Prevalence of feline panleukopenia (FPL) in domestic cats: A systematic meta-analysis https://doi.org/10.12982/VIS.2026.001
Article Sidebar
Main Article Content
Abstract
Feline panleukopenia (FPL) is a fatal, transmissible disease in cats and other members of the Felidae family. A meta-analysis was performed to determine the worldwide prevalence of FPL infections in domesticated cats. This meta-analysis was finalized according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. After a competent search, data extraction and identification of qualified articles were performed. Data were analyzed using a specific software program for meta-analysis, and the results included weight, effect size, publication bias, and heterogeneity. A total of 5820 domesticated cats from 36 accepted studies were investigated for FPLV infections. Of all, 2928 cats were found positive for FPLV infection, with a prevalence of 50.30%. The prevalence of FPL in cats varied significantly between countries (p < 0.001). The highest prevalence was recorded in Germany (15.81%), whereas the lowest prevalence was recorded in Korea (2 %). The Z-values were -10.935 (P = 0.000) and -2.903 (P = 0.004) for fixed and random effects, respectively. The Q-value (948.37), I-squared (96.309), and P (0.000) were the final heterogeneity variables. Moreover, the Tau-squared value was 0.888 with an SE of 0.316. Egger’s linear regression test for asymmetry did not indicate publication bias (intercept: -0.75382; 95% CI: -4.63013 to 3.122; t-value:0.395; p=0.695). The classic fail-safe N proposed that 1031 missing studies were required to conclude that the study result was significant (p = 0.000). The results of this meta-analysis indicated a high global prevalence of FPLV infection in cats. Wide variation in the prevalence of FPLV infection among countries may indicate the failure of preventive programs. The results also necessitate more attention to associated risk factors and strict control measures.
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
Publishing an article with open access in Veterinary Integrative Sciences leaves the copyright with the author. The article is published under the Creative Commons Attribution License 4.0 (CC-BY 4.0), which allows users to read, copy, distribute and make derivative works from the material, as long as the author of the original work is cited.
References
Abayli, H., Can-Sahna, K., Ozbek, R., Aslan, O., Tonbak, S., Bulut, H., 2021. Detection and molecular characterisation of feline viruses from swab samples. Acta Vet. Hung. 69, 194-203.
Abd-Eldaim, M., Beall, M.J., Kennedy, M.A., 2009. Detection of feline panleukopenia virus using a commercial ELISA for canine parvovirus. Vet. Ther. 10, E1-E6.
Addie, D.D., Boucraut-Baralon, C., Egberink, H., Frymus, T., Gruffydd-Jones, T., Hartmann, K., Horzinek, M.C., Hosie, M.J., Lloret, A., Lutz, H., 2015. Disinfectant choices in veterinary practices, shelters and households: ABCD guidelines on safe and effective disinfection for feline environments. J. Feline Med. Surg. 17, 594-605.
Aeffner, F., Ulrich, R., Schulze-Rückamp, L., Beineke, A., 2006. Cerebellar hypoplasia in three sibling cats after intrauterine or early postnatal parvovirus infection. DTW. Deutsche Tierarztliche Wochenschrift. 113, 403-406.
Amoroso, M.G., Serra, F., Miletti, G., Cardillo, L., de Martinis, C., Marati, L., Alfano, F., Ferrara, G., Pagnini, U., De Carlo, E., 2022. A retrospective study of viral molecular prevalences in cats in Southern Italy (Campania Region). Viruses. 14, 2583.
Awad, R.A., Khalil, W.K., Attallah, A.G., 2018. Epidemiology and diagnosis of feline panleukopenia virus in Egypt: Clinical and molecular diagnosis in cats. Vet. World. 11, 578.
Balboni, A., Bassi, F., De Arcangeli, S., Zobba, R., Dedola, C., Alberti, A., Battilani, M., 2018. Molecular analysis of carnivore Protoparvovirus detected in white blood cells of naturally infected cats. BMC Vet. Res. 14, 1-10.
