Abstract
Canine parvovirus type 2 (CPV-2) infection in dogs is associated with severe gastroenteritis, bloody diarrhea, and vomiting, resulting in high rates of death, especially in unvaccinated puppies within the first months of age. There are three variants, called CPV-2a, CPV-2b, and CPV-2c, co-circulating worldwide. Our group previously reported that the only circulating CPV-2 variant in the Guadalajara metropolitan area in western Mexico was type 2c. Now, a five-year study was performed in order to investigate the possible dominance of CPV-2c in our region. Rectal swabs were collected from 146 dogs with clinical gastroenteritis from May 2014 to August 2019 at the Veterinary Hospital of the University of Guadalajara. Of these, 90 dogs tested positive for canine parvovirus by PCR. Most of the infected dogs with CPV-2 had a partial or incomplete vaccination status (n = 88, 97.8%). Approximately 65% (n = 59) of them were mixed-breed dogs, 77.8% (n = 70) were under 6 months of age, and 37.8% (n = 34) of them died from clinical complications. RFLP analysis of amplicons derived from the vp2 gene showed that all 90 DNA samples corresponded to CPV-2c, with no evidence of the presence of CPV-2a or CPV-2b variants. Twenty-nine of the 90 DNA samples were selected for amplification of a portion of the vp2 gene, and sequencing of these amplicons showed that all of them had the sequence GAA at codon 426, encoding the amino acid glutamic acid, which is characteristic of CPV-2c. Phylogenetic analysis showed that the CPV-2c sequences were related to those of viruses from Europe and South America. The present study indicates that CPV-2c is still the only variant circulating in the dog population of the Guadalajara metropolitan area.
Similar content being viewed by others
References
Agbandje M, Kajigaya S, McKenna R, Young NS, Rossmann MG (1994) The structure of human parvovirus B19 at 8 A resolution. Virology 203:106–115
Aldaz J, Garcia-Diaz J, Calleros L, Sosa K, Iraola G, Marandino A, Hernandez M, Panzera Y, Perez R (2013) High local genetic diversity of canine parvovirus from Ecuador. Vet Microbiol 166:214–219
Allison AB, Organtini LJ, Zhang S, Hafenstein SL, Holmes EC, Parrish CR (2016) Single mutations in the VP2 300 loop region of the three-fold spike of the carnivore parvovirus capsid can determine host range. J Virol 90:753–767
Altman KD, Kelman M, Ward MP (2017) Are vaccine strain, type or administration protocol risk factors for canine parvovirus vaccine failure? Vet Microbiol 210:8–16
Amrani N, Desario C, Kadiri A, Cavalli A, Berrada J, Zro K, Sebbar G, Colaianni ML, Parisi A, Elia G, Buonavoglia C, Malik J, Decaro N (2016) Molecular epidemiology of canine parvovirus in Morocco. Infect Genet Evol 41:201–206
Appel MJ (1999) Forty years of canine vaccination. Adv Vet Med 41:309–324
Buonavoglia C, Cavalli A, Gravino E, Voigt V, Buonavoglia D, de Caprariis D (1994) Intranasal vaccination of pups with maternally derived antibodies with a modified live canine parvovirus. Zentralbl Veterinarmed B 41:3–8
Buonavoglia C, Martella V, Pratelli A, Tempesta M, Cavalli A, Buonavoglia D, Bozzo G, Elia G, Decaro N, Carmichael L (2001) Evidence for evolution of canine parvovirus type 2 in Italy. J Gen Virol 82:3021–3025
Calderon MG, Romanutti C, Wilda M, D’Antuono A, Keller L, Giacomodonato MN, Mattion N, La Torre J (2015) Resurgence of canine parvovirus 2a strain in the domestic dog population from Argentina. J Virol Methods 222:145–149
Callaway HM, Feng KH, Lee DW, Allison AB, Pinard M, McKenna R, Agbandje-McKenna M, Hafenstein S, Parrish CR (2017) Parvovirus capsid structures required for infection: mutations controlling receptor recognition and protease cleavages. J Virol 91:e01871-16
Callaway HM, Welsch K, Weichert W, Allison AB, Hafenstein SL, Huang K, Iketani S, Parrish CR (2018) Complex and dynamic interactions between parvovirus capsids, transferrin receptors and antibodies control cell infection and host range. J Virol 92:e00460-18
Carmichael LE, Joubert JC, Pollock RV (1983) A modified live canine parvovirus vaccine II. Immune response. Cornell Vet 73:13–29
Carmichael LE, Pollock RV, Joubert JC (1984) Response of puppies to canine-origin parvovirus vaccines. Mod Vet Pract 65:99–102
