Investigation of canine parvovirus occurrence in cats with clinical signs of feline panleukopenia in Slovakia – pilot study

Citarová, Alexandra; Mojžišová, Jana; Petroušková, Patrícia; Pelegrinová, Andrea; Kostičák, Maroš; Korytár, L’uboš; Prokeš, Marián; Vojtek, Boris; Ondrejková, Anna; Drážovská, Monika

doi:10.2478/jvetres-2024-0021

Abstract

Introduction

Feline panleukopenia is a contagious viral disease caused by the feline panleukopenia virus (FPV). A closely related pathogen is canine parvovirus (CPV), and amino acid substitutions in this virus allow it to acquire a feline host range. In feline hosts, the disease induced by CPV manifests with similar symptoms to those caused by FPV or milder ones, leading to its underdiagnosis. The aim of this study was to determine the presence of CPV type 2 (CPV-2) in cats with clinical symptoms of panleukopenia and to assess the use of commercial CPV antigen tests for the clinical diagnosis of FPV.

Material and Methods

Samples from 59 cats from central Slovakia were included in the study. Rectal swabs were collected and clinically tested for parvovirus infection using a commercial antigen test. Antigen-positive samples were confirmed by PCR targeting the viral VP2 gene. The sequences of the PCR products were established with the Sanger method.

Results

Of 59 samples, 23 were revealed to be positive for parvovirus infection by both antigen and PCR test (38.9%). Analysis with the National Center for Biotechnology Information BLASTn application showed 99.78–100% pairwise identity with FPV. The mortality rate of parvovirus-infected cats included in this study was 8.69% (2/23).

Conclusion

Although feline disease with CPV-2 was not confirmed, the CPV antigen test was able to detect FPV infection.

