Seroepidemiological and Clinicopathological Investigation of Canine Coronavirus Infection in Dogs, in Türkiye

Yıl: 2022 Cilt: 10 Sayı: 10 Sayfa Aralığı: 1884 - 1892 Metin Dili: İngilizce DOI: 10.24925/turjaf.v10i10.1884-1892.5375 İndeks Tarihi: 27-05-2023

Seroepidemiological and Clinicopathological Investigation of Canine Coronavirus Infection in Dogs, in Türkiye

Öz:
Domestic and wild dogs of all ages and breeds are susceptible to Canine Coronavirus (CCoV) infections and be seen in Türkiye and amongst world. CCoV has recently been declared a zoonotic disease agent and the eighth pathogenic human coronavirus. This study was conducted on 143 naturally infected dogs with gastroenteritis which were not vaccinated against CCoV in Türkiye in 2015-2020. The data of dogs were analyzed seroepidemiologically, clinicopathologically and statistically. CCOV antibodies in serum and CCOV antigens in stool were detected by ELISA and lateral immunochromatography. The rising CCoV IgG antibody titers were detected at all dogs and were as follows; <10 ng/L in 3 (2%), 10-20 ng/L in 18 (13%), 20-30 ng/L in 16 (11%), 30- 40 ng/L in 14 (%10), 40-64 ng/L in 11 (8%) and >64 ng/L in 81 (81%) dogs. CCOV and Canine Parvovirus (CPV) antigen were detected together in the stool of the 41 (28.7%) dogs. As a result, it was concluded that the CCOV agent is in circulation among dogs living in Türkiye. CCOV and CPV can cause co-infections and increased mortality. Although infection can be seen in dogs of all ages, it can be seen more frequently in dogs younger than 1 year of age, and especially in dogs younger than 6 months, and can cause enteritis, low hemoglobin, erythropenia, lymphopenia, leukopenia, thrombocytopenia, and hypoproteinemia.
Anahtar Kelime:

Belge Türü: Makale Makale Türü: Araştırma Makalesi Erişim Türü: Erişime Açık
  • Akkutay-Yoldar Z, Koç BT, Oğuzoğlu T. 2020. Phylogenetic analysis of partial transmembrane protein gene of canine coronaviruses detected in Türkiye. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 67(3): 265-271. doi: 10.33988/auvfd.619074
  • Alfano F, Fusco G, Mari V, Occhiogrosso L, Miletti G, Brunetti R, Galiero G, Desario C, Cirilli M, Decaro N. 2020. Circulation of pantropic canine coronavirus in autochthonous and imported dogs, Italy. Transboundary and Emerging Diseases, doi: https://doi.org/10.1111/tbed.13542
  • Avcı O, Yavru S, Kale M, Dik I. 2015. Barınak köpeklerinde canine coronavirus varlığının belirlenmesi. Eurasian Journal of Veterinary Science, 31(3): 184-187, doi: 10.15312/EurasianJVetSci.2015310977
  • Avcı O, Levent O, Yapici Orhan, Hasircioglu S, Simsek A. 2016. Canine coronavirus infection in dogs in Türkiye: Virological and serological evidence. Indian Journal of Animal Research, doi: https://doi.org/10.18805/ijar.11173.
  • Buller H, Adam K, Bard A, Bruce A, (Ray) Chan KW, Hinchliffe S, Morgans L, Rees G, Reyher KK. 2020. Veterinary Diagnostic Practice and the Use of Rapid Tests in Antimicrobial Stewardship on UK Livestock Farms. Frontiers in Veterinary Science, 7: 765- doi: https://doi.org/10.3389/fvets.2020.569545
  • Castro TX, Cubel Garcia R, Gonçalves LP, Costa EM, Marcello GC, Labarthe NV, Mendes-de-Almeida F. 2013. Clinical, hematological, and biochemical findings in puppies with coronavirus and parvovirus enteritis. The Canadian Veterinary Journal = La revue Veterinaire Canadienne, 54(9): 885–888. PMID: 24155496; PMCID: PMC3743577.
