Abstract
A highly pathogenic swine disease designated as ‘porcine high fever disease (PHFD)’ appeared recently in China. Porcine reproductive and respiratory syndrome virus (PRRSV) was identified as an agent associated with PHFD, and two discontiguous sequence deletions were identified as a genetic marker in the Nsp2 region of the viral genome. To examine PHFD in Shandong province, a total of 10 PRRSV isolates were recovered from pig herds that had never been vaccinated for PRRS. Sequence analysis of open reading frame 5 (ORF5) showed that the level of identity among the 10 isolates ranged between 88.2 and 99.2%. For the non-structural protein 2 (Nsp2) gene, three isolates shared high sequence identity with VR-2332, the prototype virus of the North American genotype, while the remaining seven isolates exhibited two discontiguous sequence deletions that were identical to those of PHFD: a one-amino-acid (phenylalanine) deletion at position 482 and a 29-amino-acid deletion at positions 533–561 of Nsp2. Experimental infection of pigs with SD-JN, which was one of the seven isolates containing such deletions, resulted in severe clinical symptoms characterized by red discoloration on the body and hemorrhages in the lungs, kidneys, and inguinal lymph nodes, accompanied by higher mortality and longer duration of viremia. These symptoms were similar to those of PHFD observed in the field. Our results show that VR2332-like PRRSV coexists with PHFD-associated atypical PRRSV in pig herds in the Shandong area, and different PRRSV isolates differ greatly in their pathogenesis and virulence in pigs.
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References
Albina E (1997) Epidemiology of porcine reproductive and respiratory syndrome (PRRS): an overview. Vet Microbiol 55:309–316
Allende R, Lewis TL, Lu Z, Rock DL, Kutish GF, Ali A, Doster AR, Osorio FA (1999) North American and European porcine reproductive and respiratory syndrome viruses differ in non-structural protein coding regions. J Gen Virol 80:307–315
Andreyev VG, Wesley RD, Mengeling WL, Vorwald AC, Lager KM (1997) Genetic variation and phylogenetic relationship of 22 porcine reproductive and respiratory syndrome virus (PRRSV) field strains based on sequence analysis of open reading frame 5. Arch Virol 1(142):993–1001
Blaha T (2000) The “colourful” epidemiology of PRRS. Vet Res 31:77–83
Chang CC, Yoon KJ, Zimmerman JJ, Harmon KM, Dixon PM, Dvorak CM, Murtaugh MP (2002) Evolution of porcine reproductive and respiratory syndrome virus during sequential passages in pigs. J Virol 76:4750–4763
Chen J, Liu T, Zhu CG, Jin YF, Zhang YZ (2006) Genetic variation of Chinese PRRSV strains based on ORF5 sequence. Biochem Genet 44:421–431
De Lima M, Pattnaik AK, Flores EF, Osorio FA (2006) Serologic marker candidates identified among B-cell linear epitopes of Nsp2 and structural proteins of a North American strain of porcine reproductive and respiratory syndrome virus. Virology 353:410–421
Done SH, Patton DJ, White ME (1996) Porcine reproductive and respiratory syndrome (PRRS): a review, with emphasis on pathological, virological and diagnostic aspects. Br Vet J 152:153–174
Fang Y, Kim DY, Ropp S, Steen P, Christopher-Hennings J, Nelson EA, Rowland RR (2004) Heterogeneity in Nsp2 of European-like porcine reproductive and respiratory syndrome viruses isolated in the United States. Virus Res 100:229–235
Fang Y, Rowland RR, Roof M, Lunney JK, Christopher-Hennings J, Nelson EA (2006) A full-length cDNA infectious clone of North American type 1 porcine reproductive and respiratory syndrome virus: expression of green fluorescent protein in the Nsp2 region. J Virol 80:11447–11455
Grebennikova TV, Glouser DF, Vorwald AC, Musienko MI, Mengeling WL, Lager KM, Wesley RD, Biketov SF, Zaberezhny AD, Aliper TI, Nepoklonov EA (2004) Genomic characterization of virulent attenuated, and revertant passages of a North American porcine reproductive and respiratory syndrome virus strain. Virology 321:383–390
Guo B, Chen Z, Liu W, Cui Y (1996) Isolation and identification of porcine reproductive and respiratory syndrome (PRRS) virus from fetuses suspicious of PRRS. Chin J Anim Poult Infect Dis 17:1–4
Halbur PG, Paul PS, Frey ML, Landgraf J, Eernisse K, Meng XJ, Lum MA, Andrews AA, Rathje JA (1995) Comparison of the pathogenicity of two US porcine reproductive and respiratory syndrome virus isolates with of Lelystad virus. Vet Pathol 32:648–660
