Korean Journal of Veterinary Service (한국동물위생학회지)

The Korean Society of Veterinary Service (한국동물위생학회)
권호 표지
DOI QR코드

DOI QR Code

Prevalence of feline calicivirus in Korean cats determined by an improved real-time RT-PCR assay

  • Ji-Su Baek (College of Veterinary Medicine & Animal Disease Intervention Center, Kyungpook National University) ;
  • Jong-Min Kim (College of Veterinary Medicine & Animal Disease Intervention Center, Kyungpook National University) ;
  • Hye-Ryung Kim (College of Veterinary Medicine & Animal Disease Intervention Center, Kyungpook National University) ;
  • Yeun-Kyung Shin (Foreign Animal Disease Division, Animal and Plant Quarantine Agency) ;
  • Oh-Kyu Kwon (Foreign Animal Disease Division, Animal and Plant Quarantine Agency) ;
  • Hae-Eun Kang (Foreign Animal Disease Division, Animal and Plant Quarantine Agency) ;
  • Choi-Kyu Park (College of Veterinary Medicine & Animal Disease Intervention Center, Kyungpook National University)
  • Received : 2023.05.30
  • Accepted : 2023.06.10
  • Published : 2023.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

Feline calicivirus (FCV) is considered the main viral pathogen of feline upper respiratory tract disease (URTD). The frequent mutations of field FCV strains result in the poor diagnostic sensitivity of previously developed molecular diagnostic assays. In this study, a more sensitive real-time reverse transcription-polymerase chain reaction (qRT-PCR) assay was developed for broad detection of currently circulating FCVs and comparatively evaluated the diagnostic performance with previously developed qRT-PCR assay using clinical samples collected from Korean cat populations. The developed qRT-PCR assay specifically amplified the FCV p30 gene with a detection limit of below 10 copies/reaction. The assay showed high repeatability and reproducibility, with coefficients of intra-assay and inter-assay variation of less than 2%. Based on the clinical evaluation using 94 clinical samples obtained from URTD-suspected cats, the detection rate of FCV by the developed qRT-PCR assay was 47.9%, which was higher than that of the previous qRT-PCR assay (43.6%). The prevalence of FCV determined by the new qRT-PCR assay in this study was much higher than those of previous Korean studies determined by conventional RT-PCR assays. Due to the high sensitivity, specificity, and accuracy, the new qRT-PCR assay developed in this study will serve as a promising tool for etiological and epidemiological studies of FCV circulating in Korea. Furthermore, the prevalence data obtained in this study will contribute to expanding knowledge about the epidemiology of FCV in Korea.

Keywords

Acknowledgement

This work was supported by the fund (Z-1543085-2022-23-0302) by the Research of Animal and Plant Quarantine Agency, Republic of Korea.