  • Chitwood MC, Swingen MB, Lashley MA, Flowers JR, Palamar MB, Apperson CS, Olfenbuttel C, Moorman CE, DePerno CS. 2015. Parasitology and Serology of Free-Ranging Coyotes (Canis Latrans) In North Carolina. USA, Journal of Wildlife Diseases, 51(3): 664–669, doi: https://doi.org/10.7589/2015-01-002
  • Day MJ, Carey S, Clercx C, Kohn B, MarsilIo F, Thiry E, Freyburger L, Schulz B, Walker DJ. 2020. Aetiology of Canine Infectious Respiratory Disease Complex and Prevalence of its Pathogens in Europe. Journal of Comparative Pathology, 176: 86–108, doi: https://doi.org/10.1016/j.jcpa.2020.02.005
  • Day MJ, Horzinek MC, Schultz RD, Squires RA, Vaccination Guidelines Group (VGG) of the World Small Animal Veterinary Association (WSAVA) (2016). WSAVA Guidelines for the vaccination of dogs and cats. The Journal of Small Animal Practice, 57(1): 4–8, doi: https://doi.org/10.1111/jsap.12431
  • Decaro N, Desario C, Elia G, Mari V, Lucente MS, Cordioli P, Colaianni ML, Martella V, Buonavoglia C. 2007. Serological and molecular evidence that canine respiratory coronavirus is circulating in Italy. Veterinary Microbiology, 121(3-4): 225– 230, doi: https://doi.org/10.1016/j.vetmic.2006.12.001
  • Decaro N, Buonavoglia C. 2011. Canine coronavirus: not only an enteric pathogen. The Veterinary clinics of North America, Small Animal Practice, 41(6): 1121–1132, doi: https://doi.org/10.1016/j.cvsm.2011.07.005
  • Dileepan M, Di D, Huang Q, Ahmed S, Heinrich D, Ly H, Liang Y. 2021. Seroprevalence of SARS-CoV-2 (COVID-19) exposure in pet cats and dogs in Minnesota, USA. Virulence, 12(1): 1597–1609, doi: https://doi.org/10.1080/ 21505594/ 2021/1936433
  • El Wahed A, Truyen U. 2021. Canine Coronaviren: Neu und erneut auftretende Pathogene des Hundes, Export Zitierung. Berliner und Münchener Tierärztliche Wochenschrift, 134: 1- 6, doi: https://doi.org/10.2376/1439/0299/2021.1
  • Erles K, Brownlie J. 2008. Canine respiratory coronavirus: an emerging pathogen in the canine infectious respiratory disease complex. The Veterinary clinics of North America, Small Animal Practice, 38(4): 815–818, doi: https://doi.org/10.1016/j.cvsm.2008.02.008
  • Fehr AR, Perlman S. 2015. Coronaviruses: an overview of their replication and pathogenesis. Methods in Molecular Biology (Clifton, N.J.), 1282: 1–23, doi: https://doi.org/10.1007/978/ 1.4939/2438.7.1
  • Gan J, Tang Y, Lv H, Xiong W, Tian X. 2021. Identification and phylogenetic analysis of two canine coronavirus strains. Animal Diseases, 1(1): 10, doi: https://doi.org/10.1186/s44149/021/00013.9
  • Greiner M, Gardner IA. 2000. Application of diagnostic tests in veteri-nary epidemiologic studies. Preventive Veterinary Medicine, 45(1–2): 43–59, doi: https://doi.org/10.1016/ s0167-5877 (00)00116-1
  • Gur S, Gencay A Dogan N. 2008. A Serologic Investigation for Canine Corona Virus Infection in Individually Reared Dogs in Central Anatolia. Erciyes Üniversitesi Veteriner Fakültesi Dergisi, 5(2): 67-71, doi: https://dergipark.org.tr/en/pub/ ercivet/issue/ 5820/77420
  • Hasoksuz M, Kiliç S, Saraç F. 2020. Coronaviruses and SARS- COV-2. Turkish Journal of Medical Sciences, 50(SI-1): 549– 556, DOI: https://doi.org/10.3906/sag-2004-127
  • Haake C, Cook S, Pusterla N, Murphy B. 2020. Coronavirus Infections in Companion Animals: Virology, Epidemiology, Clinical and Pathologic Features. Viruses, 12(9): 1023, doi: https://doi.org/10.3390/v12091023
  • He HJ, Zhang W, Liang J, Lu M, Wang R, Li G, He JW, Chen J, Chen J, Xing G, Chen Y. 2020. Etiology and genetic evolution of canine coronavirus circulating in five provinces of China, during 2018-2019. Microbial Pathogenesis, 145: 104209, doi: https://doi.org/10.1016/j.micpath.2020.104209
  • ICTV, 2011. International Committee on Taxonomy of Viruses (ICTV), Positive Sense RNA Viruses, Virus Taxonomy: 2019 Release, EC 51, Berlin, Germany, July 2019, Coronaviridae. International Committee on Taxonomy of Viruses, DOI: https://talk.ictvonline.org. Accessed Date: 19.05.2022.