References

Addie D.D., Jarrett O., Simpson J., Thompson H.: Feline parvovirus in pedigree kittens. Vet Rec 1996, 138, 119, doi: 10.1136/vr.142.14.353.
Open DOI Search in Google Scholar Back to article
Ahmed N., Riaz A., Zubair Z., Saqib M., Ijaz S., Nawaz-Ul-Rehman M.S., Al-Qahtani A., Mubin M.: Molecular analysis of partial VP-2 gene amplified from rectal swab samples of diarrheic dogs in Pakistan confirms the circulation of canine parvovirus genetic variant CPV-2a and detects sequences of feline panleukopenia virus (FPV). Virol J 2018, 15, 1–7, doi: 10.1186/s12985-018-0958-y.
Open DOI Search in Google Scholar Back to article
Allison A.B., Kohler D.J., Fox K.A., Brown J.D., Gerhold R.W., Shearn-Boschler V.I., Dubovi E.J., Parrish C.R., Holmes E.C.: Frequent Cross-Species Transmission of Parvoviruses among Diverse Carnivore Hosts. J Virol 2013, 87, 2342–2347, doi: 10.1128/jvi.02428-12.
Open DOI Search in Google Scholar Back to article
Allison A.B., Kohler D.J., Ortega A., Hoover E.A., Grove D.M., Holmes E.C., Parrish C.R.: Host-specific parvovirus evolution in nature is recapitulated by in vitro adaptation to different carnivore species. PLoS Pathog 2014, 10, e1004586, doi: 10.1371/journal.ppat.1004475.
Open DOI Search in Google Scholar Back to article
Balboni A., Bassi F., Arcangeli S., Zobba R., Dedola C., Alberti A., Battilani M.: Molecular analysis of carnivore Protoparvovirus detected in white blood cells of naturally infected cats. BMC Vet Res 2018, 14, 41, doi: 10.1186/s12917-018-1356-9.
Open DOI Search in Google Scholar Back to article
Barrs V.R.: Feline panleukopenia: a re-emergent disease. Vet Clin Small Anim Pract 2019, 49, 651–670, doi: 10.1016/j.cvsm.2019.02.006.
Open DOI Search in Google Scholar Back to article
Byrne P., Beatty J.A., Šlapeta J., Corley S.W., Lyons R.E., McMichael L., Kyaw-Tanner M.T., Dung P.T., Decaro N., Meers J., Barrs V.R.: Shelter-housed cats show no evidence of faecal shedding of canine parvovirus DNA. Vet J 2018, 239, 54–58, doi: 10.1016/j.tvjl.2018.08.005.
Open DOI Search in Google Scholar Back to article
Citarová A., Mojžišová J., Vojtek B., Zákutná L., Drážovská M.: The findings of FPV, CPV-2a, CPV-2b and FCoV in cats with signs of feline panleukopenia. Berl Münch Tierärztl Wochenschr 2022, 135, 1–6, doi: 10.2376/1439-0299-2022-13.
Open DOI Search in Google Scholar Back to article
Clegg S.R., Coyne K.P., Dawson S., Spibey N., Gaskell R.M., Radford A.D.: Canine parvovirus in asymptomatic feline carriers. Vet Microbiol 2012, 157, 78–85, doi: 10.1016/j.vetmic.2011.12.024.
Open DOI Search in Google Scholar Back to article
Dawson S., Willoughby K., Gaskell R.M., Wood G., Chalmers W.S.: A field trial to assess the effect of vaccination against feline herpesvirus, feline calicivirus and feline panleucopenia virus in 6-week-old kittens. J Feline Med Surg 2001, 3, 17–22, doi: 10.1053/jfms.2000.0154.
Open DOI Search in Google Scholar Back to article
Decaro N., Desario C., Miccolupo A., Campolo M., Parisi A., Martella V., Amorisco F., Lucente M.S., Lavazza A., Buonavoglia C.: Genetic analysis of feline panleukopenia viruses from cats with gastroenteritis. J Gen Virol 2008, 89, 2290–2298, doi: 10.1099/vir.0.2008/001503-0.
Open DOI Search in Google Scholar Back to article
DiGangi B.A., Levy J.K., Griffin B., Reese M.J., Dingman P.A., Tucker S.J., Dubovi E.J.: Effects of maternally-derived antibodies on serologic responses to vaccination in kittens. J Feline Med Surg 2012, 14, 118–123, doi: 10.1177/1098612x11432239.
Open DOI Search in Google Scholar Back to article
Greene C.E. Addie D.D.: Feline Parvovirus Infections. In: Canine Viral Enteritis Infections Diseases of the Dog and Cat, edited by C.E. Greene, Saunders Elsevier, St. Louis, 2006, pp.78–88.
Search in Google Scholar Back to article
Hindle E., Findlay G.M.: Bacteriological studies on feline distemper. Proc R Soc Med 1933, 26, 197–204, doi: 10.1177/003591573302600301.
Open DOI Search in Google Scholar Back to article
Hu W., Xu X., Liu Q., Ji J., Kan Y., Yao L., Bi Y., Xie Q.: Molecular characterisation and genetic diversity of canine parvovirus type 2 prevalent in Central China. J Vet Res 2020, 64, 347–354, doi: 10.2478/jvetres-2020-0056.
Open DOI Search in Google Scholar Back to article
Hueffer K., Parrish C.R.: Parvovirus host range, cell tropism and evolution. Curr Opin Microbiol 2003, 6, 392–398, doi: 10.1016/s1369-5274(03)00083-3.
Open DOI Search in Google Scholar Back to article
Ikeda Y., Mochizuki M., Naito R., Nakamura K., Miyazawa T., Mikami T., Takahashi E.: Predominance of canine parvovirus (CPV) in unvaccinated cat populations and emergence of new antigenic types of CPVs in cats. Virol 2000, 278, 13–19, doi: 10.1006/viro.2000.0653.
Open DOI Search in Google Scholar Back to article
Ikeda Y., Nakamura K., Miyazawa T., Takahashi E., Mochizuki M.: Feline host range of canine parvovirus: recent emergence of new antigenic types in cats. Emerg Infect Dis 2002, 8, 341–346, doi: 10.3201/eid0804.010228.
Open DOI Search in Google Scholar Back to article
Isaya R., Ciccarelli S., Enache D., Specchi S., Pesaresi M., Ferri F., Porporato F., Auriemma E., Contiero B., Coppola L.M., Zini E.: Gastrointestinal ultrasonographic findings in cats with Feline panleukopenia: a case series. BMC Vet Res 2021, 17, 1–8, doi: 10.1186/s12917-020-02720-w.
Open DOI Search in Google Scholar Back to article
