Top

Virology Journal

Published in:

Open Access 01-12-2022 | Tremor | Research

Genetic characterization of atypical porcine pestivirus from neonatal piglets with congenital tremor in Hubei province, China

Authors: Xujiao Ren, Ping Qian, Zihui Hu, Huanchun Chen, Xiangmin Li

Published in: Virology Journal | Issue 1/2022

Abstract

Background

Atypical porcine pestivirus (APPV) is a single-stranded RNA virus with high genetic variation that causes congenital tremor (CT) in newborn piglets, belonging to the genus Pestivirus of the family Flaviviridae. Increasing cases of APPV infection in China in the past few years would pose severe challenges to the development of pig production. In view of the high genetic variability of APPV, the genetic characteristics of APPV in Hubei province was determined.

Methods

52 tissue samples from 8 CT-affected newborn piglets were collected at two different periods in the same pig farm in Hubei province. Viral nucleic acid was extracted to detect pathogens that can cause CT in piglets or other common clinical pathogens by RT-PCR. Haematoxylin and eosin (HE) staining, immunohistochemical (IHC) analysis, and qRT-PCR were performed to observe histopathological changes and histological distribution, and detect the viral load of APPV in CT-affected piglets. The full-length genome of APPV was obtained and sequence analysis was conducted to determine the phylogenetic relationship.

Results

Histopathological observation and histological distribution analysis showed that the histological lesions and distribution of APPV were mainly in central nervous system (CNS) tissues and immune tissues. Viral load analysis revealed that the viral copy number was higher in the cerebellum, submaxillary lymph nodes, tonsil, and serum than in other tissues. Phylogenetic analysis showed that CH-HB2020 and CH-HB2021 belonged to Clade I.3, and is most closely related to APPV_CH-GX2016. Sequence alignment based on APPV encoding sequences (CDS) showed that the nucleotide identities of CH-HB2020 or CH-HB2021 with Clade I, Clade II, and Clade III strains were 83.5–98.6%, 83.1–83.5%, and 81.1–81.4%, respectively, while the amino acid identities were 91.9–99.2%, 91.2–95.3%, and 90.77–91.4%, respectively. No recombination event was observed in CH-HB2020 or CH-HB2021 strains.

Conclusions

These findings enhance our understanding of the pathogenesis of APPV and may provide potential molecular evidence for its prevalence and transmission.

Available only for authorised users

Hause BM, Collin EA, Peddireddi L, Yuan F, Chen Z, Hesse RA, Gauger PC, Clement T, Fang Y, Anderson G. Discovery of a novel putative atypical porcine pestivirus in pigs in the USA. J Gen Virol. 2015;96(10):2994–8. https://doi.org/10.1099/jgv.0.000251.PubMedCrossRef

Smith DB, Meyers G, Bukh J, Gould EA, Monath T, Scott Muerhoff A, Pletnev A, Rico-Hesse R, Stapleton JT, Simmonds P, Becher P. Proposed revision to the taxonomy of the genus Pestivirus, family Flaviviridae. J Gen Virol. 2017;98(8):2106–12. https://doi.org/10.1099/jgv.0.000873.PubMedPubMedCentralCrossRef

Lamp B, Schwarz L, Högler S, Riedel C, Sinn L, Rebel-Bauder B, Weissenböck H, Ladinig A, Rümenapf T. Novel pestivirus species in Pigs, Austria, 2015. Emerg Infect Dis. 2017;23:1176–9. https://doi.org/10.3201/eid2307.170163.PubMedPubMedCentralCrossRef

Pan S, Mou C, Chen Z. An emerging novel virus: atypical porcine pestivirus (APPV). Rev Med Virol. 2019;29(1): e2018. https://doi.org/10.1002/rmv.2018.PubMedCrossRef

Stark R, Meyers G, Rümenapf T, Thiel HJ. Processing of pestivirus polyprotein: cleavage site between autoprotease and nucleocapsid protein of classical swine fever virus. J Virol. 1993;67(12):7088–95. https://doi.org/10.1128/JVI.67.12.7088-7095.1993.PubMedPubMedCentralCrossRef

Tautz N, Tews BA, Meyers G. The molecular biology of pestiviruses. Adv Virus Res. 2015;93:47–160. https://doi.org/10.1016/bs.aivir.2015.03.002.PubMedCrossRef

de Groof A, Deijs M, Guelen L, van Grinsven L, van Os-Galdos L, Vogels W, Derks C, Cruijsen T, Geurts V, Vrijenhoek M, et al. Atypical porcine pestivirus: a possible cause of congenital tremor type A-II in newborn piglets. Viruses. 2016. https://doi.org/10.3390/v8100271.PubMedPubMedCentralCrossRef

Postel A, Hansmann F, Baechlein C, Fischer N, Alawi M, Grundhoff A, Derking S, Tenhundfeld J, Pfankuche VM, Herder V, et al. Presence of atypical porcine pestivirus (APPV) genomes in newborn piglets correlates with congenital tremor. Sci Rep. 2016;6:27735. https://doi.org/10.1038/srep27735.PubMedPubMedCentralCrossRef

Dénes L, Biksi I, Albert M, Szeredi L, Knapp DG, Szilasi A, Bálint Á, Balka G. Detection and phylogenetic characterization of atypical porcine pestivirus strains in Hungary. Transbound Emerg Dis. 2018;65(6):2039–42. https://doi.org/10.1111/tbed.12981.PubMedCrossRef

10.

