Abstract
The pet cat’s population and the number of viruses that infect them are increasing worldwide. Recently, feline chaphamaparvovirus (FeChPV, also called fechavirus) and feline bocaparvovirus (FBoV) infections, which are novel parvovirus species, have been reported in cats from different geographic regions. Here, we investigated FBoV 1–3 and FeChPVs in healthy cats in Turkey using PCR, where nuclear phosphoprotein 1 (NP1) is targeted for FBoV and NP for FeChPV. For this purpose, oropharygeal swabs were obtained from 70 healthy cats with different housing status from June 15 to December 1, 2020. After PCR screening tests, six out of 70 cats (5/47 shelter cats; 1/23 domestic cats) were found to be positive for FBOV, while two were positive for FeChPV (1/47 shelter cats; 1/23 domestic cats). No cat was found in which both viruses were detected. The nucleotide (nt) sequence comparison in the 310 base pair (bp) NP gene of the two FeChPVs identified in this study shared a high identity with each other (95.0% nt and 99% aa identities) and with previously reported FeChPVs (92.4–97.1% nt and 98.1–99.0% aa identities), including 313R/2019/ITA, 49E/2019/ITA, VRI_849, 284R/2019/ITA, and IDEXX-1. Here, the near-full length (1489 nt, 495 amino acids-aa) of the VP2 gene of the FechaV/Tur-2020/68 isolate obtained from the study was also sequenced. The nt and aa identity ratio of this isolate with other FeChPVs was 98.0–98.5%-96–96.5%, respectively. Sequences of the 465 bp NP1 gene of the six Turkish FBoV strains shared high identities with each other (99.6–100% nt and 99.3–100% aa identities) and with those of FBoV-2 strains (97.8–99.1% nt and 98.0–100% aa identities), including 16SY0701, 17CC0505-BoV2, HFXA-6, and POR1. All FBoVs detected in this study were classified as genotype 2, similar to the study conducted in Japan and Portugal. Here, the NS1 (partial), NP1, VP1 and VP2 gene of the FBoV-2/TUR/2020–14 strain obtained from the study were also sequenced and the nt and aa sequences showed high identities to the above-mentioned FBoV-2 strain/isolates (> 96%, except for the aa ratio of strain 16SY0701). In conclusion, this study shows that FBoV and FeChPV are present in healthy cats in Turkey, and these viruses can be detected from oropharyngeal swabs. Our findings contribute to further investigation of the prevalence, genotype distribution, and genetic diversity of Turkish FBoVs and FeChPVs, adding to the molecular epidemiology of FBoV and FeChPVs worldwide.
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References
Addie DD, Jarrett O (1992) A study of naturally occurring feline coronavirus infections in kittens. Vet Rec 130:133–137. https://doi.org/10.1136/vr.130.7.133
Baker KS, Leggett RM, Bexfield NH, Alston M, Daly G, Todd S, Tachedjian M, Holmes CE, Crameri S, Wang LF, Heeney JL, Suu-Ire R, Kellam P, Cunningham AA, Wood JL, Caccamo M, Murcia PR (2013) Metagenomic study of the viruses of African straw-coloured fruit bats: detection of a chiropteran poxvirus and isolation of a novel adenovirus. Virology 441:95–106. https://doi.org/10.1016/j.virol.2013.03.014
Bodewes R, Lapp S, Hahn K, Habierski A, Förster C, König M, Wohlsein P, Osterhaus AD, Baumgärtner W (2014) Novel canine bocavirus strain associated with severe enteritis in a dog litter. Vet Microbiol 174:1–8. https://doi.org/10.1016/j.vetmic.2014.08.025
Cheng W, Chen J, Xu Z, Yu J, Huang C, Jin M, Li H, Zhang M, Jin Y, Duan ZJ (2011) Phylogenetic and recombination analysis of human bocavirus 2. BMC Infect Dis 11:50. https://doi.org/10.1186/1471-2334-11-50
Chong R, Shi M, Grueber CE, Holmes EC, Hogg CJ, Belov K, Barrs VR (2019) Fecal viral diversity of captive and wild tasmanian devils characterized using virion-enriched metagenomics and metatranscriptomics. J Virol 93:e00205-e219. https://doi.org/10.1128/JVI.00205-19
