Evaluation of PRRSv specific, maternally derived and induced immune response in Ingelvac PRRSFLEX EU vaccinated piglets in the presence of maternally transferred immunity

English version

Autoři: Christian Kraft ^aff001; Rimma Hennies ^aff001; Karla Dreckmann ^aff001; Marta Noguera ^aff001; Poul Henning Rathkjen ^aff002; Michael Gassel ^aff002; Marcus Gereke ^aff001
Působiště autorů: Boehringer Ingelheim Veterinary Research Center GmbH & Co. KG., Hanover, Germany ^aff001; Boehringer Ingelheim Vetmedica GmbH, Ingelheim, Germany ^aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223060

Souhrn

In this study, we analyzed PRRS virus (PRRSv) specific lymphocyte function in piglets vaccinated with Ingelvac PRRSFLEX EU^® at two and three weeks of age in the presence of homologous maternal immunity. Complete analysis of maternal immunity to PRRSv was evaluated postpartum, as well as passive transfer of antibodies and T cells to the piglet through colostrum intake and before and after challenge with a heterologous PRRSv at ten weeks of age. Maternal-derived antibodies were detected in piglets but declined quickly after weaning. However, vaccinated animals restored PRRSv-specific antibody levels by anamnestic response to vaccination. Cell analysis in colostrum and milk revealed presence of PRRSv-specific immune cells at suckling with higher concentrations found in colostrum than in milk. In addition, colostrum and milk contained PRRSv-specific IgA and IgG that may contribute to protection of newborn piglets. Despite the presence of PRRSv-specific Peripheral Blood Mononuclear cells (PBMCs) in colostrum and milk, no PRRSv-specific cells could be detected from blood of the piglets at one or two weeks of life. Nevertheless, cellular immunity was detectable in pre-challenged piglets up to 7 weeks after vaccination while the non-vaccinated control group showed no interferon (IFN) γ response to PRRSv stimulation. After challenge, all piglets developed a PRRSv-specific IFNγ-response, which was more robust at significantly higher levels in vaccinated animals compared to the primary response to PRRSv in non-vaccinated animals. Cytokine analysis in the lung lumen showed a reduction of pro-inflammatory responses to PRRSv challenge in vaccinated animals, especially reduced interferon (IFN) α levels. In conclusion, vaccination of maternally positive piglets at 2 and 3 weeks of age with Ingelvac PRRSFLEX EU induced a humoral and cellular immune response to PRRSv and provided protection against virulent, heterologous PRRSv challenge.

Klíčová slova:

Antibodies – Breast milk – Cytokines – Enzyme-linked immunoassays – Swine – Vaccination and immunization – Vaccines – Cell-mediated immunity

Zdroje

1. Holtkamp DJ, Kliebenstein JB, Neumann EJ. Assessment of the economic impact of porcine reproductive and respiratory syndrome virus on United States pork producers. Journal of Swine Health and Production. 2013;21(2):72–84.

2. Christianson WT, Kim HS, Yoon IJ, Joo HS. Transplacental infection of porcine fetuses following experimental challenge inoculation with encephalomyocarditis virus. Am J Vet Res. 1992;53(1):44–7. Epub 1992/01/01. 1311538.

3. Adams MJ, Lefkowitz EJ, King AMQ, Harrach B, Harrison RL, Knowles NJ, et al. Changes to taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2017). Arch Virol. 2017;162(8):2505–38. Epub 2017/04/24. doi: 10.1007/s00705-017-3358-5 28434098.

4. Han K, Seo HW, Oh Y, Kang I, Park C, Chae C. Comparison of the virulence of European and North American genotypes of porcine reproductive and respiratory syndrome virus in experimentally infected pigs. Vet J. 2013;195(3):313–8. Epub 2012/07/27. doi: 10.1016/j.tvjl.2012.06.035 22831992.

5. Morgan SB, Frossard JP, Pallares FJ, Gough J, Stadejek T, Graham SP, et al. Pathology and Virus Distribution in the Lung and Lymphoid Tissues of Pigs Experimentally Inoculated with Three Distinct Type 1 PRRS Virus Isolates of Varying Pathogenicity. Transbound Emerg Dis. 2016;63(3):285–95. Epub 2014/11/11. doi: 10.1111/tbed.12272 25382098.

