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Booster administration can make a difference in the antibody response to intradermal foot-and-mouth disease vaccination in cattle

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Abstract

Foot-and-mouth disease (FMD) is a highly contagious and economically important viral disease of cloven-hoofed animals. Routine vaccination is one of the preferred methods of protection against this disease in endemic countries. For protective immunity against FMD, repeated immunizations with frequent administration are required. Intradermal immunization has many advantages over intramuscular administration of vaccines. In this study, a commercial tetravalent FMD vaccine adjuvanted with Montanide ISA 206 was administered to cattle via the intramuscular (2 mL [n = 10] and 0.5 mL [n = 9]) and intradermal (0.5 mL [n = 11]) routes. Booster doses were administered 28 days later using the same vaccine and routes. Serum samples were collected on days 0, 7, 14, and 28 post-vaccination (pv) and at 30 and 60 days post-booster. Homologous and heterologous virus neutralization tests and liquid-phase blocking and isotype ELISAs were used to measure the antibody response. The results showed that intradermal administration of quarter doses of the vaccine provides an equal or better virus neutralization antibody response than intramuscular administration of the same dose of vaccine after booster administration in cattle. This means that four times more cattle can be immunized with the same amount of vaccine using the intradermal route without compromising immunity.

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References

  1. Singh RK, Sharma GK, Mahajan S, Dhama K, Basagoudanavar SH, Hosamani M, Sreenivasa BP, Chaicumpa W, Gupta VK, Sanyal A (2019) Foot-and-mouth disease virus: immunobiology, advances in vaccines and vaccination strategies addressing vaccine failures—an Indian perspective. Vaccines (Basel) 7(3):90. https://doi.org/10.3390/vaccines7030090 (PMID: 31426368; PMCID: PMC6789522)

    Article  CAS  Google Scholar 

  2. Dar P, Kalaivanana R, Sieda N, Mamoa B, Kishorea S, Suryanarayanad VVS, Kondabattulaa G (2013) Montanide ISATM201 adjuvanted FMD vaccine induces improved immune responses and protection in cattle. Vaccine 31:3327–3332. https://doi.org/10.1016/j.vaccine.2013.05.078

    Article  CAS  PubMed  Google Scholar 

  3. Orsel K, Bouma A (2009) The effect of foot-and-mouth disease (FMD) vaccination on virus transmission and the significance for the field. Can Vet J 50(10):1059–1063

    PubMed  PubMed Central  Google Scholar 

  4. Doel TR (1999) Optimisation of the immune response to foot-and-mouth disease vaccines. Vaccine 17:1767–1771

    Article  CAS  Google Scholar 

  5. Paton DJ, Reeve R, Capozzo AV, Ludi A (2019) Estimating the protection afforded by foot-and-mouth disease vaccines in the laboratory. Vaccine 37:5515–5524. https://doi.org/10.1016/j.vaccine.2019.07.102

    Article  CAS  PubMed  Google Scholar 

  6. Tekleghiorghis T, Weerdmeester K, van Hemert-Kluitenberg F, Moormann RJM, Dekker A (2014) No significant differences in the breadth of the foot-and-mouth disease serotype A vaccine induced antibody responses in cattle, using different adjuvants, mixed antigens and different routes of administration. Vaccine 32(41):5330–5336. https://doi.org/10.1016/j.vaccine.2014.07.033

    Article  CAS  PubMed  Google Scholar 

  7. Wigdorovitz A, Carrillo C, Dus Santos MJ, Trono K, Peralta A, Gómez MC, Ríos RD, Franzone PM, Sadir AM, Escribano JM, Borca MV (1999) Induction of a protective antibody response to foot and mouth disease virus in mice following oral or parenteral immunization with alfalfa transgenic plants expressing the viral structural protein VP1. Virology 255(2):347–353. https://doi.org/10.1006/viro.1998.9590

    Article  CAS  PubMed  Google Scholar 

  8. Fischer D, Rood D, Barrette RW, Zuwallack A, Kramer E, Brown F, Silbart LK (2003) Intranasal ımmunization of guinea pigs with an ımmunodominant foot-and-mouth disease virus peptide conjugate ınduces mucosal and humoral antibodies and protection against challenge. J Virol 77(13):7486–7491. https://doi.org/10.1128/JVI.77.13.7486-7491.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Hunsaker BD, Perino LJ (2001) Efficacy of intradermal vaccination. Vet Immunol Immunopathol 79(1–2):1–13. https://doi.org/10.1016/s0165-2427(01)00244-6