Barrs, V.R., 2019. Feline panleukopenia: a re-emergent disease. Vet. Clin. N. Am. Small. Anim. Pract. 49, 651-670.
Bayati, H.A.M.A., 2016. Detection of feline parvovirus (FPV) from cats infected with enteritis using rapid test and polymerase chain reaction in Iraq. Kufa J. Vet. Med. Sci. 7.
Begg, C.B., Mazumdar, M., 1994. Operating characteristics of a rank correlation test for publication bias. Biom. 50, 1088-1101.
Bezerra, J.A.B., Limeira, C.H., de Miranda Maranhão, A.C.P., de Paula Antunes, J.M.A., de Azevedo, S.S., 2024. Global seroprevalence and factors associated with seropositivity for feline immunodeficiency virus (FIV) in cats: a systematic review and meta-analysis. Prev. Vet. Med. 106315.
Borenstein, M., Hedges, L.V., Higgins, J.P., Rothstein, H.R., 2021. Introduction to meta-analysis. John Wiley & Sons, New Jersey.
Bukar-Kolo, Y.M., Buba, E., Igbokwe, I.O., Egwu, G.O., 2018. Prevalence of feline panleukopenia virus in pet and stray cats and associated risk factors in Maiduguri, Nigeria. Alexandria. J. Vet. Sci. 59.
Cao, L., Chen, Q., Ye, Z., Li, J., Zhang, Y., Wang, Y., Chen, L., Chen, Z., Jin, J., Cao, S., 2023. Epidemiological survey of feline viral infectious diseases in China from 2018 to 2020. Anim. Res. One Health. 1, 233–241.
Chowdhury, Q.M.K., Alam, S., Chowdhury, M.S.R., Hasan, M., Uddin, M.B., Hossain, M.M., Islam, M.R., Rahman, M.M., Rahman, M.M., 2021. First molecular characterization and phylogenetic analysis of the VP2 gene of feline panleukopenia virus in Bangladesh. Arch. Virol. 166, 2273-2278.
Christensen, J., Tattersall, P., 2002. Parvovirus initiator protein NS1 and RPA coordinate replication fork progression in a reconstituted DNA replication system. J. Virol. 76, 6518-6531.
Cotmore, S.F., Agbandje-McKenna, M., Canuti, M., Chiorini, J.A., Eis-Hubinger, A.M., Hughes, J., Mietzsch, M., Modha, S., Ogliastro, M., Pénzes, J.J., 2019. ICTV virus taxonomy profile: Parvoviridae. J. Gen. Virol. 100, 367-368.
Dall’Ara, P., Labriola, C., Sala, E., Spada, E., Magistrelli, S., Lauzi, S., 2019. Prevalence of serum antibody titres against feline panleukopenia, herpesvirus and calicivirus infections in stray cats of Milan, Italy. Prev. Vet. Med. 167, 32-38.
Day, M.J., Horzinek, M., Schultz, R., Squires, R., 2016. WSAVA Guidelines for the vaccination of dogs and cats. The J. Small Anim. Pract. 57, E1.
DiGangi, B.A., Levy, J.K., Griffin, B., McGorray, S.P., Dubovi, E.J., Dingman, P.A., Tucker, S.J., 2012. Prevalence of serum antibody titers against feline panleukopenia virus, feline herpesvirus 1, and feline calicivirus in cats entering a Florida animal shelter. J. Am. Vet. Med. Assoc. 241, 1320-1325.
Dishow, M.H., Alsarhan, Q.T., Al-Naqshabendy, A.A., 2023. Prevalence of feline panleukopenia virus in cats in Duhok Province, Iraq. Egyp. J. Vet. Sci. 54, 917-926.
Duffield, T.F., Rabiee, A.R., Lean, I.J., 2008. A meta-analysis of the impact of monensin in lactating dairy cattle. Part 1. Metabolic effects. J. Dairy Sci. 91, 1334-1346.
