Advertisement

Immunologic Research

, Volume 66, Issue 6, pp 777–782 | Cite as

From the bluetongue vaccination campaigns in sheep to overimmunization and ovine ASIA syndrome

  • J. Asín
  • M. Pérez
  • P. Pinczowski
  • M. Gimeno
  • L. LujánEmail author
Original Article

Abstract

The use of vaccines has proven to be very effective in controlling and eradicating infectious diseases, both in veterinary and human medicine; however, vaccines can be also the source of an array of problems caused by procedures such as overimmunization. Bluetongue, an orbiviral disease that affects ruminants, is best controlled by the use of inactivated vaccines. During the last years of the past decade, these vaccines were applied all over Europe to control the spreading of the disease, a goal that was accomplished; however, at the same time, several adverse effects related to the vaccination were reported. Especially in sheep, this vaccination campaign brought out a new cachectic and neurologic disease with harmful consequences for the ovine industry. This disease is now recognized as the ovine version of the autoimmune/inflammatory syndrome induced by adjuvants (ASIA syndrome) and poses an immense challenge in veterinary medicine, immunology, and vaccinology.

Keywords

Sheep Overimmunization Ovine ASIA syndrome Bluetongue Aluminum-based adjuvant 

Notes

Compliance with ethical standards

Conflict of Interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

References

  1. 1.
    Strassburg MA. The global eradication of smallpox. Am J Infect Control. 1982;10:53–9.CrossRefGoogle Scholar
  2. 2.
    Roeder PL. Rinderpest: the end of cattle plague. Prev Vet Med. 2011;102:98–106.  https://doi.org/10.1016/j.prevetmed.2011.04.004.CrossRefGoogle Scholar
  3. 3.
    Greenwood B. The contribution of vaccination to global health: past, present and future. Philos Trans R Soc Lond Ser B Biol Sci. 2014;369:20130433.  https://doi.org/10.1098/rstb.2013.0433.CrossRefGoogle Scholar
  4. 4.
    Pastoret PP, Jones P. Veterinary vaccines for animal and public health. Dev Biol (Basel). 2004;119:15–29.Google Scholar
  5. 5.
    Garrido JM, Sevilla IA, Beltrán-Beck B, Minguijón E, Ballesteros C, Galindo RC, et al. Protection against tuberculosis in Eurasian wild boar vaccinated with heat-inactivated Mycobacterium bovis. PLoS One. 2011;6:e24905.  https://doi.org/10.1371/journal.pone.0024905.CrossRefGoogle Scholar
  6. 6.
    Lütticken D, Segers RP, Visser N. Veterinary vaccines for public health and prevention of viral and bacterial zoonotic diseases. Rev Sci Tech. 2007;26:165–77.CrossRefGoogle Scholar
  7. 7.
    Meeusen EN, Walker J, Peters A, Pastoret PP, Jungersen G. Current status of veterinary vaccines. Clin Microbiol Rev. 2007;20:489–510.CrossRefGoogle Scholar
  8. 8.
    van Oirschot JT. Vaccination in food animal populations. Vaccine. 1994;12:415–8.CrossRefGoogle Scholar
  9. 9.
    Cockburn TA. The evolution and eradication of infectious diseases. Baltimore: The Johns Hopkins University Press; 1963.Google Scholar
  10. 10.
    Morens DM, Folkers GK, Fauci AS. The challenge of emerging and re-emerging infectious diseases. Nature. 2004;430:242–9.CrossRefGoogle Scholar
  11. 11.
