Molecular characterization of canine astrovirus, vesivirus and circovirus, isolated from diarrheic dogs in Turkey

Document Type : Full paper (Original article)

Authors

Virology Department, Faculty of Veterinary Medicine, Sivas Cumhuriyet University, 58140, Sivas, Turkey

Abstract

Background: Canine astrovirus (CAstV) has been considered the primary cause of gastroenteritis in young animals worldwide, while canine vesivirus (CVeV) and canine circovirus (CCiV) are occasionally reported. Aims: This study aimed to investigate the existence and molecular characteristics for these three viruses in Turkey. Methods: Faecal samples from 150 shelter dogs with gastrointestinal problems (127 adults and 23 puppies) were collected and examined by reverse transcription-polymerase chain reaction (RT-PCR) analysis based on the partial sequence of RdRp gene (ORF1b) for CAstV, ORF2 gene of CVeV and capsid protein (Cap) and replication associated protein (Rep) gene of CCiV. Randomly selected positive samples were submitted to sequencing and molecular analyses were conducted based on partial sequences. Results: It was found that 66% (99/150) of diarrhoeic dogs were positive for CAstV, 3.33% (5/150) for CVeV, and 6% (9/150) for CCiV. Four sub-genotypes for CAstV and two sub-genotypes for CVeV were suggested according to molecular analyses. The phylogenetic relationship of CCiV with other strains obtained from various areas was further demonstrated. Conclusion: This study emphasizes the importance of emerging viruses for canids, classification of them and their proportional contribution in gastroenteritis cases. We concluded that astrovirus infection must be considered as the major cause of diarrhea in dogs; However, the prevalences of vesivirus and circovirus were relatively low in cases makes them less important in Turkey.

