Simultaneous detection and phylogenetic analysis of porcine epidemic diarrhea virus and porcine circovirus 4 in Henan province, China.
Journal
Archives of virology
ISSN: 1432-8798
Titre abrégé: Arch Virol
Pays: Austria
ID NLM: 7506870
Informations de publication
Date de publication:
13 May 2023
13 May 2023
Historique:
received:
16
09
2022
accepted:
20
04
2023
medline:
15
5
2023
pubmed:
14
5
2023
entrez:
13
5
2023
Statut:
epublish
Résumé
Porcine circovirus 4 (PCV4) is a recently discovered circovirus that was first reported in 2019 in several pigs in Hunan province of China and has also been identified in pigs infected with porcine epidemic diarrhea virus (PEDV). To further investigate the coinfection and genetic diversity of these two viruses, 65 clinical samples (including feces and intestinal tissues) were collected from diseased piglets on 19 large-scale pig farms in Henan province of China, and a duplex SYBR Green I-based quantitative real-time polymerase chain reaction (qPCR) assay was developed for detecting PEDV and PCV4 simultaneously. The results showed that the limit of detection was 55.2 copies/μL and 44.1 copies/μL for PEDV and PCV4, respectively. The detection rate for PEDV and PCV4 was 40% (26/65) and 38% (25/65), respectively, and the coinfection rate for the two viruses was 34% (22/65). Subsequently, the full-length spike (S) gene of eight PEDV strains and a portion of the genome containing the capsid (Cap) gene of three PCV4 strains were sequenced and analyzed. Phylogenetic analysis showed that all of the PEDV strains from the present study clustered in the G2a subgroup and were closely related to most of the PEDV reference strains from China from 2011 to 2021, but they differed genetically from a vaccine strain (CV777), a Korean strain (virulent DR1), and two Chinese strains (SD-M and LZC). It is noteworthy that two PEDV strains (HEXX-24 and HNXX-24XIA) were identified in one sample, and the HNXX-24XIA strain had a large deletion at amino acids 31-229 of the S protein. Moreover, a recombination event was observed in strain HEXX-24. Phylogenetic analysis based on the amino acid sequence of the PCV4 Cap protein revealed that PCV4 strains were divided into three genotypes: PCV4a1, PCV4a2, and PCV4b. Three strains in the present study belonged to PCV4a1, and they had a high degree of sequence similarity (>98% identity) to other PCV4 reference strains. This study not only provides technical support for field investigation of PEDV and PCV4 coinfection but also provides data for their prevention and control.
Identifiants
pubmed: 37179263
doi: 10.1007/s00705-023-05791-w
pii: 10.1007/s00705-023-05791-w
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
161Subventions
Organisme : National Key Research and Development Program
ID : No.2021YFD1801105
Organisme : Henan open competition mechanism to select the best candidates Program
ID : No. 211110111000
Organisme : Program for Scientific and Technological Innovation Talents in Universities of Ministry of Education of Henan Province
ID : No. 21HASTIT039
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Austria, part of Springer Nature.
Références
Hamel AL, Lin LL, Nayar GP (1998) Nucleotide sequence of porcine circovirus associated with postweaning multisystemic wasting syndrome in pigs. J Virol 72:5262–5267
pubmed: 9573301
pmcid: 110114
doi: 10.1128/JVI.72.6.5262-5267.1998
Brian DA, Baric RS (2005) Coronavirus genome structure and replication. Curr Top Microbiol Immunol 287:1–30
pubmed: 15609507
Chang L, Jian T, Yuanmei Ma, Xueya L, Yang G (2015) Receptor usage and cell entry of porcine epidemic diarrhea coronavirus. J Virol 89:6121–6125
doi: 10.1128/JVI.00430-15
