Abstract
To evaluate the effect of natural infection with TTSuV1 on the antibody response to vaccination with PRRS vaccine and clinical signs when co-infected with virulent PRRSV, 15 4-week-old TTSuV1-positive piglets and 20 TTSuV1-negative piglets were selected by PCR from two pig farms in Jiangsu province. TTSuV1-negative pigs were divided into four groups, and TTSuV1-positive pigs were divided into three groups. Experimental pigs were vaccinated with a PRRSV modified live virus (MLV) at 6 weeks of age and subsequently challenged with a virulent strain of PRRSV at 10 weeks of age. A TTSuV1-negative control group and an unvaccinated PRRS MLV control group were tested at the same time. The levels of antibody/cytokine and protective efficiency against PRRS MLV vaccine were evaluated. TTSuV1-infected/PRRSV-vaccinated pigs had lower levels of PRRSV antibody, as well as IFN-γ, IL-10 and T lymphocyte proliferation, than the TTSuV1-uninfected/PRRSV-vaccinated group (P < 0.05, except IL-10) after vaccination at only one time point. TTSuV1-infected/PRRS MLV-vaccinated/PRRSV-challenged pigs had more severe clinical signs (P > 0.05), more macroscopic lung lesions (P < 0.05) and lower levels of PRRSV antibody (P < 0.05 at 7 to 14 days post-PRRSV-challenge) than TTSuV1-uninfected/PRRSV-vaccinated/PRRSV-challenged pigs. These data indicate that TTSuV1 natural infection has an adverse effect on the development of host immune responses, suppresses immunization by the PRRS MLV vaccine, and exacerbates PRRS to a certain extent in pigs.
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Abbreviations
- MLV:
-
Modified live virus
- PMWS:
-
Postweaning multisystemic wasting syndrome
- PRRS:
-
Porcine reproductive and respiratory syndrome
- PRRSV:
-
Porcine reproductive and respiratory syndrome virus
- TTSuV1:
-
Torque teno sus virus 1
- TTSuV2:
-
Torque teno sus virus 2
References
Kekarainen T, Segales J (2009) Torque teno virus infection in the pig and its potential role as a model of human infection. Vet J 180(2):163–168. doi:10.1016/j.tvjl.2007.12.005
Maggi F, Pifferi M, Tempestini E, Fornai C, Lanini L, Andreoli E, Vatteroni M, Presciuttini S, Pietrobelli A, Boner A, Pistello M, Bendinelli M (2003) TT virus loads and lymphocyte subpopulations in children with acute respiratory diseases. J Virol 77(16):9081–9083
Okamoto H, Takahashi M, Nishizawa T, Tawara A, Fukai K, Muramatsu U, Naito Y, Yoshikawa A (2002) Genomic characterization of TT viruses (TTVs) in pigs, cats and dogs and their relatedness with species-specific TTVs in primates and tupaias. J Gen Virol 83(Pt 6):1291–1297
Niel C, Diniz-Mendes L, Devalle S (2005) Rolling-circle amplification of Torque teno virus (TTV) complete genomes from human and swine sera and identification of a novel swine TTV genogroup. J Gen Virol 86(Pt 5):1343–1347. doi:10.1099/vir.0.80794-0
Aramouni M, Segales J, Cortey M, Kekarainen T (2010) Age-related tissue distribution of swine Torque teno sus virus 1 and 2. Vet Microbiol 146(3–4):350–353. doi:10.1016/j.vetmic.2010.05.036
Krakowka JE, et al. (2008) Porcine genogroup 1 torque teno virus (G1-TTV) potentiates PCV2 and PRRSV infections in gnotobiotic swine. In: Proceedings of the international pig veterinary society (Durban) vol 1, pp 99–109
Ellis JA, Allan G, Krakowka S (2008) Effect of coinfection with genogroup 1 porcine torque teno virus on porcine circovirus type 2-associated postweaning multisystemic wasting syndrome in gnotobiotic pigs. Am J Vet Res 69(12):1608–1614. doi:10.2460/ajvr.69.12.1608