Duval, S., 2005. The trim and fill method, In: Rothstein, H.R., Sutton, A.J., Borenstein, M. (Eds.), Publication bias in meta‐analysis: prevention, assessment and adjustments. John Wiley & Sons, Hoboken, pp. 127-144.
Duval, S., Tweedie, R., 2000. Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biom. 56, 455-463.
Egger, M., Davey Smith, G., Schneider, M., Minder, C., 1997. Bias in meta-analysis detected by a simple, graphical test. BMJ. 315, 629-634.
Foley, J., Orgad, U., Hirsh, D., Poland, A., Pedersen, N., 1999. Outbreak of fatal salmonellosis in cats following use of a high-titer modified-live panleukopenia virus vaccine. J. Am. Vet. Med. Assoc. 214, 67-70, 43.
Garigliany, M., Gilliaux, G., Jolly, S., Casanova, T., Bayrou, C., Gommeren, K., Fett, T., Mauroy, A., Lévy, E., Cassart, D., 2016. Feline panleukopenia virus in cerebral neurons of young and adult cats. BMC Vet. Res. 12, 1-9.
Goto, H., Horimoto, M., Shimizu, K., Hiraga, T., Matsuoka, T., Nakano, T., Morohoshi, Y., Maejima, K., Urano, T., 1981. Prevalence of feline viral antibodies in random-souce laboratory cats. Exp. Anim. 30, 283-290.
Govindasamy, L., Hueffer, K., Parrish, C.R., Agbandje-McKenna, M., 2003. Structures of host range-controlling regions of the capsids of canine and feline parvoviruses and mutants. J. Virol. 77, 12211-12221.
Haidich, A.B., 2010. Meta-analysis in medical research. Hippokratia. 14, 29-37.
Hak, T., van Rhee, H., Suurmond, R., 2016. How to interpret results of meta-analysis. Available online: https://www.erim.eur.nl/fileadmin/erim_content/images/meta-essentials/How_to_interpret_results_of_meta-analysis_1.4.pdf.
Hasırcıoglu, S., Aslım, H.P., Kale, M., Bulut, O., Koçlu, O., Orta, Y.S., 2023. Molecular characterization of carnivore protoparvovirus strains circulating in cats in Turkey. Pesquisa Veterinária Brasileira. 43, e07178.
Haynes, S., Holloway, S., 2012. Identification of parvovirus in the bone marrow of eight cats. Aust. Vet. J. 90, 136-139.
Higgins, J.P., Altman, D.G., Gøtzsche, P.C., Jüni, P., Moher, D., Oxman, A.D., Savovic, J., Schulz, K.F., Weeks, L., Sterne, J.A., 2011. The Cochrane Collaboration's tool for assessing risk of bias in randomised trials. BMJ. 343, d5928.
Higgins, J.P.T., Thomas, J., Chandler, J., Cumpston, M., Li, T., Page, M.J., Welch, V.A., 2019. Cochrane handbook for systematic reviews of interventions, 2nd Edition. John Wiley & Sons, Chichester.
Hu, T., Zhang, H., Zhang, X., Hong, X., Zhang, T., 2024. Prevalence and risk factors associated with Feline Infectious Peritonitis (FIP) in Mainland China between 2008 and 2023: a systematic review and meta-analysis. Anim. 14, 1220.
Huedo-Medina, T.B., Sánchez-Meca, J., Marín-Martínez, F., Botella, J., 2006. Assessing heterogeneity in meta-analysis: Q statistic or I2 index? Psychol. Methods. 11, 193-206.
Islam, M., Rahman, M., Rony, S., Uddin, M., Rahman, A., 2010. Antigenic detection of feline panleukopenia virus in local breed cats at Tangail district in Bangladesh. Int. J. Bioresearch. 2, 25-28.