Chen P, Wang K, Hou Y, Li H, Li X, Yu L, Jiang Y, Gao F, Tong W, Yu H (2019) Genetic evolution analysis and pathogenicity assessment of porcine epidemic diarrhea virus strains circulating in part of China during 2011–2017. Infect Genet Evol 69:153–165
pubmed: 30677534
pmcid: 7106134
doi: 10.1016/j.meegid.2019.01.022
Cheung AK (2012) Porcine circovirus: transcription and DNA replication. Virus Res 164:46–53
pubmed: 22036834
doi: 10.1016/j.virusres.2011.10.012
Cui JT, Qiao H, Hou CY, Zheng HH, Li XS, Zheng LL, Chen HY (2020) Characteristics of the spike and ORF3 genes of porcine epidemic diarrhea virus in Henan and Shanxi provinces of China. Adv Virol 165:2323–2333
Debouck P, Pensaert M, Coussement W (1981) The pathogenesis of an enteric infection in pigs, experimentally induced by the coronavirus-like agent, CV 777. Vet Microbiol 6:157–165
pmcid: 7117293
doi: 10.1016/0378-1135(81)90007-9
Diep NV, Norimine J, Sueyoshi M, Lan NT, Yamaguchi R (2017) Novel porcine epidemic diarrhea virus (PEDV) variants with large deletions in the spike (S) gene coexist with PEDV strains possessing an intact S gene in domestic pigs in Japan: a new disease situation. PLoS ONE 12:e0170126
pubmed: 28095455
pmcid: 5241010
doi: 10.1371/journal.pone.0170126
Dupont K, Nielsen E, Baekbo P, Larsen L (2008) Genomic analysis of PCV2 isolates from Danish archives and a current PMWS case–control study supports a shift in genotypes with time. Vet Microbiol 128:56–64
pubmed: 17996404
doi: 10.1016/j.vetmic.2007.09.016
Fu X, Fang B, Ma J, Liu Y, Bu D, Zhou P, Wang H, Jia K, Zhang G (2018) Insights into the epidemic characteristics and evolutionary history of the novel porcine circovirus type 3 in southern China. Transbound Emerg Dis 65:e296–e303
pubmed: 29178283
doi: 10.1111/tbed.12752
Guo J, Fang L, Ye X, Chen J, Xu S, Zhu X, Miao Y, Wang D, Xiao S (2019) Evolutionary and genotypic analyses of global porcine epidemic diarrhea virus strains. Transbound Emerg Dis 66:111–118
pubmed: 30102851
doi: 10.1111/tbed.12991
Ha Z, Yu C, Xie C, Wang G, Zhang Y, Hao P, Li J, Li Z, Li Y, Rong F (2021) Retrospective surveillance of porcine circovirus 4 in pigs in Inner Mongolia, China, from 2016 to 2018. Adv Virol 166:1951–1959
Hou C-Y, Xu T, Zhang L-H, Cui J-T, Zhang Y-H, Li X-S, Zheng L-L, Chen H-Y (2021) Simultaneous detection and differentiation of porcine circovirus 3 and 4 using a SYBR Green I-based duplex quantitative PCR assay. J Virol Methods 293:114152
pubmed: 33845107
doi: 10.1016/j.jviromet.2021.114152
Hou CY, Zhang LH, Zhang YH, Cui JT, Zhao L, Zheng LL, Chen HY (2022) Phylogenetic analysis of porcine circovirus 4 in Henan province of China: a retrospective study from 2011 to 2021. Transbound Emerg Dis 69:1890–1901
pubmed: 34076964
doi: 10.1111/tbed.14172
Hou Y, Lin CM, Yokoyama M, Yount BL, Marthaler D, Douglas AL, Ghimire S, Qin Y, Baric RS, Saif LJ, Wang Q (2017) Deletion of a 197-amino-acid region in the N-terminal domain of spike protein attenuates porcine epidemic diarrhea virus in piglets. J Virol 91:e00227–17
Kwan E, Carrai M, Lanave G, Hill J, Parry K, Kelman M, Meers J, Decaro N, Beatty JA, Martella V, Barrs VR (2021) Analysis of canine parvoviruses circulating in Australia reveals predominance of variant 2b and identifies feline parvovirus-like mutations in the capsid proteins. Transbound Emerg Dis 68:656–666
pubmed: 32657506
doi: 10.1111/tbed.13727
Lekcharoensuk P, Morozov I, Paul PS, Thangthumniyom N, Wajjawalku W, Meng XJ (2004) Epitope mapping of the major capsid protein of type 2 porcine circovirus (PCV2) by using chimeric PCV1 and PCV2. J Virol 78:8135–8145
pubmed: 15254185
pmcid: 446101
doi: 10.1128/JVI.78.15.8135-8145.2004
Li D, Feng H, Liu Y, Chen Y, Wei Q, Wang J, Liu D, Huang H, Su Y, Wang D, Cui Y, Zhang G (2018) Molecular evolution of porcine epidemic diarrhea virus and porcine deltacoronavirus strains in Central China. Res Vet Sci 120:63–69