Martinez L, Kekarainen T, Sibila M, Ruiz-Fons F, Vidal D, Gortazar C, Segales J (2006) Torque teno virus (TTV) is highly prevalent in the European wild boar (Sus scrofa). Vet Microbiol 118(3–4):223–229. doi:10.1016/j.vetmic.2006.07.022
McKeown NE, Fenaux M, Halbur PG, Meng XJ (2004) Molecular characterization of porcine TT virus, an orphan virus, in pigs from six different countries. Vet Microbiol 104(1–2):113–117. doi:10.1016/j.vetmic.2004.08.013
Bigarre L, Beven V, de Boisseson C, Grasland B, Rose N, Biagini P, Jestin A (2005) Pig anelloviruses are highly prevalent in swine herds in France. J Gen Virol 86(Pt 3):631–635. doi:10.1099/vir.0.80573-0
Kekarainen T, Lopez-Soria S, Segales J (2007) Detection of swine Torque teno virus genogroups 1 and 2 in boar sera and semen. Theriogenology 68(7):966–971. doi:10.1016/j.theriogenology.2007.07.010
Martinez-Guino L, Kekarainen T, Segales J (2009) Evidence of Torque teno virus (TTV) vertical transmission in swine. Theriogenology 71(9):1390–1395. doi:10.1016/j.theriogenology.2009.01.010
Brassard J, Gagne MJ, Lamoureux L, Inglis GD, Leblanc D, Houde A (2008) Molecular detection of bovine and porcine Torque teno virus in plasma and feces. Vet Microbiol 126(1–3):271–276. doi:10.1016/j.vetmic.2007.07.014
Martelli F, Caprioli A, Di Bartolo I, Cibin V, Pezzotti G, Ruggeri FM, Ostanello F (2006) Detection of swine torque teno virus in Italian pig herds. J Vet Med B Infect Dis Vet Public Health 53(5):234–238. doi:10.1111/j.1439-0450.2006.00949.x
Kekarainen T, Sibila M, Segales J (2006) Prevalence of swine Torque teno virus in post-weaning multisystemic wasting syndrome (PMWS)-affected and non-PMWS-affected pigs in Spain. J Gen Virol 87(Pt 4):833–837. doi:10.1099/vir.0.81586-0
Leary TP, Erker JC, Chalmers ML, Desai SM, Mushahwar IK (1999) Improved detection systems for TT virus reveal high prevalence in humans, non-human primates and farm animals. J Gen Virol 80(Pt 8):2115–2120
Gallei A, Pesch S, Esking WS, Keller C, Ohlinger VF (2009) Porcine Torque teno virus: Determination of viral genomic loads by genogroup-specific multiplex rt-PCR, detection of frequent multiple infections with genogroups 1 or 2, and establishment of viral full-length sequences. Vet Microbiol. doi:10.1016/j.vetmic.2009.12.005
Taira O, Ogawa H, Nagao A, Tuchiya K, Nunoya T, Ueda S (2009) Prevalence of swine Torque teno virus genogroups 1 and 2 in Japanese swine with suspected post-weaning multisystemic wasting syndrome and porcine respiratory disease complex. Vet Microbiol 139(3–4):347–350. doi:10.1016/j.vetmic.2009.06.010
Huang YW, Ni YY, Dryman BA, Meng XJ (2010) Multiple infection of porcine Torque teno virus in a single pig and characterization of the full-length genomic sequences of four U.S. prototype PTTV strains: implication for genotyping of PTTV. Virology 396(2):289–297. doi:10.1016/j.virol.2009.10.031
Segales J, Martinez-Guino L, Cortey M, Navarro N, Huerta E, Sibila M, Pujols J, Kekarainen T (2009) Retrospective study on swine Torque teno virus genogroups 1 and 2 infection from 1985 to 2005 in Spain. Vet Microbiol 134(3–4):199–207. doi:10.1016/j.vetmic.2008.08.002
Li J, Jiang P, Li Y, Wang X, Cao J, Zeshan B (2009) HSP70 fused with GP3 and GP5 of porcine reproductive and respiratory syndrome virus enhanced the immune responses and protective efficacy against virulent PRRSV challenge in pigs. Vaccine 27(6):825–832. doi:10.1016/j.vaccine.2008.11.088
Wang Y, Liang Y, Han J, Burkhart KM, Vaughn EM, Roof MB, Faaberg KS (2008) Attenuation of porcine reproductive and respiratory syndrome virus strain MN184 using chimeric construction with vaccine sequence. Virology 371(2):418–429. doi:10.1016/j.virol.2007.09.032
