The first comprehensive study on isolation and genetic characterization of canine parvoviruses from dogs in Mizoram, India reveals the emergence of CPV-2c

Document Type : Full paper (Original article)

Authors

1 Ph.D. Student in Veterinary Medicine, Department of Veterinary Medicine, West Bengal University of Animal and Fishery Sciences, West Bengal, Kolkata-700037, India

2 Department of Veterinary Medicine, College of Veterinary Sciences and Animal Husbandry, Central Agricultural University, Selesih-796 015, Aizawl, Mizoram, India

3 Graduated from Regional Institute of Paramedical and Nursing Sciences, Zemabawk-796 017, Aizawl, Mizoram, India

4 Department of Veterinary Microbiology, College of Veterinary Sciences and Animal Husbandry, Central Agricultural University, Selesih-796 015, Aizawl, Mizoram, India

5 MVSc in Veterinary Medicine, Department of Veterinary Medicine, College of Veterinary Sciences and Animal Husbandry, Central Agricultural University, Selesih-796 015, Aizawl, Mizoram, India

6 Department of Physiology and Biochemistry, College of Veterinary Sciences and Animal Husbandry, Central Agricultural University, Selesih-796 015, Aizawl, Mizoram, India

7 Department of Animal Breeding and Genetics, College of Veterinary Sciences and Animal Husbandry, Central Agricultural University, Selesih-796 015, Aizawl, Mizoram, India

8 MVSc in Veterinary Surgery and Radiology, Department of Veterinary Surgery and Radiology, College of Veterinary Sciences and Animal Husbandry, Central Agricultural University, Selesih-796 015, Aizawl, Mizoram, India

9 MVSc in Animal Reproduction and Gynaecology, College of Veterinary Sciences and Animal Husbandry, Central Agricultural University, Selesih-796 015, Aizawl, Mizoram, India

10 Division of Immunology (CADRAD), ICAR-Indian Veterinary Research Institute, Izatnagar, Bareilly, Uttar Pradesh, India

11 Department of Veterinary Medicine, Bihar Veterinary College, Bihar Animal Sciences University, Patna-800014, India

Abstract

Background: Canine parvovirus type-2 (CPV-2) is a highly contagious enteric pathogen of puppies with worldwide distribution. Aims: Molecular epidemiology, genetic characterization, phylogenetic analysis, and isolation of the CPV-2 virus from clinically affected dogs in Mizoram, India over eight years. Methods: A total of 202 samples (199 fecal samples, 2 vomita, and 1 tissue sample) were screened by PCR assay. Results: 103 out of 202 samples (50.99%) tested positive. Of the 103 positive samples, 83 samples were cloned and sequenced. Sequence analysis showed CPV-2c as the predominant variant (63.85%) followed by the 2a variant (26.5%), 2b (8.43%), and FPV (1.2%). Phylogenetic analyses of the CPV-2c sequences formed separate clusters and were ancestrally related to Japanese, Chinese, and Italian 2c sequences. Similarly, 2a isolates formed separate clusters under different clades and were ancestrally related to Indian, Singaporean, Japanese, Uruguayan, and Chinese 2a isolates. 2b isolates formed a single cluster with the Chinese 2b isolate. FPV isolate clustered with North American FPV. Both synonymous and non-synonymous mutations (unique to this study) were evident in all the types of CPV-2s indicative of active evolution with regional variation. In the cell culture medium, CPV-2 showed cytopathogenic effects at the third passage level. Conclusion: The study, the first in-depth report on CPV-2, showed a shift towards CPV-2c as the predominant variant in Mizoram. This variant clustered separately from current vaccine strains, highlighting the need for extensive epidemiological surveillance to better understand viral phylogenomics and evaluate current vaccine efficacy.