Cotmore SF, Agbandje-McKenna M, Canuti M, Chiorini JA, Eis-Hubinger AM, Hughes J, Mietzsch M, Modha S, Ogliastro M, Pénzes JJ, Pintel DJ, Qiu J, Soderlund-Venermo M, Tattersall P, Tijssen P (2019) Ictv Report Consortium. ICTV virus taxonomy profile: Parvoviridae. J Gen Virol 100:367–368. https://doi.org/10.1099/jgv.0.001212
Di Martino B, Di Profio F, Melegari I, Sarchese V, Cafiero MA, Robetto S, Aste G, Lanave G, Marsilio F, Martella V (2016) A novel feline norovirus in diarrheic cats. Infect Genet Evol 38:132–137. https://doi.org/10.1016/j.meegid.2015.12.019
Di Martino B, Lanave G, Di Profio F, Melegari I, Marsilio F, Camero M, Catella C, Capozza P, Bányai K, Barrs VR, Buonavoglia C, Martella V (2020) Identification of feline calicivirus in cats with enteritis. Transbound Emerg Dis 67:2579–2588. https://doi.org/10.1111/tbed.13605
Di Profio F, Sarchese V, Palombieri A, Fruci P, Massirio I, Martella V, Fulvio M, Di Martino B (2021) Feline chaphamaparvovirus in cats with enteritis and upper respiratory tract disease. Transbound Emerg Dis. https://doi.org/10.1111/tbed.14032
Diakoudi G, Lanave G, Capozza P, Di Profio F, Melegari I, Di Martino B, Pennisi MG, Elia G, Cavalli A, Tempesta M, Camero M, Buonavoglia C, Bányai K, Martella V (2019) Identification of a novel parvovirus in domestic cats. Vet Microbiol 228:246–251. https://doi.org/10.1016/j.vetmic.2018.12.006
Fahsbender E, Altan E, Seguin MA, Young P, Estrada M, Leutenegger C, Delwart E (2019) Chapparvovirus DNA found in 4% of dogs with diarrhea. Viruses 11:398. https://doi.org/10.3390/v11050398
Garigliany M, Gilliaux G, Jolly S, Casanova T, Bayrou C, Gommeren K, Fett T, Mauroy A, Lévy E, Cassart D, Peeters D, Poncelet L, Desmecht D (2016) Feline panleukopenia virus in cerebral neurons of young and adult cats. BMC Vet Res 12:28. https://doi.org/10.1186/s12917-016-0657-0
Gerba CP (2009) Environmental Microbiology. In: Maier RN, Pepper IL, Gerba CP (eds) Environmentally transmitted pathogens, 2nd edn. Academic press, Massachusetts, pp 445–484. https://doi.org/10.1016/B978-0-12-370519-8.00022-5
Hoelzer K, Shackelton LA, Holmes EC, Parrish CR (2008) Within-host genetic diversity of endemic and emerging parvoviruses of dogs and cats. J Virol 82:11096–11105. https://doi.org/10.1128/JVI.01003-08
Jin Y, Cheng WX, Xu ZQ, Liu N, Yu JM, Li HY, Jin M, Li DD, Zhang Q, Duan ZJ (2011) High prevalence of human bocavirus 2 and its role in childhood acute gastroenteritis in China. J Clin Virol 52:251–253. https://doi.org/10.1016/j.jcv.2011.07.012
Kapoor A, Mehta N, Dubovi EJ, Simmonds P, Govindasamy L, Medina JL, Street C, Shields S, Lipkin WI (2012) Characterization of novel canine bocaviruses and their association with respiratory disease. J Gen Virol 93:341–346. https://doi.org/10.1099/vir.0.036624-0
Kapusinszky B, Ardeshir A, Mulvaney U, Deng X, Delwart E (2017) Case-control comparison of enteric viromes in captive rhesus macaques with acute or idiopathic chronic diarrhea. J Virol 91:e00952-e1017. https://doi.org/10.1128/JVI.00952-17
Koseki N, Teramoto S, Kaiho M, Gomi-Endo R, Yoshioka M, Takahashi Y, Nakayama T, Sawada H, Konno M, Ushijima H, Kikuta H, Ariga T, Ishiguro N (2012) Detection of human bocaviruses 1 to 4 from nasopharyngeal swab samples collected from patients with respiratory tract infections. J Clin Microbiol 50:2118–2121. https://doi.org/10.1128/JCM.00098-12
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Lau SK, Yeung HC, Li KS, Lam CS, Cai JP, Yuen MC, Wang M, Zheng BJ, Woo PC, Yuen KY (2017) Identification and genomic characterization of a novel rat bocavirus from brown rats in China. Infect Genet Evol 47:68–76. https://doi.org/10.1016/j.meegid.2016.11.014
Lau SKP, Woo PCY, Yeung HC, Teng JLL, Wu Y, Bai R, Fan RYY, Chan KH, Yuen KY (2012) Identification and characterization of bocaviruses in cats and dogs reveals a novel feline bocavirus and a novel genetic group of canine bocavirus. J Gen Virol 93:1573–1582. https://doi.org/10.1099/vir.0.042531-0