Dessureault FG, Choinière M, Provost C, Gagnon CA. First report of atypical porcine pestivirus in piglets with congenital tremor in Canada. Can Vet J. 2018;59(4):429–32.PubMedPubMedCentral

11.

Mósena ACS, Weber MN, da Cruz RAS, Cibulski SP, da Silva MS, Puhl DE, Hammerschmitt ME, Takeuti KL, Driemeier D, de Barcellos D, Canal CW. Presence of atypical porcine pestivirus (APPV) in Brazilian pigs. Transbound Emerg Dis. 2018;65(1):22–6. https://doi.org/10.1111/tbed.12753.PubMedCrossRef

12.

Muñoz-González S, Canturri A, Pérez-Simó M, Bohórquez JA, Rosell R, Cabezón O, Segalés J, Domingo M, Ganges L. First report of the novel atypical porcine pestivirus in Spain and a retrospective study. Transbound Emerg Dis. 2017;64(6):1645–9. https://doi.org/10.1111/tbed.12699.PubMedCrossRef

13.

Schwarz L, Riedel C, Högler S, Sinn LJ, Voglmayr T, Wöchtl B, Dinhopl N, Rebel-Bauder B, Weissenböck H, Ladinig A, et al. Congenital infection with atypical porcine pestivirus (APPV) is associated with disease and viral persistence. Vet Res. 2017;48(1):1. https://doi.org/10.1186/s13567-016-0406-1.PubMedPubMedCentralCrossRef

14.

Zhang K, Wu K, Liu J, Ge S, Xiao Y, Shang Y, Ning Z. Identification of atypical porcine pestivirus infection in swine herds in China. Transbound Emerg Dis. 2017;64(4):1020–3. https://doi.org/10.1111/tbed.12659.PubMedCrossRef

15.

Kasahara-Kamiie M, Kagawa M, Shiokawa M, Sunaga F, Fukase Y, Aihara N, Shiga T, Kamiie J, Aoki H, Nagai M. Detection and genetic analysis of a novel atypical porcine pestivirus from piglets with congenital tremor in Japan. Transbound Emerg Dis. 2021. https://doi.org/10.1111/tbed.14149.PubMedCrossRef

16.

Ku X, Chen F, Li P, Wang Y, Yu X, Fan S, Qian P, Wu M, He Q. Identification and genetic characterization of porcine circovirus type 3 in China. Transbound Emerg Dis. 2017;64(3):703–8. https://doi.org/10.1111/tbed.12638.PubMedPubMedCentralCrossRef

17.

Chen Y, Xu Q, Chen H, Luo X, Wu Q, Tan C, Pan Q, Chen JL. Evolution and genetic diversity of porcine circovirus 3 in China. Viruses. 2019. https://doi.org/10.3390/v11090786.PubMedPubMedCentralCrossRef

18.

Chen GH, Mai KJ, Zhou L, Wu RT, Tang XY, Wu JL, He LL, Lan T, Xie QM, Sun Y, Ma JY. Detection and genome sequencing of porcine circovirus 3 in neonatal pigs with congenital tremors in South China. Transbound Emerg Dis. 2017;64(6):1650–4. https://doi.org/10.1111/tbed.12702.PubMedCrossRef

19.

Yang T, Yu X, Luo B, Yan M, Li R, Qu T, Ren X. Epidemiology and molecular characterization of Porcine teschovirus in Hunan, China. Transbound Emerg Dis. 2018;65(2):480–90. https://doi.org/10.1111/tbed.12728.PubMedCrossRef

20.

Liu J, Li Z, Ren X, Li H, Lu R, Zhang Y, Ning Z. Viral load and histological distribution of atypical porcine pestivirus in different tissues of naturally infected piglets. Arch Virol. 2019;164(10):2519–23. https://doi.org/10.1007/s00705-019-04345-3.PubMedCrossRef

21.

Ren X, Qian P, Liu S, Chen H, Li X. Fc-mediated E2-dimer subunit vaccines of atypical porcine pestivirus induce efficient humoral and cellular immune responses in piglets. Viruses. 2021. https://doi.org/10.3390/v13122443.PubMedPubMedCentralCrossRef

22.