References

  1. Abd-Eldaim MM, Wilkes RP, Thomas KV, Kennedy MA. 2009. Development and validation of a TaqMan real-time reverse transcription-PCR for rapid detection of feline calicivirus. Arch Virol 154: 555-560. https://doi.org/10.1007/s00705-009-0337-5
  2. Afonso MM, Pinchbeck GL, Smith SL, Daly JM, Gaskell RM, Dawson S, Radford AD. 2017. A multi-national European cross-sectional study of feline calicivirus epidemiology, diversity and vaccine cross-reactivity. Vaccine 35: 2753-2760. https://doi.org/10.1016/j.vaccine.2017.03.030
  3. Berger A, Willi B, Meli ML, Boretti FS, Hartnack S, Dreyfus A, Lutz H, Hofmann-Lehmann R. 2015. Feline calicivirus and other respiratory pathogens in cats with feline calicivirus-related symptoms and in clinically healthy cats in Switzerland. BMC Vet Res 11: 282.
  4. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT. 2009. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55: 611-622. https://doi.org/10.1373/clinchem.2008.112797
  5. Cai Y, Fukushi H, Koyasu S, Kuroda E, Yamaguchi T, Hirai K. 2002. An etiological investigation of domestic cats with conjunctivitis and upper respiratory tract disease in Japan. J Vet Med Sci 64: 215-219. https://doi.org/10.1292/jvms.64.215
  6. Cao L, Li Q, Shi K, Wei L, Ouyang H, Ye Z, Du W, Ye J, Hui X, Li J, Cal S, Zhou D. 2022a. Isolation and phylogenetic analysis of feline calicivirus strains from various region of China. Anim Dis 2: 16.
  7. Cao N, Tang Z, Zhang X, Li W, Li B, Tian Y, Xu D. 2022b. Development and application of a triplex TaqMan quantitative real-time PCR assay for simultaneous detection of feline calicivirus, feline parvovirus, and feline herpesvirus 1. Front Vet Sci 8: 792322.
  8. Chander Y, Tiwari K., Sajja S, Ramakrishnan A, Faaberg K and Sagar M. 2007. A TaqManR RT-PCR assay for the detection of feline calicivirus. Int J Virol 3: 100-106. https://doi.org/10.3923/ijv.2007.100.106
  9. Coyne KP, Christley RM, Pybus OG, Dawson S, Gaskell RM, Radford AD. 2012. Large-scale spatial and temporal genetic diversity of feline calicivirus. J Virol 86: 11356-11367. https://doi.org/10.1128/JVI.00701-12
  10. Di Martino B, Di Francesco CE, Meridiani I, Marsilio F. 2007. Etiological investigation of multiple respiratory infections in cats. New Microbiol 30: 455-461.
  11. Fernandez M, Manzanilla EG, Lloret A, Leon M, Thibault JC. 2017. Prevalence of feline herpesvirus-1, feline calicivirus, Chlamydophila felis and Mycoplasma felis DNA and associated risk factors in cats in Spain with upper respiratory tract disease, conjunctivitis and/or gingivostomatitis. J Feline Med Surg 19: 461-469. https://doi.org/10.1177/1098612X16634387
  12. Guo J, Zeng H, Long J, Wei Z, Ouyang K, Huang W, Chen Y. 2022. Co-circulation and evolution of genogroups I and II of respiratory and enteric feline calicivirus isolates in cats. Transbound Emerg Dis 69: 2924-2937. https://doi.org/10.1111/tbed.14447
  13. Helps CR, Lait P, Damhuis A, Bjornehammar U, Bolta D, Brovida C, Chabanne L, Egberink H, Ferrand G, Fontbonne A, Pennisi MG, Gruffydd-Jones T, Gunn-Moore D, Hartmann K, Lutz H, Malandain E, Mostl K, Stengel C, Harbour DA, Graat EA. 2005. Factors associated with upper respiratory tract disease caused by feline herpesvirus, feline calicivirus, Chlamydophila felis and Bordetella bronchiseptica in cats: experience from 218 European catteries. Vet Rec 156: 669-673. https://doi.org/10.1136/vr.156.21.669
  14. Helps CR, Lait P, Tasker S, Harbour D. 2002. Melting curve analysis of feline calicivirus isolates detected by real-time reverse transcription PCR. J Virol Methods 106: 241-244. https://doi.org/10.1016/S0166-0934(02)00167-2