Li Y, Gordon E, Idle A, Altan E, Seguin MA, Estrada M, Deng X, Delwart E (2020) Virome of a feline outbreak of diarrhea and vomiting includes bocaviruses and a novel chapparvovirus. Viruses 12:506. https://doi.org/10.3390/v12050506
Lima DA, Cibulski SP, Tochetto C, Varela APM, Finkler F, Teixeira TF, Loiko MR, Cerva C, Junqueira DM, Mayer FQ, Roehe PM (2019) The intestinal virome of malabsorption syndrome-affected and unaffected broilers through shotgun metagenomics. Virus Res 261:9–20. https://doi.org/10.1016/j.virusres.2018.12.005
Lin MY, Chan HC, Chi H, Chiu SC, Nora-Krukle Z, Rasa-Dzelzkaleja S, Vilmane A, Murovska M, Lin JH, Liu HF (2020) Genetic diversity and phylogenetic analysis of human bocavirus 2 in pediatric patients with acute gastroenteritis in Taiwan. Int J Environ Res Public Health 17:1086. https://doi.org/10.3390/ijerph17031086
Liu C, Liu F, Li Z, Qu L, Liu D (2018) First report of feline bocavirus associated with severe enteritis of cat in Northeast China, 2015. J Vet Med Sci 80:731–735. https://doi.org/10.1292/jvms.17-0444
Liu X, Wang H, Liu X, Li Y, Chen J, Zhang J, Wang X, Shen S, Wang H, Deng F, Wang M, Guan W, Hu Z (2020) Genomic and transcriptional analyses of novel parvoviruses identified from dead peafowl. Virology 539:80–91. https://doi.org/10.1016/j.virol.2019.10.013
Manteufel J, Truyen U (2008) Animal bocaviruses: a brief review. Intervirology 51:328–334. https://doi.org/10.1159/000173734
Meriluoto M, Hedman L, Tanner L, Simell V, Mäkinen M, Simell S, Mykkänen J, Korpelainen J, Ruuskanen O, Ilonen J, Knip M, Simell O, Hedman K, Söderlund-Venermo M (2012) Association of human bocavirus 1 infection with respiratory disease in childhood follow-up study, Finland. Emerg Infect Dis 18:264–271. https://doi.org/10.3201/eid1802.111293
Miranda C, Thompson G (2016) Canine parvovirus: the worldwide occurrence of antigenic variants. J Gen Virol 97:2043–2057. https://doi.org/10.1099/jgv.0.000540
Ng TF, Mesquita JR, Nascimento MS, Kondov NO, Wong W, Reuter G, Knowles NJ, Vega E, Esona MD, Deng X, Vinjé J, Delwart E (2014) Feline fecal virome reveals novel and prevalent enteric viruses. Vet Microbiol 171:102–111. https://doi.org/10.1016/j.vetmic.2014.04.005
Palinski RM, Mitra N, Hause BM (2016) Discovery of a novel Parvovirinae virus, porcine parvovirus 7, by metagenomic sequencing of porcine rectal swabs. Virus Genes 52:564–567. https://doi.org/10.1007/s11262-016-1322-1
Parrish CR (1995) Pathogenesis of feline panleukopenia virus and canine parvovirus. Baillieres Clin Haematol 8:57–71. https://doi.org/10.1016/s0950-3536(05)80232-x
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. https://doi.org/10.1146/annurev.micro.59.030804.121059
Pénzes JJ, Söderlund-Venermo M, Canuti M, Eis-Hübinger AM, Hughes J, Cotmore SF, Harrach B (2020) Reorganizing the family Parvoviridae: a revised taxonomy independent of the canonical approach based on host association. Arch Virol 165:2133–2146. https://doi.org/10.1007/s00705-020-04632-4
Pfankuche VM, Bodewes R, Hahn K, Puff C, Beineke A, Habierski A, Osterhaus AD, Baumgärtner W (2016) Porcine bocavirus infection associated with encephalomyelitis in a pig, Germany. Emerg Infect Dis 22:1310–1312. https://doi.org/10.3201/eid2207.152049
Piewbang C, Kasantikul T, Pringproa K, Techangamsuwan S (2019) Feline bocavirus-1 associated with outbreaks of hemorrhagic enteritis in household cats: potential first evidence of a pathological role, viral tropism and natural genetic recombination. Sci Rep 9:16367. https://doi.org/10.1038/s41598-019-52902-2
Priestnall SL, Mitchell JA, Walker CA, Erles K, Brownlie J (2014) New and emerging pathogens in canine infectious respiratory disease. Vet Pathol 51:492–504. https://doi.org/10.1177/0300985813511130