Keywords

Main Subjects


Anderson, A; Hartmann, K; Leutenegger, CM; Proksch, AL; Mueller, RS and Unterer, S (2017). Role of Canine circovirus in dogs with acute haemorrhagic diarrhoea. Vet. Rec., 180: 542.
Appleton, H and Higgins, PG (1975). Viruses and gastro-enteritis in infants. Lancet. 1: 1297.
Bexton, S; Wiersma, LC; Getu, S; van Run, PR; Verjans, GMGM; Schipper, D; Schapendonk, CME; Bodewes, R; Oldroyd, L; Haagmans, BL; Koopmans, MMP and Smits, SL (2015). Detection of circovirus in foxes with Meningoencephalitis, United Kingdom, 2009-2013. Emerg. Infect. Dis., 21: 1205-1208.
Bhatta, TR; Chamings, A; Vibin, J and Alexandersen, S (2019). Detection and characterisation of Canine astrovirus, Canine parvovirus and Canine papillomavirus in puppies using next generation sequencing. Sci. Rep., 9: 4602.
Binn, LN; Norby, EA; Marchwicki, RH; Jarman, RG; Keiser, PB and Hang, J (2018). Canine caliciviruses of four serotypes from military and research dogs recovered in 1963-1978 belong to two phylogenetic clades in the Vesivirus genus. Virol. J., 15: 39.
Breitbart, M; Delwart, E; Rosario, K; Segales, J and Varsani, A (2017). ICTV virus taxonomy profile: Circoviridae. J. Gen. Virol., 98: 1997-1998.
Caddy, SL and Goodfellow, I (2015). Complete genome sequence of Canine astrovirus with molecular and epidemiological characterisation of UK strains. Vet. Microbiol., 177: 206-213.
Castro, TX; Cubel Garcia, RCN; Costa, EM; Leal, RM; Xavier, MDPT and Leite, JPG (2013). Molecular characterisation of calicivirus and astrovirus in puppies with enteritis. Vet. Rec., 172: 557.
Choi, S; Lim, S; Kim, Y; Cho, Y; Song, J and An, D (2014). Phylogenetic analysis of astrovirus and kobuvirus in Korean dogs. J. Vet. Med. Sci., 78: 1141-1145.
Cruz, TF; Batista, TN; Vieira, EM; Portela, LMF; Baccarin, AM; Gradiz, JJ and Junior JPA (2020). Genomic characterization of Canine circovirus detected in a dog with intermittent hemorrhagic gastroenteritis in Brazil. Ciência Rural. 50: e20190909.
Decaro, N; Martella, V; Desario, C; Lanave, G; Circella, E; Cavalli, A; Elia, G; Camero, M and Buonavoglia, C (2014). Genomic characterization of a circovirus associated with fatal hemorrhagic enteritis in dog, Italy. PLoS One. 9: e105909.
Desselberger, U (2019). Caliciviridae other than Noroviruses. Viruses. 11: 286.
Di Martino, B; Di Rocco, C; Ceci, C and Marsilio, F (2009). Characterization of a strain of feline calicivirus isolated from a dog faecal sample. Vet. Microbiol., 139: 52-57.
Dowgier, G; Lorusso, E; Decaro, N; Desario, C; Mari, V; Lucente, MS; Lanave, G; Buonavoglia, C and Elia, G (2017). A molecular survey for selected viral enteropathogens revealed a limited role of Canine circovirus in the development of canine acute gastroenteritis. Vet. Microbiol., 204: 54-58.
Edgar, RC (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res., 32: 1792-1797.
Evermann, JF; Bryan, GM and Mckeirnan, A (1981). Isolation of a calicivirus from a case of canine glossitis. Canine Pract., 8: 36-39.
Evermann, JF; Mckeirnan, AJ; Smith, AW; Skilling, DE and Ott, RL (1985). Isolation and identification of caliciviruses from dogs with enteric infections. Am. J. Vet. Res., 46: 218-220.
Gabriel, S; Tohya, Y and Mochizuki, M (1996). Isolation of a calicivirus antigenically related to feline caliciviruses from feces of a dog with diarrhoea. J. Vet. Med. Sci., 58: 1041-1043.
Gentil, M; Gruber, AD and Müller, E (2017). Nachweishäufigkeit von dog circovirus bei gesunden und an Durchfall erkrankten Hunden. Tierarztl Prax Ausg K Kleintiere Heimtiere. 45: 89-94.
Grellet, A; De Battisti, C; Feugier, A; Pantile, M; Marciano, S; Grandjean, D and Cattoli, G (2012). Prevalence and risk factors of astrovirus infection in puppies from French breeding kennels. Vet. Microbiol., 157: 214-219.
Gutierrez-Escolano, AL (2017). Calicivirus biology. In: Ludert, JE; Pujol, FH and Arbiza, J (Eds.), Human virology in Latin America from biology to control. (1st Edn.), Switzerland, Springer. PP: 43-54.