Castro TX, Costa EM, Leite JP, Labarthe NV, Cubel Garcia RC (2010) Partial VP2 sequencing of canine parvovirus (CPV) strains circulating in the state of Rio de Janeiro, Brazil: detection of the new variant CPV-2c. Braz J Microbiol 41:1093–1098
Cotmore SF, Tattersall P (2007) Parvoviral host range and cell entry mechanisms. Adv Virus Res 70:183–232
Day MJ, Crawford C, Marcondes M, Squires RA (2020) Recommendations on vaccination for Latin American small animal practitioners: a report of the WSAVA Vaccination Guidelines Group. J Small Anim Pract 61:E1–E35
Decaro N, Campolo M, Desario C, Elia G, Martella V, Lorusso E, Buonavoglia C (2005) Maternally-derived antibodies in pups and protection from canine parvovirus infection. Biologicals 33:261–267
Decaro N, Desario C, Addie DD, Martella V, Vieira MJ, Elia G, Zicola A, Davis C, Thompson G, Thiry E, Truyen U, Buonavoglia C (2007) The study molecular epidemiology of canine parvovirus, Europe. Emerg Infect Dis 13:1222–1224
Decaro N, Buonavoglia C (2012) Canine parvovirus—a review of epidemiological and diagnostic aspects, with emphasis on type 2c. Vet Microbiol 155:1–12
Decaro N, Crescenzo G, Desario C, Cavalli A, Losurdo M, Colaianni ML, Ventrella G, Rizzi S, Aulicino S, Lucente MS, Buonavoglia C (2014) Long-term viremia and fecal shedding in pups after modified-live canine parvovirus vaccination. Vaccine 32:3850–3853
Dogonyaro BB, Bosman AM, Sibeko KP, Venter EH, van Vuuren M (2013) Genetic analysis of the VP2-encoding gene of canine parvovirus strains from Africa. Vet Microbiol 165:460–465
Duque-Garcia Y, Echeverri-Zuluaga M, Trejos-Suarez J, Ruiz-Saenz J (2017) Prevalence and molecular epidemiology of Canine parvovirus 2 in diarrheic dogs in Colombia, South America: a possible new CPV-2a is emerging? Vet Microbiol 201:56–61
Faz M, Martinez JS, Gomez LB, Quijano-Hernandez I, Fajardo R, Del Angel-Caraza J (2019) Origin and genetic diversity of canine parvovirus 2c circulating in Mexico. Adv Virol 164:371–379
Figueiredo J, Miranda C, Souto R, Silva E, Fafetine J, Thompson G (2017) Genetic characterization of canine parvovirus type 2 subtypes in Maputo, Mozambique. Arch Microbiol 199:543–549
Freisl M, Speck S, Truyen U, Reese S, Proksch AL, Hartmann K (2017) Faecal shedding of canine parvovirus after modified-live vaccination in healthy adult dogs. Vet J 219:15–21
Geng Y, Guo D, Li C, Wang E, Wei S, Wang Z, Yao S, Zhao X, Su M, Wang X, Wang J, Wu R, Feng L, Sun D (2015) Co-circulation of the rare CPV-2c with unique Gln370Arg substitution, new CPV-2b with unique Thr440Ala substitution, and new CPV-2a with high prevalence and variation in Heilongjiang Province, Northeast China. PLoS One 10:e0137288
Goddard A, Leisewitz AL (2010) Canine parvovirus. Vet Clin North Am Small Anim Pract 40:1041–1053
Grecco S, Iraola G, Decaro N, Alfieri A, Alfieri A, Gallo Calderon M, da Silva AP, Name D, Aldaz J, Calleros L, Marandino A, Tomas G, Maya L, Francia L, Panzera Y, Perez R (2018) Inter- and intracontinental migrations and local differentiation have shaped the contemporary epidemiological landscape of canine parvovirus in South America. Virus Evol 4:vey011
Hong C, Decaro N, Desario C, Tanner P, Pardo MC, Sanchez S, Buonavoglia C, Saliki JT (2007) Occurrence of canine parvovirus type 2c in the United States. J Vet Diagn Investig 19:535–539
Kapil S, Cooper E, Lamm C, Murray B, Rezabek G, Johnston L 3rd, Campbell G, Johnson B (2007) Canine parvovirus types 2c and 2b circulating in North American dogs in 2006 and 2007. J Clin Microbiol 45:4044–4047
Kelman M, Norris JM, Barrs VR, Ward MP (2020) A history of canine parvovirus in Australia: what can we learn? Aust Vet J 98:504–510
la Torre D, Mafla E, Puga B, Erazo L, Astolfi-Ferreira C, Ferreira AP (2018) Molecular characterization of canine parvovirus variants (CPV-2a, CPV-2b, and CPV-2c) based on the VP2 gene in affected domestic dogs in Ecuador. Vet World 11:480–487
Li C, Tang J, Chen Z, Li Q, Huang Z, Wang Q, Meng C, Wang Y, Liu G (2018) Genetic characterization of the complete genome of a mutant canine parvovirus isolated in China. Adv Virol 163:521–525
Li G, Ji S, Zhai X, Zhang Y, Liu J, Zhu M, Zhou J, Su S (2017) Evolutionary and genetic analysis of the VP2 gene of canine parvovirus. BMC Genomics 18:534