  • Jeoung SK, Ahn S-J, Kim D. 2008. Co-in fection of dogs with canine coronavirus and canine parvovirus in Korea. Journal of Veterinary Clininic, 25: 1 (Suppl.) 76.
  • Jeoung SK, Ahn SJ, Pak SI, Kim D. 2010. Prevalence of canine coronaviral enteritis in Korea. Journal of Veterinary Clinic, 27(3): 209-215.
  • Kaneshima T, Hohdatsu T, Satoh K, Takano T, Motokawa K, Koyama H. 2006. The prevalence of a group 2 coronavirus in dogs in Japan. The Journal of Veterinary Medical Science, 68(1): 21–25, doi: https://doi.org/10.1292/jvms.68.21
  • Kirwood BR, Sterne JAC. 2003. Essential Medical Statistics, Blackwell Publishing: 2nd Ed. ISBN: 978-0199589920.
  • Küçük Hayvan Veteriner Hekimler Derneği Aşı Rehberi. 2018. doi: http://www.khvhd.org.tr/FileUpload/ds303192/File/ khvhd_ulusal_asi_rehberi.pdf. Accessed Date: 20.05.2022.
  • Lednicky JA, Tagliamonte MS, White SK, Blohm GM, Alam MM, Iovine NM, Salemi M, Mavian C, Morris JG. 2021. Isolation of a Novel Recombinant Canine Coronavirus from a Visitor to Haiti: Further Evidence of Transmission of Coronaviruses of Zoonotic Origin to Humans. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America, ciab924, Advance online publication, doi: https://doi.org/10.1093/cid/ciab924
  • Licitra BN, Duhamel GE, Whittaker GR. 2014. Canine enteric coronaviruses: emerging viral pathogens with distinct recombinant spike proteins. Viruses 6: 3363–3376, doi: 10.3390/v6083363.
  • Perera R, Ko R, Tsang O, Hui D, Kwan M, Brackman CJ, To E, Yen HL, Leung K, Cheng, S, Chan KH, Chan K, Li K, C, Saif L, Barrs VR, Wu JT, Sit T, Poon L, Peiris M. 2021.