Hsu, HS; Lin, TH; Wu, HY; Lin, LS; Chung, CS; Chiou, MT and Lin, CN (2016). High detection rate of dog circovirus in diarrheal dogs. BMC Vet. Res., 12: 116.
Kapoor, A; Dubovi, EJ; Henriquez-Rivera, JA and Lipkin, WI (2012). Complete genome sequence of the first Canine circovirus. J. Virol., 86: 7018.
Kearse, M; Moir, R; Wilson, A; Stones-Havas, S; Cheung, M; Sturrock, S; Buxton, S; Cooper, A; Markowitz, S; Duran, C; Thierer, T; Ashton, B; Meintjes, P and Drummond, A (2012). Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 28: 1647-1649.
Kotsias, F; Bucafusco, D; Nuñez, DA; Lago Borisovsky, LA; Rodriguez, M and Bratanich, AC (2019). Genomic characterization of Canine circovirus associated with fatal disease in dogs in South America. PLoS One., 14: e0218735.
Li, L; McGraw, S; Zhu, K; Leutenegger, CM; Marks, SL; Kubiski, S; Gaffney, P; Dela Cruz Jr, FN; Wang, C; Delwart, E and Pesavento, PA (2013). Circovirus in tissues of dogs with Vasculitis and Hemorrhage. Emerg. Infect. Dis., 19: 534-541.
Li, L; Pesavento, PA; Shan, T; Leutenegger, CM; Wang, C and Delwart, E (2011). Viruses in diarrhoeic dogs include novel kobuviruses and sapoviruses. J. Gen. Virol., 92: 2534-2541.
MacLachlan, NJ; Dubovi, EJ; Barthold, SW; Swayne, DE and Winton, JR (2017). Caliciviridae and Astroviridae. In: Fenner’s veterinary virology. (5th Edn.), London, Elsevier. PP: 497-510.
Madeley, CR and Cosgrove, BP (1975). 28 nm particles in faeces in infantile gastroenteritis. Lancet. 2: 451-452.
Martella, V; Decaro, N; Lorusso, E; Radogna, A; Moschidou, P; Amorisco, F; Lucente, MS; Desario, C; Mari, V; Elia, G; Banyai, K; Carmichael, LE and Buonavoglia, C (2019). Genetic heterogeneity and recombination in Canine noroviruses. J. Virol., 83: 11391-11396.
Martella, V; Moschidou, P; Lorusso, E; Mari, V; Camero, M; Bellacicco, A; Losurdo, M; Pinto, P; Desario, C; Banyai, K; Elia, G; Decaro, N and Buonavoglia, C (2011). Detection and characterization of Canine astroviruses. J. Gen. Virol., 92: 1880-1887.
Martella, V; Pinto, P; Lorusso, E; Di Martino, B; Wang, Q; Larocca, V; Cavalli, A; Camero, M; Decaro, N; Bányai, K; Saif, LJ and Buonavoglia, C (2015). Detection and full-length genome characterization of novel Canine vesiviruses. Emerg. Infect. Dis., 21: 1433-1436.
Martella, V; Pratelli, A; Gentile, M; Buonavoglia, D; Decaro, N; Fiorante, P and Buonavoglia, C (2002). Analysis of the capsid protein gene of a feline-like calicivirus isolated from a dog. Vet. Microbiol., 85: 315-322.
Martin-Alonso, JM; Skilling, DE; Gonzalez-Molleda, L; del Barrio, G; Machin, A; Keefer, NK; Matson, DO; Iversen, PL; Smith, AW and Parra, F (2005). Isolation and characterization of a new vesivirus from rabbits. Virology. 337: 373-383.
Matsuura, Y; Tohya, Y; Nakamura, K; Shimojima, M; Roerink, F; Mochizuki, M; Takase, K; Akashi, H and Sugimura, T (2002). Complete nucleotide sequence, genome organisation and phylogenic analysis of the Canine calicivirus. Virus Genes. 25: 67-73.
Mendez, E and Arias, C (2013). Astroviruses. In: Knipe, DM and Howley, P (Eds.), Field’s virology. (6th Edn.), Philadelphia, Lippincott Willliams & Wilkins. PP: 609-628.
Mihalov-Kovács, E; Martella, V; Lanave, G; Bodnar, L; Fehér, E; Marton, S; Kemenesi, G; Jakab, F and Bányai, K (2017). Genome analysis of Canine astroviruses reveals genetic heterogeneity and suggests possible inter-species transmission. Virus Res., 232: 162-170.
Mochizuki, M; Hashimoto, M; Roerink, F; Tohya, Y; Matsuura, Y and Sasaki, N (2002). Molecular and seroepidemiological evidence of Canine calicivirus infections in Japan. J. Clin. Microbiol., 40: 2629-2631.
Moser, LA and Schultz-Cherry, S (2005). Pathogenesis of astrovirus infection. Viral Immunol., 18: 4-10.
Ntafis, V; Xylouri, E; Radogna, A; Buonavoglia, C and Martella, V (2010). Outbreak of Canine norovirus infection in young dogs. J. Clin. Microbiol., 48: 2605-2608.