Liu J, Ren X, Li H, Yu X, Zhao B, Liu B, Ning Z. Development of the reverse genetics system for emerging atypical porcine pestivirus using in vitro and intracellular transcription systems. Virus Res. 2020. https://doi.org/10.1016/j.virusres.2020.197975.PubMedPubMedCentralCrossRef

23.

Zhang H, Wen W, Hao G, Chen H, Qian P, Li X. A subunit vaccine based on E2 protein of atypical porcine pestivirus induces Th2-type immune response in mice. Viruses. 2018. https://doi.org/10.3390/v10120673.PubMedPubMedCentralCrossRef

24.

Zhang H, Wen W, Hao G, Hu Y, Chen H, Qian P, Li X. Phylogenetic and genomic characterization of a novel atypical porcine pestivirus in China. Transbound Emerg Dis. 2018;65(1):e202–4. https://doi.org/10.1111/tbed.12675.PubMedCrossRef

25.

Tamura K, Stecher G, Kumar S. MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol. 2021;38:3022–7. https://doi.org/10.1093/molbev/msab120.PubMedPubMedCentralCrossRef

26.

Guo Z, Wang L, Qiao S, Deng R, Zhang G. Genetic characterization and recombination analysis of atypical porcine pestivirus. Infect Genet Evol. 2020;81: 104259. https://doi.org/10.1016/j.meegid.2020.104259.PubMedCrossRef

27.

Cagatay GN, Antos A, Suckstorff O, Isken O, Tautz N, Becher P, Postel A. Porcine complement regulatory protein cd46 is a major receptor for atypical porcine pestivirus but not for classical swine fever virus. J Virol. 2021. https://doi.org/10.1128/jvi.02186-20.PubMedPubMedCentralCrossRef

28.

Li J, Li X, Ma H, Ren X, Hao G, Zhang H, Zhao Z, Fang K, Li X, Rong Z, et al. Efficient mucosal vaccination of a novel classical swine fever virus E2-Fc fusion protein mediated by neonatal Fc receptor. Vaccine. 2020;38(29):4574–83. https://doi.org/10.1016/j.vaccine.2020.05.013.PubMedCrossRef

29.

Kinsley AT. Dancing pigs? Vet Med. 1922;17:123.

30.

Gatto IRH, Harmon K, Bradner L, Silva P, Linhares DCL, Arruda PH, de Oliveira LG, Arruda BL. Detection of atypical porcine pestivirus in Brazil in the central nervous system of suckling piglets with congenital tremor. Transbound Emerg Dis. 2018;65(2):375–80. https://doi.org/10.1111/tbed.12824.PubMedCrossRef

31.

Mou C, Pan S, Wu H, Chen Z. Disruption of interferon-β production by the N(pro) of atypical porcine pestivirus. Virulence. 2021;12(1):654–65. https://doi.org/10.1080/21505594.2021.1880773.PubMedPubMedCentralCrossRef

32.

Zhang Q, Yu Y, Song C, Cao Z. Genetic characterization of atypical porcine pestivirus (APPV) in China and the successful isolation of a novel APPV strain within genotype 2. Microb Pathog. 2021;161(Pt A): 105282. https://doi.org/10.1016/j.micpath.2021.105282.PubMedCrossRef

33.

Beer M, Wernike K, Dräger C, Höper D, Pohlmann A, Bergermann C, Schröder C, Klinkhammer S, Blome S, Hoffmann B. High prevalence of highly variable atypical porcine pestiviruses found in Germany. Transbound Emerg Dis. 2017;64(5):e22–6. https://doi.org/10.1111/tbed.12532.PubMedCrossRef

34.

Yuan J, Han Z, Li J, Huang Y, Yang J, Ding H, Zhang J, Zhu M, Zhang Y, Liao J, et al. Atypical porcine pestivirus as a novel type of pestivirus in pigs in China. Front Microbiol. 2017;8:862. https://doi.org/10.3389/fmicb.2017.00862.PubMedPubMedCentralCrossRef

35.

Yan XL, Li YY, He LL, Wu JL, Tang XY, Chen GH, Mai KJ, Wu RT, Li QN, Chen YH, et al. 12 novel atypical porcine pestivirus genomes from neonatal piglets with congenital tremors: a newly emerging branch and high prevalence in China. Virology. 2019;533:50–8. https://doi.org/10.1016/j.virol.2019.04.010.PubMedCrossRef

36.

Arruda BL, Arruda PH, Magstadt DR, Schwartz KJ, Dohlman T, Schleining JA, Patterson AR, Visek CA, Victoria JG. Identification of a divergent lineage porcine pestivirus in nursing piglets with congenital tremors and reproduction of disease following experimental inoculation. PLoS ONE. 2016;11(2): e0150104. https://doi.org/10.1371/journal.pone.0150104.PubMedPubMedCentralCrossRef

37.