  • Evaluation of a SARS-CoV-2 Surrogate Virus Neutralization Test for Detection of Antibody in Human, Canine, Cat, and Hamster Sera. Journal of Clinical Microbiology, 59(2): e02504-20, doi: https://doi.org/10.1128/JCM.02504-20
  • Pourhatami A, Kaviyani-Charati M, Kargar B, Baziyad H, Kargar M, Olmeda-Gómez C. 2021. Mapping the intellectual structure of the coronavirus field (2000-2020): a co-word analysis. Scientometrics, 126(8): 6625–6657, doi: https://doi.org/10.1007/s11192-021-04038-2
  • Pratelli A, Elia G, Martella V, Palmieri A, Cirone F, Tinelli A, Corrente M, Buonavoglia C. 2002. Prevalence of canine coronavirus antibodies by an enzyme-linked immunosorbent assay in dogs in the south of Italy. Journal of Virological Methods, 102(1-2): 67–71, doi: https://doi.org/10.1016/ s0166-0934 (01)00450-5
  • Pratelli A, Tinelli A, Decaro N, Martella V, Camero M, Tempesta M, Martini M, Carmichael, LE, Buonavoglia C. 2004. Safety and efficacy of a modified-live canine coronavirus vaccine in dogs. Veterinary Microbiology, 99(1): 43–49, doi: https://doi.org/10.1016/j.vetmic.2003.07.009
  • Pratelli A, Tempesta M, Elia G, Martella V, Decaro N, Buonavoglia C. 2022. The knotty biology of canine coronavirus: A worrying model of coronaviruses' danger. Research in Veterinary Science, 144: 190–195, doi: https://doi.org/10.1016/j.rvsc.2021.11.014
  • Priestnall SL. 2020. Canine Respiratory Coronavirus: A Naturally Occurring Model of COVID-19? Veterinary Pathology, 57(4): 467–471, doi: https://doi.org/10.1177/0300985820926485
  • Rowland H, Holding E, Falces PM, Wissink-Argilaga N, Stidworthy MF, Denk D, Weir W, Krumrie S, Dunbar D, Hopper JS. 2021. Canine coronavirus subtype 2a associated with outbreaks of fatal diarrhoea in bush dog (Speothos venaticus) groups, Fatale Diarrhoe bei Waldhunden (Speothos venaticus) durch Canines Coronavirus Subtyp 2a. Schweizer Archiv fur Tierheilkunde, 164(10): 661–671, doi: https://doi.org/10.17236/sat00320
  • Sulehria MU, Ahmad SS, Ijaz M, Mushtaq MH, Khan AY Ghaffar A. 2020. Molecular evidence and hematological alterations associated with the occurrence of coronavirus in domestic dogs in Pakistan. Tropical Biomedicine, 37(4): 963–972, doi: https://doi.org/10.47665/tb.37.4.963
  • Szczepanski A, Owczarek K, Bzowska M, Gula K., Drebot I, Ochman M, Maksym B, Rajfur Z, Mitchell JA, Pyrc K. 2019. Canine Respiratory Coronavirus, Bovine Coronavirus, and Human Coronavirus OC43: Receptors and Attachment Factors. Viruses, 11(4): 328, doi: https://doi.org/10.3390/v11040328
  • Takano T, Yamashita S, Murata-Ohkubo M, Satoh K, Doki T, Hohdatsu T. 2016. Prevalence of canine coronavirus (CCoV) in dog in Japan: detection of CCoV RNA and retrospective serological analysis. The Journal of Veterinary Medical Science, 78(2): 341–345, doi: https://doi.org/10.1292/ jvms.15-0347
  • Tekelioglu BK, Berriatua E, Turan N, Helps CR, Kocak M, Yilmaz H. 2015. A retrospective clinical and epidemiological study on feline coronavirus (FCoV) in cats in Istanbul, Türkiye. Preventive Veterinary Medicine, 119(1-2): 41–47, doi: https://doi.org/10.1016/ jprevetmed.2015.01.017
  • Tekelioglu BK. 2016. Virüsler Geleceğin Doğal Afet Adayları, Mimar ve Mühendis, 88(03-04): 64-65.
  • Tekelioglu BK. 2020. Seroepidemiological and clinicopathological study of feline coronavirus (FCoV) and feline infectious peritonitis (FIP), could guide to COVID-19 in ‘One Health’ approach, Alinteri Journal of Agriculture Science, 35(2): 181-196. doi: https://doi.org/10.28955/ alinterizbd.788313
  • Tekelioglu BK. 2021. Veterinerlikte Akademik Araştırmalar, In: Cengizler İ. (Editör), Canine Coronavirüsleri, İksad Publications, pp. 35-72. ISBN: 978-625-8061-00-0 (Online).