Qiu J, Cheng F, Johnson FB, Pintel D (2007) The transcription profile of the bocavirus bovine parvovirus is unlike those of previously characterized parvoviruses. J Virol 81:12080–12085. https://doi.org/10.1128/JVI.00815-07
Reuter G, Boros Á, Delwart E, Pankovics P (2014) Novel circular single-stranded DNA virus from turkey faeces. Arch Virol 159:2161–2164. https://doi.org/10.1007/s00705-014-2025-3
Sabshin SJ, Levy JK, Tupler T, Tucker SJ, Greiner EC, Leutenegger CM (2012) Enteropathogens identified in cats entering a Florida animal shelter with normal feces or diarrhea. J Am Vet Med Assoc 241:331–337. https://doi.org/10.2460/javma.241.3.331
Soma T, Ogata M, Ohta K, Yamashita R, Sasai K (2020) Prevalence of astrovirus and parvovirus in Japanese domestic cats. J Vet Med Sci 82:1243–1246. https://doi.org/10.1292/jvms.20-0205
Stuetzer B, Hartmann K (2014) Feline parvovirus infection and associated diseases. Vet J 201:150–155. https://doi.org/10.1016/j.tvjl.2014.05.027
Takano T, Takadate Y, Doki T, Hohdatsu T (2016) Genetic characterization of feline bocavirus detected in cats in Japan. Arch Virol 161:2825–2825. https://doi.org/10.1007/s00705-016-2972-y
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
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. https://doi.org/10.1093/nar/22.22.4673
Truyen U, Addie D, Belák S, Boucraut-Baralon C, Egberink H, Frymus T, Gruffydd-Jones T, Hartmann K, Hosie MJ, Lloret A, Lutz H, Marsilio F, Pennisi MG, Radford AD, Thiry E, Horzinek MC (2009) ABCD guidelines on prevention and management. J Feline Med Surg 11:538–546. https://doi.org/10.1016/j.jfms.2009.05.002
Verbeke V, Reynders M, Floré K, Vandewal W, Debulpaep S, Sauer K, Cardoen F, Padalko E (2019) Human bocavirus infection in Belgian children with respiratory tract disease. Arch Virol 164:2919–2930. https://doi.org/10.1007/s00705-019-04396-6
Wang Y, Yang S, Liu D, Zhou C, Li W, Lin Y, Wang X, Shen Q, Wang H, Li C, Zong M, Ding Y, Song Q, Deng X, Qi D, Zhang W, Delwart E (2019) The fecal virome of red-crowned cranes. Arch Virol 164:3–16. https://doi.org/10.1007/s00705-018-4037-x
Williams SH, Che X, Garcia JA, Klena JD, Lee B, Muller D, Ulrich W, Corrigan RM, Nichol S, Jain K, Lipkin WI (2018) Viral diversity of house mice in New York City. Mbio 9:e01354-e1417. https://doi.org/10.1128/mBio.01354-17
Yang S, Liu Z, Wang Y, Li W, Fu X, Lin Y, Shen Q, Wang X, Wang H, Zhang W (2016) A novel rodent Chapparvovirus in feces of wild rats. Virol J 13:133. https://doi.org/10.1186/s12985-016-0589-0
Yi S, Niu J, Wang H, Dong G, Zhao Y, Dong H, Guo Y, Wang K, Hu G (2018) Detection and genetic characterization of feline bocavirus in Northeast China. Virol J 15:125. https://doi.org/10.1186/s12985-018-1034-3
Zhang W, Li L, Deng X, Kapusinszky B, Pesavento PA, Delwart E (2014) Faecal virome of cats in an animal shelter. J Gen Virol 95:2553–2564. https://doi.org/10.1099/vir.0.069674-0
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. https://doi.org/10.1007/s00705-019-04394-8
Ziemele I, Xu M, Vilmane A, Rasa-Dzelzkaleja S, Hedman L, Hedman K, Söderlund-Venermo M, Nora-Krukle Z, Murovska M, Gardovska D (2019) Acute human bocavirus 1 infection in child with life-threatening bilateral bronchiolitis and right-sided pneumonia: a case report. J Med Case Reports 13:290. https://doi.org/10.1186/s13256-019-2222-5
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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by HA, and KCS. The first draft of the manuscript was written by HA and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Abayli, H., Can-Sahna, K. First detection of feline bocaparvovirus 2 and feline chaphamaparvovirus in healthy cats in Turkey. Vet Res Commun 46, 127–136 (2022). https://doi.org/10.1007/s11259-021-09836-w
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DOI: https://doi.org/10.1007/s11259-021-09836-w