6. Stadejek T, Oleksiewicz MB, Scherbakov AV, Timina AM, Krabbe JS, Chabros K, et al. Definition of subtypes in the European genotype of porcine reproductive and respiratory syndrome virus: nucleocapsid characteristics and geographical distribution in Europe. Arch Virol. 2008;153(8):1479–88. Epub 2008/07/02. doi: 10.1007/s00705-008-0146-2 18592131.

7. Labarque G, Reeth KV, Nauwynck H, Drexler C, Van Gucht S, Pensaert M. Impact of genetic diversity of European-type porcine reproductive and respiratory syndrome virus strains on vaccine efficacy. Vaccine. 2004;22(31–32):4183–90. doi: 10.1016/j.vaccine.2004.05.008 15474708.

8. Pileri E, Gibert E, Soldevila F, Garcia-Saenz A, Pujols J, Diaz I, et al. Vaccination with a genotype 1 modified live vaccine against porcine reproductive and respiratory syndrome virus significantly reduces viremia, viral shedding and transmission of the virus in a quasi-natural experimental model. Vet Microbiol. 2015;175(1):7–16. doi: 10.1016/j.vetmic.2014.11.007 25439650.

9. Piontkowski M, Kroll J, Kraft C, Coll T. Safety and early onset of immunity with a novel European porcine reproductive and respiratory syndrome virus vaccine in young piglets. Can J Vet Res. 2016;80(2):124–33. 27127339; PubMed Central PMCID: PMC4836038.

10. Scortti M, Prieto C, Martinez-Lobo FJ, Simarro I, Castro JM. Effects of two commercial European modified-live vaccines against porcine reproductive and respiratory syndrome viruses in pregnant gilts. Vet J. 2006;172(3):506–14. doi: 10.1016/j.tvjl.2005.07.015 16169756.

11. Zuckermann FA, Garcia EA, Luque ID, Christopher-Hennings J, Doster A, Brito M, et al. Assessment of the efficacy of commercial porcine reproductive and respiratory syndrome virus (PRRSV) vaccines based on measurement of serologic response, frequency of gamma-IFN-producing cells and virological parameters of protection upon challenge. Vet Microbiol. 2007;123(1–3):69–85. doi: 10.1016/j.vetmic.2007.02.009 17376612.

12. Rooke JA, Bland IM. The acquisition of passive immunity in the new-born piglet. Livestock Production Science. 2002;78(1):13–23. http://dx.doi.org/10.1016/S0301-6226(02)00182-3.

13. Nechvatalova K, Kudlackova H, Leva L, Babickova K, Faldyna M. Transfer of humoral and cell-mediated immunity via colostrum in pigs. Vet Immunol Immunopathol. 2011;142(1–2):95–100. doi: 10.1016/j.vetimm.2011.03.022 21524802.

14. Bandrick M, Ariza-Nieto C, Baidoo SK, Molitor TW. Colostral antibody-mediated and cell-mediated immunity contributes to innate and antigen-specific immunity in piglets. Dev Comp Immunol. 2014;43(1):114–20. doi: 10.1016/j.dci.2013.11.005 24252519; PubMed Central PMCID: PMC3902642.

15. Declerck I, Dewulf J, Sarrazin S, Maes D. Long-term effects of colostrum intake in piglet mortality and performance. J Anim Sci. 2016;94(4):1633–43. doi: 10.2527/jas.2015-9564 27136022.

16. Geldhof MF, Van Breedam W, De Jong E, Lopez Rodriguez A, Karniychuk UU, Vanhee M, et al. Antibody response and maternal immunity upon boosting PRRSV-immune sows with experimental farm-specific and commercial PRRSV vaccines. Vet Microbiol. 2013;167(3–4):260–71. Epub 2013/09/18. doi: 10.1016/j.vetmic.2013.08.017 24041768.