Olortegui, MP; Rouhani, S; Yori, PP; Salas, MS; Trigoso, DR; Mondal, D; Bodhidatta, L; Platts-Mills, J; Samie, A; Kabir, F; Lima, A; Babji, S; Shrestha, SK; Mason, CJ; Kalam, A; Bessong, P; Ahmed, T; Mduma, E; Bhutta, ZA; Lima, I; Ramdass, R; Moulton, LH; Lang, D; George, A; Zaidi, AKM; Kang, G; Houpt, ER; Kosek, MN and on behalf of the MAL-ED Network (2018). Astrovirus infection and diarrhea in 8 countries pediatrics. 141: e20171326.
Piewbang, C; Jo, WK; Puf, C; van der Vries, E; Kesdangsakonwut, S; Rungsipipat, A; Kruppa, L; Jung, K; Baumgärtner, W; Techangamsuwan, S; Ludlow, M and Osterhau, ADME (2018). Novel Canine circovirus strains from Thailand: Evidence for genetic recombination. Sci. Rep., 8: 7524.
Pratelli, A; Greco, G; Camero, M; Normanno, G and Buonavoglia, C (2000). Isolation and identification of a calicivirus from a dog with diarrhea. New Microbiol., 23: 257-260.
Radford, AD; Coyne, KP; Dawson, S; Porter, CJ and Gaskell, RM (2007). Feline calicivirus. Vet. Res., 38: 319-335.
Renshaw, RW; Griffing, J; Weisman, J; Crofton, LM; Laverack, MA; Poston, RP; Duhamel, GE and Dubovi, EJ (2018). Characterization of a vesivirus associated with an outbreak of acute hemorrhagic gastroenteritis in domestic dogs. J. Clin. Microbiol., 56: e01951-17.
Roerink, F; Hashimoto, M; Tohya, Y and Mochizuki, M (1999). Organization of the Canine calicivirus genome from the RNA polymerase gene to the poly(A) tail. J. Gen. Virol., 80: 929-935.
Rosario, K; Breitbart, M; Harrach, B; Segales, J; Delwart, E; Biagini, P and Varsani, A (2017). Revisiting the taxonomy of the family Circoviridae: establishment of the genus cyclovirus and removal of the genus gyrovirus. Arch. Virol., 162: 1447-1463.
Schaffer, FL; Soergel, ME; Black, JW; Skilling, DE; Smith, AW and Cubitt, WD (1985). Characterization of a new calicivirus isolated from feces of a dog. Arch. Virol., 84: 181-195.
Smith, AW; Skilling, DE; Cherry, N; Mead, JH and Matson, DO (1998). Calicivirus emergence from ocean reservoirs: zoonotic and interspecies movements. Emerg. Infect. Dis., 4: 13-20.
Smith, AW; Skilling, DE; Matson, DO; Kroeker, AD; Stein, DA; Berke, T and Iverse, PL (2002). Detection of vesicular exanthema of swine-like calicivirus in tissues from a naturally infected spontaneously aborted bovine fetus. J. Am. Vet. Med. Assoc., 220: 455-458.
Sun, W; Zhang, H; Zheng, M; Cao, H; Lu, H; Zhao, G; Xie, C; Cao, L; Wei, X; Bi, J; Yi, C; Yin, G and Jin, N (2019). The detection of Canine circovirus in Guangxi, China. Virus Res., 259: 85-89.
Tamura, K and 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.
Vinjé, 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.
Weber, MN; Cibulski, SP; Olegario, JC; da Silva, MS; Puhl, DE; Mosena, ACS; Alves, CDBT; Paim, WP; Baumbach, LF; Mayer, FQ; Fernandes, ARF; Azevedo, SS and Canal, CW (2018). Characterization of dog serum
virome from Northeastern Brazil. Virology. 525: 192-199.
Williams, F (1980). Astrovirus-like, coronavirus-like, and parvovirus-like particles detected in the diarrheal stools of beagle pup. Arch. Virol., 66: 215-226.
Xia, M; Wei, C; Wang, L; Cao, D; Meng, XJ; Jiang, X and Tan, M (2016). A trivalent vaccine candidate against hepatitis E virus, norovirus, and astrovirus. Vaccine. 34: 905-913.
Zaccaria, G; Malatesta, D; Scipioni, G; Di Felice, E; Campolo, M; Casaccia, C; Savini, G; Di Sabatino, D and Lorusso, A (2016). Circovirus in domestic and wild carnivores: An important opportunistic agent? Virology. 490: 69-74.
Zhang, W; Wang, R; Liang, J; Zhao, N; Li, G; Gao, Q and Su, S (2020). Epidemiology, genetic diversity, and evolution of Canine astrovirus. Transbound. Emerg. Dis., 00: 1-10.
Zhu, LA; Zhao, W; Yin, H; Shan, TL; Zhu, CX; Yang, X; Hua, XG and Cui, L (2011). Isolation and characterization of Canine astrovirus in China. Arch. Virol., 156: 1671-1675.