    Article  CAS  PubMed  Google Scholar 

  10. Bal SM, Slütter B, Verheul R, Bouwstra JA, Jiskoot W (2012) Adjuvanted, antigen loaded N-trimethyl chitosan nanoparticles for nasal and intradermal vaccination: adjuvant- and site-dependent immunogenicity in mice. Eur J Pharm Sci 45(4):475–481

    Article  CAS  Google Scholar 

  11. Holland D, Booy R, Looze FD, Eizenberg P, McDonald J, Karrasch J, McKeirnan M, Salem H, Mills G, Reid J, Weber F, Saville M (2008) Intradermal influenza vaccine administered using a new microinjection system produces superior immunogenicity in elderly adults: a randomized controlled trial. J Infect Dis 198:650–658

    Article  Google Scholar 

  12. Propst T, Propst A, Lhotta K, Vogel W, Konig P (1998) Reinforced intradermal hepatitis B vaccination in hemodialysis patients is superior in antibody response to intramuscular or subcutaneous vaccination. Am J Kidney Dis 32:1041–1045

    Article  CAS  Google Scholar 

  13. Arrazuria R, Ladero I, Molina E, Fuertes M, Juste R, Fernández M, Pérez V, Garrido J, Elguezabal N (2020) Alternative vaccination routes against paratuberculosis modulate local immune response and interference with tuberculosis diagnosis in laboratory animal models. Vet Sci 7:7. https://doi.org/10.3390/vetsci7010007

    Article  PubMed Central  Google Scholar 

  14. Makoschey B (2015) Modes of vaccine administration at a glance. Berl Münch Tierärztl Wochenschr 128(11–12):451–455. https://doi.org/10.2376/0005-9366-128-451

    Article  PubMed  Google Scholar 

  15. Pandya M, Pacheco JM, Bishop E, Kenney M, Milward F, Doel T, Golde WT (2012) An alternate delivery system improves vaccine performance against foot-and-mouth disease virus (FMDV). Vaccine 20:3106–3111

    Article  Google Scholar 

  16. Wangmo K, Laven R, Cliquet F, Wasniewski M, Yang A (2019) Comparison of antibody titres between intradermal and intramuscular rabies vaccination using inactivated vaccine in cattle in Bhutan. PLoS One 14(6):e0209946. https://doi.org/10.1371/journal.pone.0209946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Samina I, Zakay-Rones Z, Weller JI, Peleg BA (1998) Host factors affecting the homologous and heterologous immune response of cattle to FMDV: genetic background, age, virus strains and route of administration. Vaccine 4:335–339. https://doi.org/10.1016/s0264-410x(97)00212-0

    Article  Google Scholar 

  18. Eblé PL, Weerdmeester K, van Hemert-Kluitenberg F, Dekker A (2009) Intradermal vaccination of pigs against FMD with 1/10 dose results in comparable vaccine efficacy as intramuscular vaccination with a full dose. Vaccine 27:1272–1278. https://doi.org/10.1016/j.vaccine.2008.12.011

    Article  CAS  PubMed  Google Scholar 

  19. OIE (2019) Manual of diagnositic tests and vaccines for terrestrial animals (Terrestrial Manual). OIE, Paris

    Google Scholar 

  20. Hamblin C, Barnett IT, Hedger RS (1986) A new enzyme-linked immunosorbent assay (ELISA) for the detection of antibodies against foot-and-mouth disease virus I Development and method of ELISA. J Immunol Methods 93(1):115–121

    Article  CAS  Google Scholar 

  21. Xiao CW, Rajput ZI, Hu SH (2007) Improvement of a commercial foot-and-mouth vaccine by supplement of Quil A. Vaccine 25(25):4795–4800

    Article  CAS  Google Scholar 

  22. Oreskovic Z, Kudlackova H, Krejci J, Nechvatalova K, Faldyna M (2017) Oil-based adjuvants delivered intradermally induce high primary IgG2 immune response in swine. Res Vet Sci 114:41–43. https://doi.org/10.1016/j.rvsc.2017.03.007

    Article  CAS  PubMed  Google Scholar 

  23. Künzi V, Klap JM, Seiberling MK, Herzog C, Hartmann K, Kürsteiner O, Kompier R, Grimaldi R, Goudsmit J (2009) Immunogenicity and safety of low dose virosomal adjuvanted influenza vaccine administered intradermally compared to intramuscular full dose administration. Vaccine 27:3561–3567. https://doi.org/10.1016/j.vaccine.2009.03.062

    Article  CAS  PubMed  Google Scholar 

  24. Krejci J, Nechvatalova K, Kudlackova H, Leva L, Bernardy J, Toman M, Faldyn M (2013) Effects of adjuvants on the immune response of pigs after intradermal administration of antigen. Res Vet Sci 94:73–76