17. Kitikoon P, Nilubol D, Erickson BJ, Janke BH, Hoover TC, Sornsen SA, et al. The immune response and maternal antibody interference to a heterologous H1N1 swine influenza virus infection following vaccination. Vet Immunol Immunopathol. 2006;112(3–4):117–28. doi: 10.1016/j.vetimm.2006.02.008 16621020

18. Tielen MJ, van Exsel AC, Brus DH, Truijen WT. [Aujeszky's disease: serological responsiveness after vaccination of 6-10-week-old piglets with maternal antibody (author's transl)]. Tijdschr Diergeneeskd. 1981;106(15):739–47. 6269250.

19. Fablet C, Renson P, Eono F, Mahe S, Eveno E, Le Dimna M, et al. Maternally-derived antibodies (MDAs) impair piglets' humoral and cellular immune responses to vaccination against porcine reproductive and respiratory syndrome (PRRS). Vet Microbiol. 2016;192:175–80. doi: 10.1016/j.vetmic.2016.07.014 27527780.

20. Martelli P, Gozio S, Ferrari L, Rosina S, De Angelis E, Quintavalla C, et al. Efficacy of a modified live porcine reproductive and respiratory syndrome virus (PRRSV) vaccine in pigs naturally exposed to a heterologous European (Italian cluster) field strain: Clinical protection and cell-mediated immunity. Vaccine. 2009;27(28):3788–99. doi: 10.1016/j.vaccine.2009.03.028 19442420.

21. Balka G, Dreckmann K, Papp G, Kraft C. Vaccination of piglets at 2 and 3 weeks of age with Ingelvac PRRSFLEX(R) EU provides protection against heterologous field challenge in the face of homologous maternally derived antibodies. Porcine Health Manag. 2016;2:24. doi: 10.1186/s40813-016-0037-y 28405450; PubMed Central PMCID: PMC5382426.

22. Balasch M, Fort M, Taylor LP, Calvert JG. Vaccination of 1-day-old pigs with a porcine reproductive and respiratory syndrome virus (PRRSV) modified live attenuated virus vaccine is able to overcome maternal immunity. Porcine Health Manag. 2018;4:25. Epub 2018/11/22. doi: 10.1186/s40813-018-0101-x 30459958; PubMed Central PMCID: PMC6237022.

23. Friess AE, Sinowatz F, Skolek-Winnisch R, Traautner W. The placenta of the pig. I. Finestructural changes of the placental barrier during pregnancy. Anat Embryol (Berl). 1980;158(2):179–91. Epub 1980/01/01. doi: 10.1007/bf00315905 7356176.

24. Dvorak CMT, Payne BJ, Seate JL, Murtaugh MP. Effect of Maternal Antibody Transfer on Antibody Dynamics and Control of Porcine Circovirus Type 2 Infection in Offspring. Viral Immunol. 2018;31(1):40–6. Epub 2017/08/18. doi: 10.1089/vim.2017.0058 28817375.

25. Tuboly S, Bernath S. Intestinal absorption of colostral lymphoid cells in newborn animals. Adv Exp Med Biol. 2002;503:107–14. Epub 2002/05/25. doi: 10.1007/978-1-4615-0559-4_12 12026009.

26. Ogawa S, Tsukahara T, Imaoka T, Nakanishi N, Ushida K, Inoue R. The effect of colostrum ingestion during the first 24 hours of life on early postnatal development of piglet immune systems. Anim Sci J. 2016;87(12):1511–5. Epub 2016/03/19. doi: 10.1111/asj.12573 26990379.

27. Bandrick M, Pieters M, Pijoan C, Molitor TW. Passive transfer of maternal Mycoplasma hyopneumoniae-specific cellular immunity to piglets. Clin Vaccine Immunol. 2008;15(3):540–3. doi: 10.1128/CVI.00466-07 18184823; PubMed Central PMCID: PMC2268269.

28. Lauritsen KT, Hagedorn-Olsen T, Jungersen G, Riber U, Stryhn H, Friis NF, et al. Transfer of maternal immunity to piglets is involved in early protection against Mycoplasma hyosynoviae infection. Vet Immunol Immunopathol. 2017;183:22–30. Epub 2017/01/09. doi: 10.1016/j.vetimm.2016.12.002 28063473.