Gatto IRH, Arruda PH, Visek CA, Victoria JG, Patterson AR, Krull AC, Schwartz KJ, de Oliveira LG, Arruda BL. Detection of atypical porcine pestivirus in semen from commercial boar studs in the United States. Transbound Emerg Dis. 2018;65(2):e339–43. https://doi.org/10.1111/tbed.12759.PubMedCrossRef

38.

Szymanski MR, Fiebach AR, Tratschin JD, Gut M, Ramanujam VM, Gottipati K, Patel P, Ye M, Ruggli N, Choi KH. Zinc binding in pestivirus N(pro) is required for interferon regulatory factor 3 interaction and degradation. J Mol Biol. 2009;391(2):438–49. https://doi.org/10.1016/j.jmb.2009.06.040.PubMedCrossRef

39.

Gil LH, Ansari IH, Vassilev V, Liang D, Lai VC, Zhong W, Hong Z, Dubovi EJ, Donis RO. The amino-terminal domain of bovine viral diarrhea virus Npro protein is necessary for alpha/beta interferon antagonism. J Virol. 2006;80(2):900–11. https://doi.org/10.1128/jvi.80.2.900-911.2006.PubMedPubMedCentralCrossRef

40.

La Rocca SA, Herbert RJ, Crooke H, Drew TW, Wileman TE, Powell PP. Loss of interferon regulatory factor 3 in cells infected with classical swine fever virus involves the N-terminal protease, Npro. J Virol. 2005;79(11):7239–47. https://doi.org/10.1128/jvi.79.11.7239-7247.2005.PubMedPubMedCentralCrossRef

41.

Charleston B, Fray MD, Baigent S, Carr BV, Morrison WI. Establishment of persistent infection with non-cytopathic bovine viral diarrhoea virus in cattle is associated with a failure to induce type I interferon. J Gen Virol. 2001;82(Pt 8):1893–7. https://doi.org/10.1099/0022-1317-82-8-1893.PubMedCrossRef

42.

Liu J, Zhang P, Chen Y, Zhong W, Li B, Pi M, Ning Z. Vaccination with virus-like particles of atypical porcine pestivirus inhibits virus replication in tissues of BALB/c mice. Arch Virol. 2021;166(10):2733–41. https://doi.org/10.1007/s00705-021-05185-w.PubMedPubMedCentralCrossRef

43.

Possatti F, Headley SA, Leme RA, Dall Agnol AM, Zotti E, de Oliveira TES, Alfieri AF, Alfieri AA. Viruses associated with congenital tremor and high lethality in piglets. Transbound Emerg Dis. 2018;65:331–7. https://doi.org/10.1111/tbed.12807.PubMedCrossRef

44.

Chen F, Knutson TP, Braun E, Jiang Y, Rossow S, Marthaler DG. Semi-quantitative duplex RT-PCR reveals the low occurrence of porcine pegivirus and atypical porcine pestivirus in diagnostic samples from the United States. Transbound Emerg Dis. 2019;66:1420–5. https://doi.org/10.1111/tbed.13154.PubMedPubMedCentralCrossRef

45.

Shi K, Xie S, Sun W, Liu H, Zhao J, Yin Y, Si H, Qu S, Lu W. Evolution and genetic diversity of atypical porcine pestivirus (APPV) from piglets with congenital tremor in Guangxi Province, Southern China. Vet Med Sci. 2021;7:714–23. https://doi.org/10.1002/vms3.407.PubMedCrossRef

Title: Genetic characterization of atypical porcine pestivirus from neonatal piglets with congenital tremor in Hubei province, China
Authors: Xujiao Ren
Ping Qian
Zihui Hu
Huanchun Chen
Xiangmin Li
Publication date: 01-12-2022
Publisher: BioMed Central
Keyword: Tremor
Published in: Virology Journal / Issue 1/2022
Electronic ISSN: 1743-422X
DOI: https://doi.org/10.1186/s12985-022-01780-8

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin

Prof. Florian Limbourg

Prof. Anoop Chauhan

Developed by: Springer Medicine

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2022

Identification of a novel interaction site between the large hepatitis delta antigen and clathrin that regulates the assembly of genotype III hepatitis delta virus

Whole-genome sequence analysis reveals the circulation of multiple SARS-CoV-2 variants of concern in Nairobi and neighboring counties, Kenya between March and July 2021

Development of a multiplex droplet digital PCR assay for detection of enterovirus, parechovirus, herpes simplex virus 1 and 2 simultaneously for diagnosis of viral CNS infections

Neutralizing monoclonal antibody in patients with coronavirus disease 2019: an observational study

The molecular mechanism of SARS-CoV-2 evading host antiviral innate immunity

The role of N-linked glycosylation in proteolytic processing and cell surface transport of the Cedar virus fusion protein

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

At a glance: The STEP trials