Johnson W, Roof M, Vaughn E, Christopher-Hennings J, Johnson CR, Murtaugh MP (2004) Pathogenic and humoral immune responses to porcine reproductive and respiratory syndrome virus (PRRSV) are related to viral load in acute infection. Vet Immunol Immunopathol 102:233–247
Key KF, Haqshenas G, Guenette DK, Swenson SK, Toth TE, Meng XJ (2001) Genetic variation and phylogenetic analyses of the ORF5 gene of acute porcine reproductive and respiratory syndrome virus isolates. Vet Microbiol 83:249–263
Li Y, Wang X, Bo K, Wang X, Tang B, Yang B, Jiang W, Jiang P (2007) Emergence of a highly pathogenic porcine reproductive and respiratory syndrome virus in the Mid-Eastern region of China. Vet J 174:577–584
Mateu E, Díaz I, Darwich L, Casal J, Martín M, Pujols J (2006) Evolution of ORF5 of Spanish porcine reproductive and respiratory syndrome virus strains from 1991 to 2005. Virus Res 115:198–206
Meulenberg JJ (2000) PRRSV, the virus. Vet Res 31:11–21
Neumann EJ, Kliebenstein JB, Johnson CD, Mabry JW, Bush EJ, Seitzinger AH, Green AL, Zimmerman JJ (2005) Assessment of the economic impact of porcine reproductive and respiratory syndrome on swine production in the United States. J Am Vet Med Assoc 227:385–392
Oleksiewicz MB, Bøtner A, Toft P, Normann P, Storgaard T (2001) Epitope mapping porcine reproductive and respiratory syndrome virus by phage display: the nsp2 fragment of the replicase polyprotein contains a cluster of B-cell epitopes. J Virol 75:3277–3290
Reed LJ, Muench H (1938) A simple method of estimating fifty percent endpoints. Am J Hyg 27:493–497
Shen S, Kwang J, Liu W, Liu DX (2000) Determination of the complete nucleotide sequence of a vaccine strain of porcine reproductive and respiratory syndrome virus and identification of the Nsp2 gene with a unique insertion. Arch Virol 145:871–883
Tian K, Yu X, Zhao T, Feng Y, Cao Z, Wang C, Hu Y, Chen X, Hu D, Tian X, Liu D, Zhang S, Deng X, Ding Y, Yang L, Zhang Y, Xiao H, Qiao M, Wang B, Hou L, Wang X, Yang X, Kang L, Sun M, Jin P, Wang S, Kitamura Y, Yan J, Gao GF (2007) Emergence of fatal PRRSV variants: unparalleled outbreaks of atypical PRRS in China and molecular dissection of the unique hallmark. PLoS one 6:1–10
Tong GZ, Zhou YJ, Hao XF, Tian ZJ, An TQ, Qiu HJ (2007) Highly pathogenic porcine reproductive and respiratory syndrome in China. Emerg Infect Dis 13:1434–1436
Wesley RD, Mengeling WL, Lager KM, Clouser DF, Landgraf JG, Frey ML (1998) Differentiation of a porcine reproductive and respiratory syndrome virus vaccine strain from North American field strains by restriction fragment length polymorphism analysis of ORF 5. J Vet Diagn Invest 10:140–144
Wootton S, Yoo D, Rogan D (2000) Full-length sequence of a Canadian porcine reproductive and respiratory syndrome virus (PRRSV) isolate. Arch Virol 145:2297–2323
Wu J, Wang J, Liu Y, Wang W, Zhang X, Yoo D (2008) Relationship between herd size and the prevalence of porcine reproductive and respiratory syndrome in China. Vet Rec 163:90–91
Yoo D, Welch SK, Lee C, Calvert JG (2004) Infectious cDNA clones of porcine reproductive and respiratory syndrome virus and their potential as vaccine vectors. Vet Immunol Immunopathol 102:143–154
Zhou L, Zhang J, Zeng J, Yin S, Li Y, Zheng L, Guo X, Ge X, Yang H (2009) The 30-amino-acid deletion in the Nsp2 of highly pathogenic porcine reproductive and respiratory syndrome virus emerging in China is not related to its virulence. J Virol 83:5156–5167
Zhou YJ, Hao XF, Tian JZ, Tong GZ, Yoo D, An TQ, Zhou T, Li GX, Qiu HJ, Wei TC, Yuan XF (2008) Highly virulent porcine reproductive and respiratory syndrome virus emerged in China. Transbound Emerg Dis 55:152–164
Acknowledgments
This study was supported by the Shandong Academy of Agricultural Sciences Youth Funds (Grant No. 2005YQ039), Natural Scientific Funds of Shandong Province (Grant No. Z2007-D06), and Main and Special Funds for Science and Technology of Shandong Province (Grant No. 2007-ZHZX11103). DY is a recipient of the grant from USDA National Research Initiative Competitive Grants Program (2008-35204-04634).
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Wu, J., Li, J., Tian, F. et al. Genetic variation and pathogenicity of highly virulent porcine reproductive and respiratory syndrome virus emerging in China. Arch Virol 154, 1589–1597 (2009). https://doi.org/10.1007/s00705-009-0478-6
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DOI: https://doi.org/10.1007/s00705-009-0478-6