  15. Henzel A, Sa e Silva M, Luo S, Lovato LT, Weiblen R. 2012. Genetic and phylogenetic analyses of capsid protein gene in feline calicivirus isolates from Rio Grande do Sul in southern Brazil. Virus Res 163: 667-671. https://doi.org/10.1016/j.virusres.2011.12.008
  16. Hofmann-Lehmann R, Hosie MJ, Hartmann K, Egberink H, Truyen U, Tasker S, Belak S, Boucraut-Baralon C, Frymus T, Lloret A, Marsilio F, Pennisi MG, Addie DD, Lutz H, Thiry E, Radford AD, Mostl K. 2022. Calicivirus Infection in Cats. Viruses 14: 937.
  17. Hou J, Sanchez-Vizcaino F, McGahie D, Lesbros C, Almeras T, Howarth D, O'Hara V, Dawson S, Radford AD. 2016. European molecular epidemiology and strain diversity of feline calicivirus. Vet Rec 178: 114-115. https://doi.org/10.1136/vr.103446
  18. Jeon GT, Kim HR, Kim J.M, Baek JS, Shin YK, Kwon OK, Kang HE, Cho HS, Cheon DS, Park CK. 2023a. Tailored multiplex real-time RT-PCR with speciesspecific internal positive controls for detecting SARS-CoV-2 in canine and feline clinical samples. Animals 13: 602.
  19. Jeon GT, Kim HR, Shin YK, Kwon OK, Kang HE, Kwon OD, Park CK. 2023c. An improved duplex real-time quantitative RT-PCR assay with a canine endogenous internal positive control for more sensitive and reliable detection of canine parainfluenza virus 5. Vet Sci 10: 142.
  20. Jeon GT, Kim JM, Park JH, Kim HR, Baek JS, Lee HJ, Shin YK, Kwon OK, Kang HE, Kim SK, Kim JH, Kim YH, Park CK. 2023b. A triplex real-time PCR assay for simultaneous and differential detection of Bordetella bronchiseptica, Mycoplasma cynos, and Mycoplasma canis in respiratory diseased dogs. Korean J Vet Serv 46: 15-27. https://doi.org/10.7853/kjvs.2023.46.1.15
  21. Johnson G, Nolan T, Bustin SA. 2013. Real-time quantitative PCR, pathogen detection and MIQE. Methods Mol Biol 943: 1-16.
  22. Kang BT, Park HM. 2008. Prevalence of feline herpesvirus 1, feline calicivirus and Chlamydophila felis in clinically normal cats at a Korean animal shelter. J Vet Sci 9: 207-209. https://doi.org/10.4142/jvs.2008.9.2.207
  23. Kim HR, Jeon GT, Kim JM, Baek JS, Shin YK, Kwon OK, Kang HE, Cho HS, Cheon DS, Park CK. 2022. Prevalence of Bordetella bronchiseptica, Mycoplasma felis, and Chlamydia felis using a newly developed triplex real-time polymerase chain reaction assay in Korean cat population. Korean J Vet Serv 45: 305-316. https://doi.org/10.7853/kjvs.2022.45.4.305
  24. Kim JM, Kim HR, Jeon GT, Baek JS, Kwon OD, Park CK. 2023. Molecular detection of porcine parainfluenza viruses 1 and 5 using a newly developed duplex real-time RT-PCR in South Korea. Animals (Basel) 13: 598.
  25. Kim SJ, Park YH, Park KT. 2020. Development of a novel reverse transcription PCR and its application to field sample testing for feline calicivirus prevalence in healthy stray cats in Korea. J Vet Sci 21:e71.
  26. Kwiecien R, Kopp-Schneider A, Blettner M. 2011. Concordance analysis: part 16 of a series on evaluation of scientific publications. Dtsch Arztebl Int 108: 515-521. https://doi.org/10.3238/arztebl.2011.0515
  27. Lee MJ, Park JH. 2022. Prevalence study of respiratory pathogens in Korean cats using real-time polymerase chain reaction. Korean J Vet Serv 45: 145-153. https://doi.org/10.7853/kjvs.2022.45.3.145
  28. Lee SY, Kim YK, Kim YS, Na EJ, Kim YJ, Oem JK. 2021. Intergenic recombination in feline calicivirus associated with a hemorrhagic-like disease in the Republic of Korea. Acta Virol 65: 232-236. https://doi.org/10.4149/av_2021_206
  29. Liu C, Liu Y, Qian P, Cao Y, Wang J, Sun C, Huang B, Cui N, Huo N, Wu H, Wang L, XiX, Tian K. 2020. Molecular and serological investigation of cat viral infectious diseases in China from 2016 to 2019. Transbound Emerg Dis 67: 2329-2335. https://doi.org/10.1111/tbed.13667