Miranda C, Thompson G (2016) Canine parvovirus: the worldwide occurrence of antigenic variants. J Gen Virol 97:2043–2057
Naidu H, Subramanian BM, Chinchkar SR, Sriraman R, Rana SK, Srinivasan VA (2012) Typing of canine parvovirus isolates using mini-sequencing based single nucleotide polymorphism analysis. J Virol Methods 181:197–201
Pedroza-Roldan C, Paez-Magallan V, Charles-Nino C, Elizondo-Quiroga D, De Cervantes-Mireles RL, Lopez-Amezcua MA (2015) Genotyping of Canine parvovirus in western Mexico. J Vet Investig 27:107–111
Pedroza-Roldán C, Páez-Magallan V, Charles-Niño C, Elizondo-Quiroga D, Leonel De Cervantes-Mireles R, López-Amezcua MA (2015) Genotyping of Canine parvovirus in western Mexico. J Vet Diagn Investig 27:107–111
Perez R, Francia L, Romero V, Maya L, Lopez I, Hernandez M (2007) First detection of canine parvovirus type 2c in South America. Vet Microbiol 124:147–152
Perez R, Bianchi P, Calleros L, Francia L, Hernandez M, Maya L, Panzera Y, Sosa K, Zoller S (2012) Recent spreading of a divergent canine parvovirus type 2a (CPV-2a) strain in a CPV-2c homogenous population. Vet Microbiol 155:214–219
Pollock RV, Coyne MJ (1993) Canine parvovirus. Vet Clin North Am Small Anim Pract 23:555–568
Qi S, Zhao J, Guo D, Sun D (2020) A mini-review on the epidemiology of canine parvovirus in China. Front Vet Sci 7:5
Quino Quispe R, Luna Espinoza L, Rimac Beltran R, Rosadio Alcantara R, Maturrano Hernandez L (2018) Canine parvovirus types 2a and 2c detection from dogs with suspected parvoviral enteritis in Peru. Virusdisease 29:109–112
Rosales DC (2019) Caracterizacion genetica de cepas de Parvovirus canino presentes en el area metropolitana de Monterrey. Universidad Autonoma de Nuevo Leon, Nuevo Leon, p 55
Ryan S, Bacon H, Endenburg N, Hazel S, Jouppi R, Lee N, Seksel K, Takashima G (2019) WSAVA animal welfare guidelines. J Small Anim Pract 60:E1–E46
Sehata G, Sato H, Yamanaka M, Takahashi T, Kainuma R, Igarashi T, Oshima S, Noro T, Oishi E (2017) Substitutions at residues 300 and 389 of the VP2 capsid protein serve as the minimal determinant of attenuation for canine parvovirus vaccine strain 9985–46. J Gen Virol 98:2759–2770
Wilson S, Illambas J, Siedek E, Stirling C, Thomas A, Plevova E, Sture G, Salt J (2014) Vaccination of dogs with canine parvovirus type 2b (CPV-2b) induces neutralising antibody responses to CPV-2a and CPV-2c. Vaccine 32:5420–5424
Zhong Z, Liang L, Zhao J, Xu X, Cao X, Liu X, Zhou Z, Ren Z, Shen L, Geng Y, Gu X, Peng G (2014) First isolation of new canine parvovirus 2a from Tibetan mastiff and global analysis of the full-length VP2 gene of canine parvoviruses 2 in China. Int J Mol Sci 15:12166–12187
Zhou P, Zeng W, Zhang X, Li S (2017) The genetic evolution of canine parvovirus—a new perspective. PLoS One 12:e0175035
Funding
This work was partially supported by the SNI and SNCA 2019 Production Improvement Support Program, granted to CPR by the University of Guadalajara. P3e328894.
Author information
Authors and Affiliations
Contributions
Conceived the study: CPR and CCN. Performed experiments: MAHA, DEQ, AGO, CMAM, and SDCRG. Interpreted data: CPR, DEQ, ABO, and MRQ. Wrote the manuscript: CPR, DEQ, and MRQ. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no potential conflicts of interest with respect to the research, authorship, and publication of this article.
Ethical approval
The study was approved by the biosafety, research, and ethics committees of the Veterinary Hospital of the University of Guadalajara. The pets' owners were informed about the purpose and procedures of the study and gave consent for taking a rectal swab sample from the dogs. The study followed federal regulations such as NOM-087-SEMARNAT- SSA1-2002, NOM-033-ZOO-1995, and NOM-062-ZOO- 1999.
Additional information
Handling Editor: Sheela Ramamoorthy.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Pedroza-Roldán, C., Hernández-Almaraz, M.A., Elizondo-Quiroga, D. et al. Exclusive circulation of canine parvovirus type 2c in the Guadalajara metropolitan area in western Mexico: a five-year study. Arch Virol 167, 2109–2121 (2022). https://doi.org/10.1007/s00705-022-05522-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-022-05522-7