Halbur PG, Miller LD, Paul PS, Meng XJ, Huffman EL, Andrews JJ (1995) Immunohistochemical identification of porcine reproductive and respiratory syndrome virus (PRRSV) antigen in the heart and lymphoid system of three-week-old colostrum-deprived pigs. Vet Pathol 32(2):200–204
Mengeling WL, Lager KM, Vorwald AC, Clouser DF (2003) Comparative safety and efficacy of attenuated single-strain and multi-strain vaccines for porcine reproductive and respiratory syndrome. Vet Microbiol 93(1):25–38 (pii:S0378113502004261)
Opriessnig T, McKeown NE, Harmon KL, Meng XJ, Halbur PG (2006) Porcine circovirus type 2 infection decreases the efficacy of a modified live porcine reproductive and respiratory syndrome virus vaccine. Clin Vaccine Immunol 13(8):923–929. doi:10.1128/CVI.00074-06
Rossow KD, Bautista EM, Goyal SM, Molitor TW, Murtaugh MP, Morrison RB, Benfield DA, Collins JE (1994) Experimental porcine reproductive and respiratory syndrome virus infection in one-, four-, and 10-week-old pigs. J Vet Diagn Invest 6(1):3–12
Morrison RB, Collins JE, Harris L, Christianson WT, Benfield DA, Chladek DW, Gorcyca DE, Joo HS (1992) Serologic evidence incriminating a recently isolated virus (ATCC VR-2332) as the cause of swine infertility and respiratory syndrome (SIRS). J Vet Diagn Invest 4(2):186–188
Halbur PG, Rothschild MF, Thacker BJ et al. (1998) Differences in susceptibility of Duroc, Hampshire, and Meishan pigs to infection with a high virulence strain (VR2385) of porcine reproductive and respiratory syndrome virus (PRRSV). J Anim Breed Genet 115(3):181–189
Sibila M, Martinez-Guino L, Huerta E, Mora M, Grau-Roma L, Kekarainen T, Segales J (2009) Torque teno virus (TTV) infection in sows and suckling piglets. Vet Microbiol 137(3–4):354–358. doi:10.1016/j.vetmic.2009.01.008
Zhu CX, Cui L, Shan TL, Luo XN, Liu ZJ, Yuan CL, Lan DL, Zhao W, Liu ZW, Hua XG (2010) Porcine torque teno virus infections in China. J Clin Virol 48(4):296–298. doi:10.1016/j.jcv.2010.04.012
Kekarainen T, Martinez-Guino L, Segales J (2009) Swine torque teno virus detection in pig commercial vaccines, enzymes for laboratory use and human drugs containing components of porcine origin. J Gen Virol 90(Pt 3):648–653. doi:10.1099/vir.0.006841-0
Simmonds P, Prescott LE, Logue C, Davidson F, Thomas AE, Ludlam CA (1999) TT virus–part of the normal human flora? J Infect Dis 180(5):1748–1750. doi:10.1086/315103
Zein NN (2000) TT virus infection: an emerging pathogen in search of its identity. J Pediatr 136(5):573–575. doi:10.1067/mpd.2000.106900
Krakowka S, Ellis JA (2008) Evaluation of the effects of porcine genogroup 1 torque teno virus in gnotobiotic swine. Am J Vet Res 69(12):1623–1629. doi:10.2460/ajvr.69.12.1623
Acknowledgments
This work was supported by Program for New Century Excellent Talents (NCET) at the University (No.NCET-08-0794) of China, Natural Science Foundation of the Higher Education Institutions of Jiangsu, China (Grant No.10kjd230003), Doctoral Research Foundation of Jinling Institution of Technology (no.40610047) and Graduate Research and Innovation Project of Jiangsu Province (CX09B_ 246Z).
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Zhang, Z., Wang, Y., Fan, H. et al. Natural infection with torque teno sus virus 1 (TTSuV1) suppresses the immune response to porcine reproductive and respiratory syndrome virus (PRRSV) vaccination. Arch Virol 157, 927–933 (2012). https://doi.org/10.1007/s00705-012-1249-3
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DOI: https://doi.org/10.1007/s00705-012-1249-3