Jacobson, L.S., Janke, K.J., Giacinti, J., Weese, J.S., 2021. Diagnostic testing for feline panleukopenia in a shelter setting: a prospective, observational study. J. Feline Med. Surg. 23, 1192-1199.
Jacobson, L.S., Janke, K.J., Ha, K., Giacinti, J.A., Weese, J.S., 2022. Feline panleukopenia virus DNA shedding following modified live virus vaccination in a shelter setting. Vet. J. 279, 105783.
Joober, R., Schmitz, N., Annable, L., Boksa, P., 2012. Publication bias: what are the challenges and can they be overcome?. J. Psychiatry. Neurosci. 149-152.
Kabir, A., Habib, T., Chouhan, C.S., Hassan, J., Rahman, A.A., Nazir, K.N.H., 2023. Epidemiology and molecular characterization of Feline panleukopenia virus from suspected domestic cats in selected Bangladesh regions. Plos One. 18, e0282559.
Kim, S., Lee, K., Kim, H., Park, H., 2013. Prevalence of feline panleukopenia virus in stray and household cats in Seoul, Korea. J. Vet. Clin. 30, 333-338.
Koç, B.T., Akkutay-Yoldar, Z., Ülgenalp, O., Oğuzoğlu, T.Ç., 2018. A statistical assessment study on feline infectious peritonitis (FIP) and feline panleukopenia virus (FPV). In 2nd International Congress on Advances in Bioscience and Biotechnology, Podgorica, Montenegro, 26-30 June 2018, pp. 36-38.
Kruse, B., Unterer, S., Horlacher, K., Sauter‐Louis, C., Hartmann, K., 2010. Prognostic factors in cats with feline panleukopenia. J. Vet. Intern. Med. 24, 1271-1276.
Levy, J., Crawford, P., Lappin, M., Dubovi, E., Levy, M., Alleman, R., Tucker, S., Clifford, E., 2008. Infectious diseases of dogs and cats on Isabela Island, Galapagos. J. Vet. Intern. Med. 22, 60-65.
Light, R., Pillemer, D.B., 1986. Summing up: the science of reviewing research. Harvard University Press, Cambridge, MA.
Litster, A., Benjanirut, C., 2014. Case series of feline panleukopenia virus in an animal shelter. J. Feline Med. Surg. 16, 346-353.
Liu, M., Li, M., Ma, C., Shi, C., 2020. Detection of canine parvovirus and feline panleukopenia virus in fecal samples by strand exchange amplification. J. Vet. Diagn. Invest. 32, 880-886.
Ludwick, K., Clymer, J.W., 2019. Comparative meta-analysis of feline leukemia virus and feline immunodeficiency virus seroprevalence correlated with GDP per capita around the globe. Res. Vet. Sci. 125, 89-93.
Mende, K., Stuetzer, B., Truyen, U., Hartmann, K., 2014. Evaluation of an in-house dot enzyme-linked immunosorbent assay to detect antibodies against feline panleukopenia virus. J. Feline Med. Surg. 16, 805-811.
Miranda, C., Vieira, M., Silva, E., Carvalheira, J., Parrish, C., Thompson, G., 2017. Genetic analysis of feline panleukopenia virus full‐length VP 2 Gene in domestic cats between 2006–2008 and 2012–2014, Portugal. Transbound. Emerg. Dis. 64, 1178-1183.
Moher, D., Liberati, A., Tetzlaff, J., Altman, D.G., Group, P., 2010. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int. J. Surg. 8, 336-341.
Moher, D., Liberati, A., Tetzlaff, J., Altman, D.G., PRISMA Group, 2009. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med. 6(7), e1000097.
Mosallanejad, B., Avizeh, R., Ghorbanpoor Najafabadi, M., 2009. Antigenic detection of Feline Panleukopenia virus (FPV) in diarrhoeic companion cats in Ahvaz area. Iran. J. Vet. Res. 10, 289-293.