  30. Meli ML, Berger A, Willi B, Spiri AM, Riond B, Hofmann-Lehmann R. 2018. Molecular detection of feline calicivirus in clinical samples: a study comparing its detection by RT-qPCR directly from swabs and after virus isolation. J Virol Methods 251: 54-60. https://doi.org/10.1016/j.jviromet.2017.10.001
  31. Michael HT, Waterhouse T, Estrada M, Seguin MA. 2021. Frequency of respiratory pathogens and SARS-CoV-2 in canine and feline samples submitted for respiratory testing in early 2020. J Small Anim Pract 62: 336-342. https://doi.org/10.1111/jsap.13300
  32. Nguyen D, Barrs VR, Kelman M, Ward MP. 2019. Feline upper respiratory tract infection and disease in Australia. J Feline Med Surg 21: 973-978. https://doi.org/10.1177/1098612X18813248
  33. Palombieri A, Sarchese V, Giordano MV, Fruci P, Crisi PE, Aste G, Bongiovanni L, Rinaldi V, Sposato A, Camero M, Lanave G, Martella V, Marsilio F, Di Martino B, Di Profio F. 2023. Detection and characterization of feline calicivirus associated with paw and mouth disease. Animals 13: 65.
  34. Park JI, Suh SI, Hyun C. 2015. Virulent systemic feline calicivirus infection in a kitten. J Vet Clin 32: 445-448. https://doi.org/10.17555/jvc.2015.10.32.5.445
  35. Pesavento PA, Chang KO, Parker JS. 2008. Molecular virology of feline calicivirus. Vet Clin North Am Small Anim Pract 38: 775-786. https://doi.org/10.1016/j.cvsm.2008.03.002
  36. Radford AD, Addie D, Belak S, Boucraut-Baralon C, Egberink H, Frymus T, Gruffydd-Jones T, Hartmann K, Hosie MJ, Lloret A, Lutz H, Marsilio F, Pennisi MG, Thiry E, Truyen U, Horzinek MC. 2009. Feline calicivirus infection. ABCD guidelines on prevention and management. J Feline Med Surg 11: 556-564. https://doi.org/10.1016/j.jfms.2009.05.004
  37. Radford AD, Dawson S, Coyne KP, Porter CJ, Gaskell RM. 2006. The challenge for the next generation of feline calicivirus vaccines. Vet Microbiol 117: 14-18. https://doi.org/10.1016/j.vetmic.2006.04.004
  38. Radford AD, Willoughby K, Dawson S, McCracken C, Gaskell RM. 1999. The capsid gene of feline calicivirus contains linear B-cell epitopes in both variable and conserved regions. J Virol 73: 8496-8502. https://doi.org/10.1128/JVI.73.10.8496-8502.1999
  39. Sato Y, Ohe K, Murakami M, Fukuyama M, Furuhata K, Kishikawa S, Suzuki Y, Kiuchi A, Hara M, Ishikawa Y, Taneno A. 2002. Phylogenetic analysis of field isolates of feline calicivirus (FCV) in Japan by sequencing part of its capsid gene. Vet Res Commun 26: 205-119.
  40. Scansen BA, Wise AG, Kruger JM, Venta PJ, Maes RK. 2004. Evaluation of a p30 gene-based real-time reverse transcriptase polymerase chain reaction assay for detection of feline caliciviruses. J Vet Intern Med 18: 135-138. https://doi.org/10.1111/j.1939-1676.2004.tb00150.x
  41. Spiri AM. 2022. An update on feline calicivirus. Schweiz Arch Tierheilkd 164: 225-241. https://doi.org/10.17236/sat00346
  42. Sykes JE, Allen JL, Studdert VP, Browning GF. 2001. Detection of feline calicivirus, feline herpesvirus 1 and Chlamydia felis mucosal swabs by multiplex RT-PCR/PCR. Vet Microbiol 81: 95-108. https://doi.org/10.1016/S0378-1135(01)00340-6
  43. Vinje J, Estes MK, Esteves P, Green KY, Katayama K, Knowles NJ, L'Homme Y, Martella V, Vennema H, White PA, Ictv Report Consortium. 2019. ICTV Virus Taxonomy Profile: Caliciviridae. J Gen Virol 100: 1469-1470. https://doi.org/10.1099/jgv.0.001332
  44. Yang DK, Park YR, Yoo JY, Choi SS, Park Y, An S, Park J, Kim HJ, Kim J, Kim HH, Hyun BH. 2020. Biological and molecular characterization of feline caliciviruses isolated from cats in South Korea. Korean J Vet Res 60: 195-202. https://doi.org/10.14405/kjvr.2020.60.4.195
  45. Zhou L, Fu N, Ding L, Li Y, Huang J, Sha X, Zhou Q, Song X, Zhang B. 2021. Molecular characterization and cross-reactivity of feline calicivirus circulating in Southwestern China. Viruses 13: 1812.