Keywords

Main Subjects


Battilani, M; Modugno, F; Mira, F; Purpari, G; Di bella, S; Guercio, A and Balboni, A (2019). Molecular epidemiology of canine parvovirus type 2 in Italy from 1994 to 2017: recurrence of the CPV-2b variant. BMC Vet. Res., 15: 1-13.
Behera, SK; Singh, YD; Roychoudhury, P; Arya, RS; Behera, P; Ali, MA; Prasad, H; Sarma, K; Rajesh, JB and Chethan, GE (2020). Clinico-pathological and necropsy findings in a 4-month old mixed-breed pup with canine parvovirus-2 infection and its genetic characterization. J. Entomol. Zool. Stud., 8: 573-577.
Buonavoglia, C; Martella, V; Pratelli, A; Tempesta, M; Cavalli, A; Buonavoglia, D; Bozzo, G; Elia, G; Decaro, N and Carmichael, L (2001). Evidence for evolution of canine parvovirus type 2 in Italy. J. Gen. Virol., 82: 3021-3025.
Calderón, MG; Romanutti, C; Antuono, DA; Keller, L; Mattion, N and Torre, JL (2011). Evolution of canine parvovirus in Argentina between years 2003 and 2010: CPV2c has become the predominant variant affecting the domestic dog population. Virus Res., 157: 106-110.
Castro, TX; Garcia, CR; Gonçalves, CLP; Costa, EM; Marcello, GC; Labarthe, NV and Mendes-De-Almeida, F (2013). Clinical, hematological, and biochemical findings in puppies with coronavirus and parvovirus enteritis. Can. Vet. J., 54: 885-888.
Chakraborty, P (2022). Molecular characterization of canine parvovirus-2 infection in dogs and its therapeutic management using homeopathic formulation. MVSc Thesis, Central Agricultural University, Imphal, Manipur, India. PP: 10-135.
Chang, AY; Chau, VWY; Landas, JA and Pang, Y (2017). Preparation of calcium competent Escherichia coli and heat-shock transformation. UJEMI., 1: 22-25.
Charoenkul, K; Tangwangvivat, R; Janetanakit, T; Boonyapisitsopa, S; Bunpapong, N; Chaiyawong, S and Amonsin, A (2019). Emergence of canine parvovirus type 2c in domestic dogs and cats from Thailand. Transbound. Emerg. Dis., 66: 1518-1528.
Chiang, SY; Wu, HY; Chiou, MT; Chang, M and Lin, CN (2016). Identification of a novel canine parvovirus type 2c in Taiwan. Virol. J., 13: 1-7.
Clark, NJ; Seddon, JM; Kyaw-Tanner, M; Al-Alawneh, J; Harper, G; Mcdonagh, P and Meers, J (2018). Emergence of canine parvovirus subtype 2b (CPV-2b) infections in Australian dogs. Infect. Genet. Evol., 58: 50-55.
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 and Tijssen, P (2019). ICTV report consortium. ICTV virus taxonomy profile: Parvoviridae. J. Gen. Virol., 100: 367-368.
Cságola, A; Varga, S; Lőrincz, M and Tuboly, T (2014). Analysis of the full-length VP2 protein of canine parvoviruses circulating in Hungary. Arch. Virol., 159: 2441-2444.
Decaro, N and Buonavoglia, C (2012). Canine parvovirus—a review of epidemiological and diagnostic aspects, with emphasis on type 2c. Vet. Microbiol., 155: 1-12.
Decaro, N; Buonavoglia, C and Barrs, VR (2020). Canine parvovirus vaccination and immunisation failures: are we far from disease eradication? Vet. Microbiol., 247: 108760.
Diakoudi, G; Desario, C; Lanave, G; Salucci, S; Ndiana, LA; Zarea, AAK; Fouad, EA; Lorusso, A; Alfano, F; Cavalli, A; Buonavoglia, C; Martella, V and Decaro, N (2022). Feline panleukopenia virus in dogs from Italy and Egypt. Emerg. Infect. Dis., 28: 1933-1935.
Dong, B; Zhang, G; Zhang, J; Bai, J and Lin, W (2020). A systematic literature review and meta-analysis of characterization of canine parvoviruses 2 prevalent in mainland China. Virol. J., 17: 1-10.
Folitse, RD; Kodie, DO; Amemor, E; Dei, D; Tasiame, W; Burimuah, V and Emikpe, BO (2018). Detection of canine parvovirus antigen in dogs in Kumasi, Ghana. Afr. J. Infect. Dis., 12: 28-32.
Fu, P; He, D; Cheng, X; Niu, X; Wang, C; Fu, Y; Li, K; Zhu, H; Lu, W; Wang, J and Chu, B (2022). Prevalence and characteristics of canine parvovirus type 2 in Henan Province, China. Microbiol. Spectr., 10: e01856-22.
Geng, Y; Guo, D; Li, C; Wang, E; Wei, S; Wang, Z; Yao, S; Zhao, X; Su, M; Wang, X and Wang, J (2017). 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.
Gupta, V; Chander, V; Chakravarti, S; Sharma, GK; Malla, JA; Gupta, VK and Nandi, S (2018). Multiplex amplification refractory mutation system PCR (ARMS-PCR) provides convenient method for differentiation of canine parvovirus vaccine and field strains. Virusdisease. 29: 565-568.
Hao, X; Li, Y; Xiao, X; Chen, B; Zhou, P and Li, S (2022). The changes in canine parvovirus variants over the years. Int. J. Mol. Sci., 23: 11540.