Möstl, K., Egberink, H., Addie, D., Frymus, T., Boucraut-Baralon, C., Truyen, U., Hartmann, K., Lutz, H., Gruffydd-Jones, T., Radford, A.D., 2013. Prevention of infectious diseases in cat shelters: ABCD guidelines. J. Feline Med. Surg. 15, 546-554.
Neuerer, F.F., Horlacher, K., Truyen, U., Hartmann, K., 2008. Comparison of different in-house test systems to detect parvovirus in faeces of cats. J. Feline. Med. Surg. 10, 247-251.
Paris, J.K., Wills, S., Balzer, H.J., Shaw, D.J., Gunn-Moore, D.A., 2014. Enteropathogen co-infection in UK cats with diarrhoea. BMC Vet. Res. 10, 1-11.
Parrish, C.R., 1995. 3 Pathogenesis of feline panleukopenia virus and canine parvovirus. Baillieres Clin. Haematol. 8, 57-71.
Parthiban, M., Aarthi, K.S., Balagangatharathilagar, M., Kumanan, K., 2014. Evidence of feline panleukopenia infection in cats in India. Virus. Dis. 25, 497-499.
Peters, J.L., Sutton, A.J., Jones, D.R., Abrams, K.R., Rushton, L., 2006. Comparison of two methods to detect publication bias in meta-analysis. JAMA. 295, 676-680.
Peters, J.L., Sutton, A.J., Jones, D.R., Abrams, K.R., Rushton, L., 2007. Performance of the trim and fill method in the presence of publication bias and between-study heterogeneity. Stat. Med. 26, 4544-4562.
Raheena, K.P., Priya, P., Mani, B.K., Mini, M., Pillai, U.N., 2017. Comparison of different diagnostic test to detect feline panleukopenia virus among cats in Kerala, India. Indian. J. Anim. Res. 51, 347-349.
Reed, A.P., Jones, E.V., Miller, T.J., 1988. Nucleotide sequence and genome organization of canine parvovirus. J. Virol. 62, 266-276.
Rehme, T., Hartmann, K., Truyen, U., Zablotski, Y., Bergmann, M., 2022b. Feline panleukopenia outbreaks and risk factors in cats in animal shelters. Viruses. 14, 1248.
Riya, B., Rathish, R., Deepa, P., John, L., Janus, A., Vijaykumar, K., 2020. Clinical manifestations in cats with feline panleukopenia. J. Vet. Anim. Sci. 51, 97-100.
Rosenthal, R., 1979a. The file drawer problem and tolerance for null results. Psychol. Bull. 86, 638-641.
Rothstein, H.R., Sutton, A.J., Borenstein, M., 2005. Publication bias in meta-analysis, In: Rothstein, H.R., Sutton, A.J., Borenstein, M. (Eds.), Publication bias in meta‐analysis. John Wiley & Sons, Hoboken, pp. 1-7.
Rücker, G., Schwarzer, G., Carpenter, J., 2008. Arcsine test for publication bias in meta-analyses with binary outcomes. Stat. Med. 27, 746-763.
Schulz, K.F., Chalmers, I., Hayes, R.J., Altman, D.G., 1995. Empirical evidence of bias. Dimensions of methodological quality associated with estimates of treatment effects in controlled trials. JAMA. 273, 408-412.
Sibel, G., Avdatek, K., 2016. A serological investigation for feline panleukopenia virus in Cats in Afyonkarahisar. Kocatepe Vet. J. 9, 165-170.
Sterne, J.A., Gavaghan, D., Egger, M., 2000. Publication and related bias in meta-analysis: power of statistical tests and prevalence in the literature. J. Clin. Epidemiol. 53, 1119-1129.
Stuetzer, B., Hartmann, K., 2014. Feline parvovirus infection and associated diseases. Vet. J. 201, 150-155.
Suntz, M., Failing, K., Hecht, W., Schwartz, D., Reinacher, M., 2010. High prevalence of non-productive FeLV infection in necropsied cats and significant association with pathological findings. Vet. Immunol. Immunopathol. 136, 71-80.
