Sun D (2015) Co-circulation of the rare CPV-2c with unique Gln370Arg substitution, new CPV-2b with unique Thr440Ala substitution, and new CPV-2a with high prevalence and variation in Heilongjiang Province, Northeast China. PLoS One 10:e0137288

    Article  PubMed  PubMed Central  Google Scholar 

  30. Steinel A, Venter EH, Van Vuuren M, Parrish CR, Truyen U (1998) Antigenic and genetic analysis of canine parvoviruses in southern Africa. Onderstepoort J Vet Res 65:239–242

    CAS  PubMed  Google Scholar 

  31. Shams F, Pourtaghi H, Abdolmaleki Z (2022) The first evaluation of the effectiveness of canine vaccination schedule by two commercial vaccines in Iran. BMC Vet Res 18:119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Pratelli A, Tempesta M, Roperto FP, Sagazio P, Carmichael L, Buonavoglia C (1999) Fatal coronavirus infection in puppies following canine parvovirus 2b infection. J Vet Diagn Investig 11:550–553

    Article  CAS  Google Scholar 

  33. Decaro N, Martella V, Desario C, Bellacicco AL, Camero M, Manna L, d’Aloja D, Buonavoglia C (2006) First detection of canine parvovirus type 2c in pups with haemorrhagic enteritis in Spain. J Vet Med B Infect Dis Vet Public Health 53:468–472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Hu W, Zheng L, Xu X, Liu Q, Ji J, Yao L, Kan Y, Bi Y (2020) Genetic characterisation and local genotypes of canine parvovirus strains collected from pet dogs in central and Eastern China during 2018–2019. J Vet Res 64:477–486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Parrish CR, Have P, Foreyt WJ, Evermann JF, Senda M, Carmichael LE (1988) The global spread and replacement of canine parvovirus strains. J Gen Virol 69:1111–1116

    Article  PubMed  Google Scholar 

  36. Allison AB, Kohler DJ, Ortega A, Hoover EA, Grove DM, Holmes EC, Parrish CR (2014) Host-specific parvovirus evolution in nature is recapitulated by in vitro adaptation to different carnivore species. PLoS Pathog 10:e1004475

    Article  PubMed  PubMed Central  Google Scholar 

  37. Kaelber JT, Demogines A, Harbison CE, Allison AB, Goodman LB, Ortega AN, Sawyer SL, Parrish CR (2012) Evolutionary reconstructions of the transferrin receptor of Caniforms supports canine parvovirus being a re-emerged and not a novel pathogen in dogs. PLoS Pathog 8:e1002666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Decaro N, Desario C, Addie DD, Martella V, Vieira MJ, Elia G, Zicola A, Davis C, Thompson G, Thiry E, Truyen U, Buonavoglia C (2007) The study molecular epidemiology of canine parvovirus, Europe. Emerg Infect Dis 13:1222–1224

    Article  PubMed  PubMed Central  Google Scholar 

  39. Parrish CR, Aquadro CF, Strassheim ML, Evermann JF, Sgro JY, Mohammed HO (1991) Rapid antigenic-type replacement and DNA sequence evolution of canine parvovirus. J Virol 65:6544–6552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Liu C, Gao J, Li H, Sun F, Liang H, Liu H, Yi J (2021) Phylogenetic characteristics of canine parvovirus type 2c variant endemic in Shanghai, China. Viruses 13:2257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Hoang M, Lin WH, Le VP, Nga BTT, Chiou MT, Lin CN (2019) Molecular epidemiology of canine parvovirus type 2 in Vietnam from November 2016 to February 2018. Virol J 16:52

    Article  PubMed  PubMed Central  Google Scholar 

  42. Wang J, Lin P, Zhao H, Cheng Y, Jiang Z, Zhu H, Wu H, Cheng S (2016) Continuing evolution of canine parvovirus in China: isolation of novel variants with an Ala5Gly mutation in the VP2 protein. Infect Genet Evol 38:73–78

    Article  CAS  PubMed  Google Scholar 

  43. Hueffer K, Parker JS, Weichert WS, Geisel RE, Sgro JY, Parrish CR (2003) The natural host range shift and subsequent evolution of canine parvovirus resulted from virus-specific binding to the canine transferrin receptor. J Virol 77:1718–1726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Balboni A, Niculae M, Di Vito S, Urbani L, Terrusi A, Muresan C, Battilani M (2021) The detection of canine parvovirus type 2c of Asian origin in dogs in Romania evidenced its progressive worldwide diffusion. BMC Vet Res 17:206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Ogbu KI, Mira F, Purpari G, Nwosuh C, Loria GR, Schirò G, Chiaramonte G, Tion MT, Di Bella S, Ventriglia G, Decaro N, Anene BM, Guercio A (2020) Nearly full-length genome characterization of canine parvovirus strains circulating in Nigeria. Transbound Emerg Dis 67:635–647

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was funded by the National Key Research and Development Program of China (grant number 2016YFD0501003) and the School Scientific Research Project of Jiangsu Agri-animal Husbandry Vocational College (grant number NSF2021ZR11).

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Author notes

  1. Zhaoyang Wang, Yajun Jiang and Ting Xin contributed equally to this work.

Authors and Affiliations

  1. Institute of Animal Sciences (IAS), Chinese Academy of Agricultural Sciences (CAAS), Beijing, China

    Zhaoyang Wang, Yajun Jiang, Ting Xin, Weifeng Yuan, Xiaoyu Guo, Hongfei Zhu & Hong Jia

  2. College of Veterinary Medicine, South China Agricultural University, Guangzhou, China

    Zhaoyang Wang

  3. Jiangsu Agri-animal Husbandry Vocational College, Taizhou, China

    Honglei Zhou

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  1. Zhaoyang Wang
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  2. Yajun Jiang
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Contributions

ZYW, YJJ, TX, and HJ participated in the study design, wrote the draft, and collected the documentation materials. WFY, XYG, HLZ, and HFZ helped revise the draft and collected the samples. All authors read and approved the manuscript.

Corresponding author

Correspondence to Hong Jia.

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Wang, Z., Jiang, Y., Xin, T. et al. Genetic characterization and evolutionary analysis of canine parvovirus in Tangshan, China. Arch Virol 167, 2263–2269 (2022). https://doi.org/10.1007/s00705-022-05502-x

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