29. Renson P, Fablet C, Andraud M, Normand V, Lebret A, Paboeuf F, et al. Maternally-derived neutralizing antibodies reduce vaccine efficacy against porcine reproductive and respiratory syndrome virus infection. Vaccine. 2019;37(31):4318–24. Epub 2019/06/30. doi: 10.1016/j.vaccine.2019.06.045 31248683.

30. Sandbulte MR, Platt R, Roth JA, Henningson JN, Gibson KA, Rajao DS, et al. Divergent immune responses and disease outcomes in piglets immunized with inactivated and attenuated H3N2 swine influenza vaccines in the presence of maternally-derived antibodies. Virology. 2014;464–465:45–54. Epub 2014/07/22. doi: 10.1016/j.virol.2014.06.027 25043588.

31. Niewiesk S. Maternal antibodies: clinical significance, mechanism of interference with immune responses, and possible vaccination strategies. Front Immunol. 2014;5:446. Epub 2014/10/04. doi: 10.3389/fimmu.2014.00446 25278941; PubMed Central PMCID: PMC4165321.

32. Diaz I, Darwich L, Pappaterra G, Pujols J, Mateu E. Different European-type vaccines against porcine reproductive and respiratory syndrome virus have different immunological properties and confer different protection to pigs. Virology. 2006;351(2):249–59. doi: 10.1016/j.virol.2006.03.046 16712895.

33. Diaz I, Gimeno M, Darwich L, Navarro N, Kuzemtseva L, Lopez S, et al. Characterization of homologous and heterologous adaptive immune responses in porcine reproductive and respiratory syndrome virus infection. Vet Res. 2012;43:30. doi: 10.1186/1297-9716-43-30 22515169; PubMed Central PMCID: PMC3403850.

34. Liu Y, Shi W, Zhou E, Wang S, Hu S, Cai X, et al. Dynamic changes in inflammatory cytokines in pigs infected with highly pathogenic porcine reproductive and respiratory syndrome virus. Clin Vaccine Immunol. 2010;17(9):1439–45. Epub 2010/07/16. doi: 10.1128/CVI.00517-09 20631336; PubMed Central PMCID: PMC2944458.

35. Buddaert W, Van Reeth K, Pensaert M. In vivo and in vitro interferon (IFN) studies with the porcine reproductive and respiratory syndrome virus (PRRSV). Adv Exp Med Biol. 1998;440:461–7. doi: 10.1007/978-1-4615-5331-1_59 9782316.

36. Van Reeth K, Labarque G, Nauwynck H, Pensaert M. Differential production of proinflammatory cytokines in the pig lung during different respiratory virus infections: correlations with pathogenicity. Res Vet Sci. 1999;67(1):47–52. doi: 10.1053/rvsc.1998.0277 10425240

37. Halbur PG, Paul PS, Frey ML, Landgraf J, Eernisse K, Meng XJ, et al. Comparison of the pathogenicity of two US porcine reproductive and respiratory syndrome virus isolates with that of the Lelystad virus. Vet Pathol. 1995;32(6):648–60. doi: 10.1177/030098589503200606 8592800.

38. Lee JA, Oh YR, Hwang MA, Lee JB, Park SY, Song CS, et al. Mycoplasma hyorhinis is a potential pathogen of porcine respiratory disease complex that aggravates pneumonia caused by porcine reproductive and respiratory syndrome virus. Vet Immunol Immunopathol. 2016;177:48–51. Epub 2016/07/21. doi: 10.1016/j.vetimm.2016.06.008 27436444.

39. Brockmeier SL, Loving CL, Palmer MV, Spear A, Nicholson TL, Faaberg KS, et al. Comparison of Asian porcine high fever disease isolates of porcine reproductive and respiratory syndrome virus to United States isolates for their ability to cause disease and secondary bacterial infection in swine. Vet Microbiol. 2017;203:6–17. Epub 2017/06/18. doi: 10.1016/j.vetmic.2017.02.003 28619168.

Evaluation of PRRSv specific, maternally derived and induced immune response in Ingelvac PRRSFLEX EU vaccinated piglets in the presence of maternally transferred immunity

Souhrn

Klíčová slova:

Zdroje

PLOS One

INSIGHTS from European Respiratory Congress

Současné pohledy na riziko v parodontologii

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií

Střevní příprava před kolonoskopií