  • Tekelioglu BK, Yüceer HB, Akın B, Koç Ö, Çelik M, Kandır S, Baykal Çelik L, Gökçe M. 2021. Osmaniye İlinde Sahipsiz Köpeklerin Rehabilitasyonu ve Viral Enfeksiyon Profilaksisi. Avrupa Bilim ve Teknoloji Dergisi, Ejosat, Özel Sayı 32: 956-966, doi: 10.31590/ejosat.1047514
  • Timurkan MO, Aydin H, Dincer E, Coskun N. 2021. Molecular characterization of canine coronaviruses: an enteric and pantropic approach. Archives of Virology, 166(1): 35–42, doi: https://doi.org/10.1007/s00705-020-04826-w
  • Tizard IR. 2020. Vaccination against coronaviruses in domestic animals. Vaccine, 38(33): 5123–5130, doi: https://doi.org/10.1016/j.vaccine.2020.06.026
  • Ün H. 2020. Coronaviridae Virus Ailesi: Genel Bir Değerlendirme. Journal of Advances in VetBio Science and Techniques, 5(1): 1-12, doi: https://dergipark.org.tr/tr/pub/ vetbio/issue/53988/726735
  • van Nguyen D, Terada Y, Minami S, Yonemitsu K, Nagata N, LE TD, Kuwata R, Shimoda H, Maeda K. 2017. Characterization of canine coronavirus spread among domestic dogs in Vietnam. The Journal of Veterinary Medical Science, 79(2): 343–349, doi: https://doi.org/10.1292/jvms.16-0538
  • Villiers E, Blackwood L. 2005. BSAVA Manual of Canine and Feline Clinical Pathology. British Small Animal, Veterinary Association: ISBN: 9780905214795
  • Vlasova AN, Diaz A, Damtie D, Xiu L, Toh TH, Lee JS, Saif LJ, Gray GC. 2022. Novel Canine Coronavirus Isolated from a Hospitalized Patient with Pneumonia in East Malaysia. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America 74(3): 446–454, doi: https://doi.org/10,1093/cid/ciab456
  • Wang J, Wang J, Li R, Liu L, Yuan W. 2017. Rapid and sensitive detection of canine distemper virus by real-time reverse transcription recombinase polymerase amplification. BMC Veterinary Research, 13(1): 241, doi: https://doi.org/10.1186/s12917-017-1180-7
  • Watts DE, Benson AM. 2016. Prevalence of Antibodies for Selected Canine Pathogens among Wolves (Canis Lupus) From the Alaska Peninsula, USA. Journal of Wildlife Diseases, 52(3): 506–515, doi: https://doi.org/10.7589/2015- 06-140
  • Wille M, Wensman JJ, Larsson S, van Damme R, Theelke AK, Hayer J, Malmberg M. 2020. Evolutionary genetics of canine respiratory coronavirus and recent introduction into Swedish dogs. Infection, genetics and evolution. Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, 82: 104290, doi: https://doi.org/10.1016/j.meegid.2020.104290
  • Woo PC, Huang Y, Lau SK, Yuen KY. 2010. Coronavirus genomics and bioinformatics analysis. Viruses, 2(8): 1804– 1820, doi: https://doi.org/10.3390/v2081803
  • Yesilbag K, Yilmaz Z, Torun S, Pratelli A. 2004. Canine coronavirus infection in Turkish dog population. Journal of Veterinary Medicine, Infectious Diseases and Veterinary Public Health, 51(7): 353–355, doi: https://doi.org/10.1111/j.1439-0450.2004.00773.x
  • Yoon SJ, Seo KW, Song KH. 2018. Clinical evaluation of a rapid diagnostic test kit for detection of canine coronavirus, Korean Journal of Veterinary Research, 58: 27–31, doi: https://doi.org/10.14405/kjvr.2018.58.1.27
  • Zappulli V, Ferro S, Bonsembiante F, Brocca G, Calore A, Cavicchioli L, Centelleghe C, Corazzola G, De Vreese S, Gelain ME, Mazzariol S, Moccia V, Rensi N, Sammarco A, Torrigiani F, Verin R, Castagnaro M. 2020. Pathology of Coronavirus Infections: A Review of Lesions in Animals in the One-Health Perspective. Animals (Basel), 11; 10(12):2377, doi: https://doi.org/10.3390/ani10122377