pubmed: 30265872
pmcid: 7111851
doi: 10.1016/j.rvsc.2018.06.001
Li W, Li H, Liu Y, Pan Y, Deng F, Song Y, Tang X, He Q (2012) New variants of porcine epidemic diarrhea virus, China, 2011. Emerg Infect Dis 18:1350
pubmed: 22840964
pmcid: 3414035
doi: 10.3201/eid1803.120002
Lin CM, Saif LJ, Marthaler D, Wang Q (2016) Evolution, antigenicity and pathogenicity of global porcine epidemic diarrhea virus strains. Virus Res 226:20–39
pubmed: 27288724
doi: 10.1016/j.virusres.2016.05.023
Nayar GPS, Hamel A, Lin L (1997) Detection and characterization of porcine circovirus associated with postweaning multisystemic wasting syndrome in pigs. Can Vet J 38:385–386
pubmed: 9187809
pmcid: 1576874
Nguyen VG, Do HQ, Huynh TML, Park YH, Park BK, Chung HC (2022) Molecular-based detection, genetic characterization and phylogenetic analysis of porcine circovirus 4 from Korean domestic swine farms. Transbound Emerg Dis 69:538–548
pubmed: 33529468
doi: 10.1111/tbed.14017
Niu G, Zhang X, Ji W, Chen S, Li X, Yang L, Zhang L, Ouyang H, Li C, Ren L (2022) Porcine circovirus 4 rescued from an infectious clone is replicable and pathogenic in vivo. Transbound Emerg Dis 69:e1632–e1641
pubmed: 35240007
doi: 10.1111/tbed.14498
Oka T, Saif LJ, Marthaler D, Esseili MA, Meulia T, Lin CM, Vlasova AN, Jung K, Zhang Y, Wang Q (2014) Cell culture isolation and sequence analysis of genetically diverse US porcine epidemic diarrhea virus strains including a novel strain with a large deletion in the spike gene. Vet Microbiol 173:258–269
pubmed: 25217400
pmcid: 7126216
doi: 10.1016/j.vetmic.2014.08.012
Pan Y, Tian X, Li W, Zhou Q, Wang D, Bi Y, Chen F, Song Y (2012) Isolation and characterization of a variant porcine epidemic diarrhea virus in China. Virol J 9:195
pubmed: 22967434
pmcid: 3487931
doi: 10.1186/1743-422X-9-195
Parrish CR, Have P, Foreyt WJ, Evermann JF, Senda M, Carmichael LE (1988) The global spread and replacement of canine parvovirus strains. J Gen Virol 69(Pt 5):1111–1116
pubmed: 2836554
doi: 10.1099/0022-1317-69-5-1111
Parrish CR, Aquadro CF, Strassheim ML, Evermann JF, Sgro JY, Mohammed HO (1991) Rapid antigenic-type replacement and DNA sequence evolution of canine parvovirus. J Virol 65:6544–6552
pubmed: 1942246
pmcid: 250707
doi: 10.1128/jvi.65.12.6544-6552.1991
Phan TG, Giannitti F, Rossow S, Marthaler D, Knutson T, Li L, Deng X, Resende T, Vannucci F, Delwart E (2016) Detection of a novel circovirus PCV3 in pigs with cardiac and multi-systemic inflammation. Virol J 13:184
pubmed: 27835942
pmcid: 5105309
doi: 10.1186/s12985-016-0642-z
Segalés J (2012) Porcine circovirus type 2 (PCV2) infections: clinical signs, pathology and laboratory diagnosis. Virus Res 164:10–19
pubmed: 22056845
doi: 10.1016/j.virusres.2011.10.007
Sun D, Feng L, Shi H, Chen J, Cui X, Chen H, Liu S, Tong Y, Wang Y, Tong G (2008) Identification of two novel B cell epitopes on porcine epidemic diarrhea virus spike protein. Vet Microbiol 131:73–81
pubmed: 18400422
pmcid: 7117171
doi: 10.1016/j.vetmic.2008.02.022
Sun W, Du Q, Han Z, Bi J, Zheng M (2020) Detection and genetic characterization of porcine circovirus 4 (PCV4) in Guangxi, China. Gene 773:145384
pubmed: 33383119
doi: 10.1016/j.gene.2020.145384
Sun W, Du Q, Han Z, Bi J, Lan T, Wang W, Zheng M (2021) Detection and genetic characterization of porcine circovirus 4 (PCV4) in Guangxi, China. Gene 773:145384
pubmed: 33383119
doi: 10.1016/j.gene.2020.145384
Tian RB, Zhao Y, Cui JT, Zheng HH, Xu T, Hou CY, Wang ZY, Li XS, Zheng LL, Chen HY (2021) Molecular detection and phylogenetic analysis of porcine circovirus 4 in Henan and Shanxi Provinces of China. Transbound Emerg Dis 68:276–282
pubmed: 32634296
doi: 10.1111/tbed.13714
Tischer I, Mields W, Wolff D, Vagt M, Griem W (1986) Studies on epidemiology and pathogenicity of porcine circovirus. Adv Virol 91:271–276