Jain, SK; Kumar, V and Saharia, M (2013). Analysis of rainfall and temperature trends in northeast India. Int. J. Climatol., 33: 968-978.
Jiang, H; Yu, Y; Yang, R; Zhang, S; Wang, D; Jiang, Y; Yang, W; Huang, H; Shi, C; Ye, L and Yang, G (2021). Detection and molecular epidemiology of canine parvovirus type 2 (CPV-2) circulating in Jilin Province, Northeast China. Comp. Immunol. Microbiol. Infect. Dis., 74: 101602.
Kang, BK; Song, DS; Lee, CS; Jung, KI; Park, SJ; Kim, EM and Park, BK (2008). Prevalence and genetic characterization of canine parvoviruses in Korea. Virus Genes. 36: 127-133.
Kaur, G; Chandra, M and Dwivedi, PN (2016). Phylogenetic analysis of VP2 gene of canine parvovirus and comparison with Indian and world isolates. Acta Virol., 60: 106-110.
Kaur, G; Chandra, M; Dwivedi, PN and Sharma, NS (2015). Isolation of canine parvovirus with a view to identify the prevalent serotype on the basis of partial sequence analysis. Vet. World. 8: 52-56.
Kulkarni, MB; Deshpande, AR; Gaikwad, SS; Majee, SB and Awandkar, SP (2019). Molecular epidemiology of canine parvovirus shows CPV-2a genotype circulating in dogs from western India. Infect. Genet. Evol., 75: 103987.
Li, C; Tang, J; Chen, Z; Niu, G and Liu, G (2019). A divergent canine parvovirus type 2c (CPV-2c) isolate circulating in China. Infect. Genet. Evol., 73: 242-247.
Manh, TN; Piewbang, C; Rungsipipat, A and Techangamsuwan, S (2021). Molecular and phylogenetic analysis of Vietnamese canine parvovirus 2C originated from dogs reveals a new Asia-IV clade. Transbound. Emerg. Dis., 68: 1445-1453.
Miranda, C and Thompson, G (2016). Canine parvovirus: the worldwide occurrence of antigenic variants. J. Gen. Virol., 97: 2043-2057.
Mukhopadhyay, HK; Matta, SL; Amsaveni, S; Antony, PX; Thanislass, J and Pillai, RM (2014). Phylogenetic analysis of canine parvovirus partial VP2 gene in India. Virus Genes. 48: 89-95.
Nakamura, M; Tohya, Y; Miyazawa, T; Mochizuki, M; Phung, HT; Nguyen, NH; Huynh, LM; Nguyen, LT; Nguyen, PN; Nguyen, PV and Nguyen, NP (2004). A novel antigenic variant of canine parvovirus from a Vietnamese dog. Arch. Virol., 149: 2261-2270.
Nandi, S; Chidri, S; Kumar, M and Chauhan, RS (2010). Occurrence of canine parvovirus type 2c in the dogs with haemorrhagic enteritis in India. Res. Vet. Sci., 88: 169-171.
Nguyen, SV; Umeda, K; Yokoyama, H; Tohya, Y and Kodama, Y (2006). Passive protection of dogs against
clinical disease due to canine parvovirus-2 by specific antibody from chicken egg yolk. Can. J. Vet. Res., 70: 62-64.
Parrish, CR; Aquadro, CF; Strassheim, ML; Evermann, JF; Sgro, JY and Mohammed, HO (1991). Rapid antigenic type replacement and DNA sequence evolution of canine parvovirus. J. Virol., 65: 6544-6552.
Phromnoi, S; Sirinarumitr, K and Sirinarumitr, T (2010). Sequence analysis of VP2 gene of canine parvovirus isolates in Thailand. Virus Genes. 41: 23-29.
Qi, S; Zhao, J; Guo, D and Sun, D (2020). A mini-review on the epidemiology of canine parvovirus in China. Front. Vet. Sci., 7: 5-15
Saitou, N and Nei, M (1987). The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol., 4: 406-425.
Schoeman, JP; Goddard, A and Leisewitz, AL (2013). Biomarkers in canine parvovirus enteritis. N. Z. Vet. J., 61: 217-222.
Sharma, S; Dhar, P; Thakur, A; Sharma, V and Sharma, M (2016). First detection of canine parvovirus type 2b from diarrheic dogs in Himachal Pradesh. Vet. World. 9: 964-969.
Tamura, K; Peterson, D; Peterson, N; Stecher, G; Nei, M and Kumar, S (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol., 28: 2731-2739.
Thomas, J; Singh, M; Goswami, TK and Verma, S (2017). Phylogenetic analysis of the partial VP2 gene of canine parvovirus-2 from the northern region of India. Vet. Arh., 87: 57-66.
Weaver, S; Shank, SD; Spielman, SJ; Li, M; Muse, SV and Pond, SLK (2018). Datamonkey 2.0: a modern web application for characterizing selective and other evolutionary processes. Mol. Biol. Evol., 35: 773-777.
Xu, J; Guo, HC; Wei, YQ; Shu, L; Wang, J; Li, JS; Cao, SZ and Sun, SQ (2015). Phylogenetic analysis of canine parvovirus isolates from Sichuan and Gansu provinces of China in 2011. Transbound. Emerg. Dis., 62: 91-105.
Zhao, Z; Liu, H; Ding, K; Peng, C; Xue, Q; Yu, Z and Xue, Y (2016). Occurrence of canine parvovirus in dogs from Henan province of China in 2009-2014. BMC Vet. Res., 12: 138-146.
Zhou, P; Zeng, W; Zhang, X and Li, S (2017). The genetic evolution of canine parvovirus – A new perspective. PLoS One. 12: e0175035.