APA Tekelioglu B (2022). Seroepidemiological and Clinicopathological Investigation of Canine Coronavirus Infection in Dogs, in Türkiye. , 1884 - 1892. 10.24925/turjaf.v10i10.1884-1892.5375
Chicago Tekelioglu Bilge Kaan Seroepidemiological and Clinicopathological Investigation of Canine Coronavirus Infection in Dogs, in Türkiye. (2022): 1884 - 1892. 10.24925/turjaf.v10i10.1884-1892.5375
MLA Tekelioglu Bilge Kaan Seroepidemiological and Clinicopathological Investigation of Canine Coronavirus Infection in Dogs, in Türkiye. , 2022, ss.1884 - 1892. 10.24925/turjaf.v10i10.1884-1892.5375
AMA Tekelioglu B Seroepidemiological and Clinicopathological Investigation of Canine Coronavirus Infection in Dogs, in Türkiye. . 2022; 1884 - 1892. 10.24925/turjaf.v10i10.1884-1892.5375
Vancouver Tekelioglu B Seroepidemiological and Clinicopathological Investigation of Canine Coronavirus Infection in Dogs, in Türkiye. . 2022; 1884 - 1892. 10.24925/turjaf.v10i10.1884-1892.5375
IEEE Tekelioglu B "Seroepidemiological and Clinicopathological Investigation of Canine Coronavirus Infection in Dogs, in Türkiye." , ss.1884 - 1892, 2022. 10.24925/turjaf.v10i10.1884-1892.5375
ISNAD Tekelioglu, Bilge Kaan. "Seroepidemiological and Clinicopathological Investigation of Canine Coronavirus Infection in Dogs, in Türkiye". (2022), 1884-1892. https://doi.org/10.24925/turjaf.v10i10.1884-1892.5375
APA Tekelioglu B (2022). Seroepidemiological and Clinicopathological Investigation of Canine Coronavirus Infection in Dogs, in Türkiye. Türk Tarım - Gıda Bilim ve Teknoloji dergisi, 10(10), 1884 - 1892. 10.24925/turjaf.v10i10.1884-1892.5375
Chicago Tekelioglu Bilge Kaan Seroepidemiological and Clinicopathological Investigation of Canine Coronavirus Infection in Dogs, in Türkiye. Türk Tarım - Gıda Bilim ve Teknoloji dergisi 10, no.10 (2022): 1884 - 1892. 10.24925/turjaf.v10i10.1884-1892.5375
MLA Tekelioglu Bilge Kaan Seroepidemiological and Clinicopathological Investigation of Canine Coronavirus Infection in Dogs, in Türkiye. Türk Tarım - Gıda Bilim ve Teknoloji dergisi, vol.10, no.10, 2022, ss.1884 - 1892. 10.24925/turjaf.v10i10.1884-1892.5375
AMA Tekelioglu B Seroepidemiological and Clinicopathological Investigation of Canine Coronavirus Infection in Dogs, in Türkiye. Türk Tarım - Gıda Bilim ve Teknoloji dergisi. 2022; 10(10): 1884 - 1892. 10.24925/turjaf.v10i10.1884-1892.5375
Vancouver Tekelioglu B Seroepidemiological and Clinicopathological Investigation of Canine Coronavirus Infection in Dogs, in Türkiye. Türk Tarım - Gıda Bilim ve Teknoloji dergisi. 2022; 10(10): 1884 - 1892. 10.24925/turjaf.v10i10.1884-1892.5375
IEEE Tekelioglu B "Seroepidemiological and Clinicopathological Investigation of Canine Coronavirus Infection in Dogs, in Türkiye." Türk Tarım - Gıda Bilim ve Teknoloji dergisi, 10, ss.1884 - 1892, 2022. 10.24925/turjaf.v10i10.1884-1892.5375
ISNAD Tekelioglu, Bilge Kaan. "Seroepidemiological and Clinicopathological Investigation of Canine Coronavirus Infection in Dogs, in Türkiye". Türk Tarım - Gıda Bilim ve Teknoloji dergisi 10/10 (2022), 1884-1892. https://doi.org/10.24925/turjaf.v10i10.1884-1892.5375