    Article  CAS  Google Scholar 

  25. Madapong A, Saeng-Chuto K, Chaikhumwang P, Tantituvanont A, Saardrak K, Pedrazuela Sanz R, Miranda Alvarez J, Nilubo D (2020) Immune response and protective efficacy of intramuscular and intradermal vaccination with porcine reproductive and respiratory syndrome virus 1 (PRRSV-1) modified live vaccine against highly pathogenic PRRSV-2 (HP-PRRSV-2) challenge, either alone or in combination with of PRRSV-1. Vet Microbiol 244:108655. https://doi.org/10.1016/j.vetmic.2020.108655 (PMID: 32402335)

    Article  CAS  PubMed  Google Scholar 

  26. Sadat SMA, Snider M, Garg R, Brownlie R, van Drunen S, van den Hurk L (2017) Local innate responses and protective immunity after intradermal immunization with bovine viral diarrhea virus E2 protein formulated with a combination adjuvant in cattle. Vaccine 35:3466–3473. https://doi.org/10.1016/j.vaccine.2017.05.029

    Article  CAS  PubMed  Google Scholar 

  27. Hwang JH, Lee KN, Kim SM, Lee G, Moon Y, Kim B, Lee JS, Park JH (2019) Needleless intradermal vaccination for foot-and-mouth disease induced granuloma-free effective protection in pigs. J Vet Sci 20(3):e29. https://doi.org/10.4142/jvs.2019.20.e29

    Article  PubMed  PubMed Central  Google Scholar 

  28. Wataradee S, Boonserm T, Srangaprakon C, Ajariyakhajorn K, Inchaisri C (2021) Use of an automatic needle-free injection device for foot-and-mouth disease vaccination in dairy heifers. Vet Med-Czech 66:87–93

    Article  CAS  Google Scholar 

  29. Mahakapuge TAN, Every AL, Scheerlinck JP (2015) Exploring local immune responses to vaccines using efferent lymphatic cannulation. Expert Rev Vaccines 14(4):579–588

    Article  CAS  Google Scholar 

  30. Cedillo-Barron L, Foster-Cuevas M, Belsham GJ, Lefevre F, Parkhouse RM (2001) Induction of a protective response in swine vaccinated with DNA encoding foot-and-mouth disease virus empty capsid proteins and the 3D RNA polymerase. J Gen Virol 82:1713–1724

    Article  CAS  Google Scholar 

  31. Doel TR (2003) FMD vaccines. Virus Res 91:81–99

    Article  CAS  Google Scholar 

  32. Mulcahy G, Gale C, Robertson P, Iyisan S, DiMarchi RD, Doel TR (1990) Isotype responses of infected, virus-vaccinated and peptide-vaccinated cattle to foot-and-mouth disease virus. Vaccine 8(3):249–256. https://doi.org/10.1016/0264-410X(90)90054-P

    Article  CAS  PubMed  Google Scholar 

  33. Capozzo AV, Periolo OH, Robiolo B, Seki C, La Torre JL, Grigera PR (1997) Total and isotype humoral responses in cattle vaccinated with foot and mouth disease virus (FMDV) immunogen produced either in bovine tongue tissue or in BHK-21 cell suspension cultures. Vaccine 15(6–7):624–630. https://doi.org/10.1016/s0264-410x(96)00284-8

    Article  CAS  PubMed  Google Scholar 

  34. Oreskovic Z, Nechvatalova K, Krejci J, Kummer V, Faldyna M (2019) Aspects of intradermal immunization with different adjuvants: The role of dendritic cells and Th1/Th2 response. PLoS One 14(2):e0211896. https://doi.org/10.1371/journal.pone.0211896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the Şap Institute's resources. The authors thank Ertan Ağtürk and Mehmet Karakaya for guidance. Banu Bayri Özbilge and Ömer Şişman are acknowledged for their technical help.

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This work was supported by the Şap Institute's resources.

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Correspondence to Can Çokçalışkan.

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The study was carried out according to the approval given by the local ethics committee of the Foot-and-Mouth (Şap) Institute (Ethics Committee Decision No: 2020/1).

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Handling Editor: Sheela Ramamoorthy.

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Çokçalışkan, C., Tuncer-Göktuna, P., Sareyyüpoğlu, B. et al. Booster administration can make a difference in the antibody response to intradermal foot-and-mouth disease vaccination in cattle. Arch Virol 167, 405–413 (2022). https://doi.org/10.1007/s00705-021-05273-x

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  • DOI: https://doi.org/10.1007/s00705-021-05273-x

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