Isidan H., Turan T.: A comprehensive study of canine parvoviruses (Carnivore protoparvovirus 1, Carnivore bocaparvovirus 1 and 2) from shelter dogs in Turkey. Vet Med 2021, 66, 423–430, doi: 10.17221/130/2020-vetmed.
Open DOI Search in Google Scholar Back to article
Jacobson L.S., Janke K.J., Giacinti J., Weese J.S.: Diagnostic testing for feline panleukopenia in a shelter setting: a prospective, observational study. J Feline Med Surg 2021, 23, 1192–1199, doi: 10.1177/1098612x211005301.
Open DOI Search in Google Scholar Back to article
Martella V., Decaro N., Elia G., Buonavoglia C.: Surveillance activity for canine parvovirus in Italy. J Vet Med B Infect Dis Vet Public Health 2005, 52, 312–315, doi: 10.1111/j.1439-0450.2005.00875.x.
Open DOI Search in Google Scholar Back to article
Miranda C., Parrish C.R., Thompson G.: Canine parvovirus 2c infection in a cat with severe clinical disease. J Vet Diagn Investig 2014, 26, 462–464, doi: 10.1177/1040638714528502.
Open DOI Search in Google Scholar Back to article
Miranda C., Thompson G.: Canine parvovirus: the worldwide occurrence of antigenic variants. J Gen Virol 2016, 97, 2043–2057, doi: 10.1099/jgv.0.000540.
Open DOI Search in Google Scholar Back to article
Miranda C., Vieira M.J., Silva E., Carvalheira J., Parrish C.R., Thompson G.: Genetic Analysis of Feline Panleukopenia Virus Full-length VP 2 Gene in Domestic Cats Between 2006–2008 and 2012–2014, Portugal. Transbound Emerg Dis 2017, 64, 1178–1183, doi: 10.1111/tbed.12483.
Open DOI Search in Google Scholar Back to article
Mochizuki M., Harasawa R., Nakatani H.: Antigenic and genomic variabilities among recently prevalent parvoviruses of canine and feline origin in Japan. Vet Microbiol 1993, 38, 1–10, doi: 10.1016/0378-1135(93)90070-n.
Open DOI Search in Google Scholar Back to article
Mochizuki M., Horiuchi M., Hiragi H., San Gabriel M.C., Yasuda N., Uno T.: Isolation of canine parvovirus from a cat manifesting clinical signs of feline panleukopenia. J Clin Microbiol 1996, 34, 2101–2105, doi: 10.1128/jcm.34.9.2101-2105.1996.
Open DOI Search in Google Scholar Back to article
Mukhopadhyay H.K., Nookala M., Hangamani N.R., Sivaprakasam A., Antony P.X., Thanislass J., Srinivas M.V., Pillai R.M.: Molecular characterisation of parvoviruses from domestic cats reveals emergence of newer variants in India. J Feline Med Surg 2017, 19, 846–852, doi: 10.1177/1098612x16661375.
Open DOI Search in Google Scholar Back to article
Nandi S., Chidri S., Kumar M.: Molecular characterization and phylogenetic analysis of a canine parvovirus isolate in India. Vet Med 2009, 54, 483–490, doi: 10.17221/147/2009-vetmed.
Open DOI Search in Google Scholar Back to article
Parrish, C.R.: Host range relationships and the evolution of canine parvovirus. Vet Microbiol 1999, 69, 29–40, doi: 10.1016/S0378-1135(99)00084-x.
Open DOI Search in Google Scholar Back to article
Parrish C.R., O’Connell P.H., Evermann J.F., Carmichael L.E.: Natural variation of canine parvovirus. Science 1985, 230, 1046–1048, doi: 10.1126/science.4059921.
Open DOI Search in Google Scholar Back to article
Poulet H.: Alternative early life vaccination programs for companion animals. J Comp Pathol 2007, 137, S67–S71, doi: 10.1016/j.jcpa.2007.04.020.
Open DOI Search in Google Scholar Back to article
Sakulwira K., Vanapongtipagorn P., Theamboonlers A., Oraveerakul K., Poovorawan Y.: Prevalence of canine coronavirus and parvovirus infections in dogs with gastroenteritis in Thailand. Vet Med 2003, 48, 163–167, doi: 10.17221/5764-vetmed.
Open DOI Search in Google Scholar Back to article
Shackleton L.A., Parrish C.R., Truyen U., Holmes E.C.: High rate of viral evolution associated with the emergence of carnivore parvovirus. Proc Natl Acad Sci U S A 2005, 102, 379–384, doi: 10.1073/pnas.0406765102.
Open DOI Search in Google Scholar Back to article
Spitzer A.L., Parrish C.R., Maxwell I.H.: Tropic determinant for canine parvovirus and feline panleukopenia virus functions through the capsid protein VP2. J Gen Virol 1997, 78, 925–928, doi: 10.1099/0022-1317-78-4-925.
Open DOI Search in Google Scholar Back to article
Stucker K.M., Pagan I., Cifuente J.O., Kaelber J.T., Lillie T.D., Hafenstein S., Holmes E.C., Parrish C.R.: The role of evolutionary intermediates in the host adaptation of canine parvovirus. J Virol 2012, 86, 1514–1521, doi: 10.1128/jvi.06222-11.
Open DOI Search in Google Scholar Back to article
Tattersall P.: The evolution of parvovirus taxonomy. In: Parvoviruses, edited by J.R. Kerr, S.F. Cotmore, M.E. Bloom, R.M. Linden, C.R. Parrish, CRC Press, Boca Raton, 2006, pp. 5–14.
Search in Google Scholar Back to article
Truyen U., Evermann J.F., Vickler E., Parrish C.R.: Evolution of canine parvovirus involved loss and gain of the feline host range. Virol 1996, 215, 186–189, doi: 10.1006/viro.1996.0021.
Open DOI Search in Google Scholar Back to article
Truyen U., Gruenberg A., Chang S.F., Obermaier B., Veijalainen P., Parrish C.R.: Evolution of the feline subgroup parvoviruses and the control of canine host range. J Virol 1995, 69, 4702–4710, doi: 10.1128/jvi.69.8.4702-4710.1995.
Open DOI Search in Google Scholar Back to article
Voorhees I.E.H., Lee H., Allison A.B., Lopez-Astacio R., Goodman L.B., Oyesola O.O., Omobowale O., Fagbohun O., Dubivi E.J., Hafenstein S.L., Holmes E.C., Parrish C.R.: Limited intrahost diversity and background evolution accompany 40 years of canine parvovirus host adaptation and spread. J Virol 2019, 94, e01162–19, doi: 10.1128/jvi.01162-19.
Open DOI Search in Google Scholar Back to article