Tohru S, Yutaka T, Luis E, Seiichi O, Wataru K (2018) S1 subunit of spike protein from a current highly virulent porcine epidemic diarrhea virus is an important determinant of virulence in piglets. Viruses 10:467
doi: 10.3390/v10090467
Wang D, Mai J, Lei B, Zhang Y, Wang N (2021) Structure, antigenic properties, and highly efficient assembly of PCV4 capsid protein. Front Vet Sci 8:695466
pubmed: 34504886
pmcid: 8421537
doi: 10.3389/fvets.2021.695466
Wang E, Guo D, Li C, Shan W, Sun D (2016) Molecular characterization of the ORF3 and S1 genes of porcine epidemic diarrhea virus non S-INDEL strains in seven regions of China, 2015. PLoS ONE 11:e0160561
pubmed: 27494026
pmcid: 4975444
doi: 10.1371/journal.pone.0160561
Wang L, Byrum B, Zhang Y (2014) New variant of porcine epidemic diarrhea virus, United States, 2014. Emerg Infect Dis 20:917
pubmed: 24750580
pmcid: 4012824
doi: 10.3201/eid2005.140195
Wei R, Trus I, Yang B, Huang L, Nauwynck HJ (2018) Breed differences in PCV2 uptake and disintegration in porcine monocytes. Viruses 10:562
pubmed: 30326643
pmcid: 6213064
doi: 10.3390/v10100562
Xu T, Hou C-Y, Zhang Y-H, Li H-X, Chen X-M, Pan J-J, Chen H-Y (2022) Simultaneous detection and genetic characterization of porcine circovirus 2 and 4 in Henan province of China. Gene 808:145991
pubmed: 34626723
doi: 10.1016/j.gene.2021.145991
Zhang D, Bai C, Ge K, Li Y, Gao W, Jiang S, Wang Y (2020) Establishment of an SYBR Green-based real-time PCR assay for porcine circovirus type 4 detection. J Virol Methods 285:113963
pubmed: 32882322
doi: 10.1016/j.jviromet.2020.113963
Zhang H, Hu W, Li J, Liu T, Xiao C (2020) Novel circovirus species identified in farmed pigs designated as Porcine circovirus 4, Hunan province, China. Transbound Emerg Dis 67:1057–1061
Zhang H, Han F, Shu X, Li Q, Ding Q, Hao C, Yan X, Xu M, Hu H (2022) Co-infection of porcine epidemic diarrhoea virus and porcine deltacoronavirus enhances the disease severity in piglets. Transbound Emerg Dis 69:1715–1726
pubmed: 33960702
doi: 10.1111/tbed.14144
Zhang J, Yim-Im W, Chen Q, Zheng Y, Schumacher L, Huang H, Gauger P, Harmon K, Li G (2018) Identification of porcine epidemic diarrhea virus variant with a large spike gene deletion from a clinical swine sample in the United States. Virus Genes 54:323–327
pubmed: 29468451
pmcid: 7088737
doi: 10.1007/s11262-018-1542-7
Zhang Y, Cheng Y, Xing G, Yu J, Liao A, Du L, Lei J, Lian X, Zhou J, Gu J (2019) Detection and spike gene characterization in porcine deltacoronavirus in China during 2016–2018. Infect Genet Evol 73:151–158
pubmed: 31026605
pmcid: 7106087
doi: 10.1016/j.meegid.2019.04.023
Zhang YH, Li HX, Chen XM, Zhang LH, Zhao YY, Luo AF, Yang YR, Zheng LL, Chen HY (2022) Genetic characteristics and pathogenicity of a novel porcine epidemic diarrhea virus with a naturally occurring truncated ORF3 gene. Viruses 14:487
pubmed: 35336894
pmcid: 8955810
doi: 10.3390/v14030487
Zhao Z, Liu H, Ding K, Peng C, Xue Q, Yu Z, Xue Y (2016) Occurrence of canine parvovirus in dogs from Henan province of China in 2009–2014. BMC Vet Res 12:138
pubmed: 27377264
pmcid: 4932751
doi: 10.1186/s12917-016-0753-1
Zheng L-L, Cui J-T, Han H-Y, Hou H-L, Wang L, Liu F, Chen H-Y (2020) Development of a duplex SYBR Green I based real-time PCR assay for detection of porcine epidemic diarrhea virus and porcine bocavirus3/4/5. Mol Cell Probes 51:101544
pubmed: 32109535
doi: 10.1016/j.mcp.2020.101544
Zhou J, Qiu Y, Zhu N, Zhou L, Dai B, Feng X, Hou L, Liu J (2021) The nucleolar localization signal of porcine circovirus type 4 capsid protein is essential for interaction with serine-48 residue of nucleolar phosphoprotein nucleophosmin-1. Front Microbiol 12:751382
pubmed: 34745055
pmcid: 8566881
doi: 10.3389/fmicb.2021.751382