Sutton, A.J., Duval, S.J., Tweedie, R.L., Abrams, K.R., Jones, D.R., 2000. Empirical assessment of effect of publication bias on meta-analyses. BMJ. 320, 1574-1577.
Tajbiur-Abir, M., 2022. Identification of risk factors associated with feline panleukopenia of cats in CVASU and TTPHRC. Chattogram Veterinary and Animal Sciences University. Khulshi, Chattogram, Bangladesh.
Terrin, N., Schmid, C.H., Lau, J., Olkin, I., 2003. Adjusting for publication bias in the presence of heterogeneity. Stat. Med. 22, 2113-2126.
Thompson, S.G., 1994. Why sources of heterogeneity in meta-analysis should be investigated. BMJ. 309, 1351-1355.
Truyen, U., Agbandje, M., Parrish, C.R., 1994. Characterization of the feline host range and a specific epitope of feline panleukopenia virus. Virol. 200, 494-503.
Truyen, U., Parrish, C., 1992. Canine and feline host ranges of canine parvovirus and feline panleukopenia virus: distinct host cell tropisms of each virus in vitro and in vivo. J. Virol. 66, 5399-5408.
Uhart, M.M., Rago, M.V., Marull, C.A., Ferreyra, H.d.V., Pereira, J.A., 2012. Exposure to selected pathogens in Geoffroy’s cats and domestic carnivores from central Argentina. J. Wildl. Dis. 48, 899-909.
Uttenthal, Å., Lund, E., Hansen, M., 1999. Mink enteritis parvovirus: Stability of virus kept under outdoor conditions. APMIS. 107, 353-358.
Vobis, M., D’Haese, J., Mehlhorn, H., Mencke, N., 2003. Evidence of horizontal transmission of feline leukemia virus by the cat flea (Ctenocephalides felis). Parasitol. Res. 91, 467-470.
Xue, H., Hu, C., Ma, H., Song, Y., Zhu, K., Fu, J., Mu, B., Gao, X., 2023a. Isolation of feline panleukopenia virus from Yanji of China and molecular epidemiology from 2021 to 2022. J. Vet. Sci. 24, e29.
Xue, H., Liang, Y., Gao, X., Song, Y., Zhu, K., Yang, M., Hao, J., Ma, H., Yu, K., 2023b. Development and application of nanoPCR method for detection of feline Panleukopenia virus. Vet. Sci. 10, 440.
Yan, M., Shang, J., Zhang, X., Wu, S., Wang, C., Wang, Z., Luo, G., Yi, L., Shan, X., Cheng, Y., Feng, E., 2023. The establishment and application of a dual Nano-PCR detection method for feline calicivirus and feline herpesvirus type I. Front. Microbiol. 14, 1285268.
Yang, D.K., Park, Y.R., Kim, E., Lee, H.J., Shin, K.S., Kim, J.H., Lee, K., Hyun, B.H., 2022. Incidence and sero-surveillance of feline viruses in Korean cats residing in Gyeonggi-do. Korean J. Vet. Res. 62, e24.
Yang, D.K., Park, Y., Park, Y.R., Yoo, J.Y., An, S., Park, J., Hyun, B.H., 2021. Expression of the VP2 protein of feline panleukopenia virus in insect cells and use thereof in a hemagglutination inhibition assay. Korean J. Vet. Res. 61, e19.
Zenad, M.M., Radhy, A.M., 2020. Clinical, serological and antigenic study of feline panleukopenia virus in cats in Baghdad, Iraq. Iraqi. J. Vet. 34.
Zhang, Q., Niu, J., Yi, S., Dong, G., Yu, D., Guo, Y., Huang, H., Hu, G., 2019. Development and application of a multiplex PCR method for the simultaneous detection and differentiation of feline panleukopenia virus, feline bocavirus, and feline astrovirus. Arch. Virol. 164, 2761-2768.