    Shoenfeld Y, Agmon-Levin N. ‘ASIA’ - autoimmune/inflammatory syndrome induced by adjuvants. J Autoimmun. 2011;36:4–8.  https://doi.org/10.1016/j.jaut.2010.07.003.CrossRefGoogle Scholar
  12. 12.
    Tsumiyama K, Miyazaki Y, Shiozawa S. Self-organized criticality theory of autoimmunity. PLoS One. 2009;4:e8382.CrossRefGoogle Scholar
  13. 13.
    Poddighe D, Castelli L, Marseglia GL, Bruni P. A sudden onset of a pseudo-neurological syndrome after HPV-16/18 AS04-adjuvated vaccine: might it be an autoimmune/inflammatory syndrome induced by adjuvants (ASIA) presenting as a somatoform disorder? Immunol Res. 2014;60(2–3):236–46.  https://doi.org/10.1007/s12026-014-8575-3.CrossRefGoogle Scholar
  14. 14.
    Cadusseau J, Ragunathan-Thangarajah N, Surenaud M, Hue S, Authier FJ, Gherardi RK. Selective elevation of circulating CCL2/MCP1 levels in patients with longstanding post-vaccinal macrophagic myofasciitis and ASIA. Curr Med Chem. 2014;21(4):511–7.CrossRefGoogle Scholar
  15. 15.
    Sturkenboom MC. The narcolepsy-pandemic influenza story: can the truth ever be unraveled? Vaccine. 2015;33(Suppl. 2):B6–B13.  https://doi.org/10.1016/j.vaccine.2015.03.026.CrossRefGoogle Scholar
  16. 16.
    Van Der Gucht A, Aoun Sebaiti M, Itti E, Aouizerate J, Evangelista E, Chalaye J, et al. Neuropsychological correlates of brain perfusion SPECT in patients with macrophagic myofasciitis. PLoS One. 2015;10(6):e0128353.  https://doi.org/10.1371/journal.pone.0128353.CrossRefGoogle Scholar
  17. 17.
    Trinca JC. Over-immunization-an ever present problem. Aust Fam Physician. 1976;5:734–55.Google Scholar
  18. 18.
    Moore GE, Guptill LF, Ward MP, Glickman NW, Faunt KK, Lewis HB, et al. Adverse events diagnosed within three days of vaccine administration in dogs. J Am Vet Med Assoc. 2005;227:1102–8.CrossRefGoogle Scholar
  19. 19.
    Moore GE, Ward MP, Kulldorff M, Caldanaro RJ, Guptill LF, Lewis HB, et al. A space-time cluster of adverse events associated with canine rabies vaccine. Vaccine. 2005;23:5557–62.CrossRefGoogle Scholar
  20. 20.
    Moore GE, DeSantis-Kerr AC, Guptill LF, Glickman NW, Lewis HB, Glickman LT. Adverse events after vaccine administration in cats: 2,560 cases (2002-2005). J Am Vet Med Assoc. 2007;231:94–100.CrossRefGoogle Scholar
  21. 21.
    Moore GE, Glickman NW, Ward MP, Engler KS, Lewis HB, Glickman LT. Incidence of and risk factors for adverse events associated with distemper and rabies vaccine administration in ferrets. J Am Vet Med Assoc. 2005;226(6):909–12.CrossRefGoogle Scholar
  22. 22.
    Day MJ. Vaccine safety in the neonatal period. J Comp Pathol. 2007;137(Suppl. 1):S51–6.CrossRefGoogle Scholar
  23. 23.
    HogenEsch H, Azcona-Olivera J, Scott-Moncrieff C, Snyder PW, Glickman LT. Vaccine-induced autoimmunity in the dog. Adv Vet Med. 1999;41:733–47.CrossRefGoogle Scholar
  24. 24.
    Ortloff A, Morán G, Olavarría A, Folch H. Membranoproliferative glomerulonephritis possibly associated with over-vaccination in a cocker spaniel. J Small Anim Pract. 2010;51:499–502.  https://doi.org/10.1111/j.1748-5827.2010.00978.x.CrossRefGoogle Scholar
  25. 25.
    Koppang EO, Bjerkås I, Haugarvoll E, Chan EK, Szabo NJ, Ono N, et al. Vaccination-induced systemic autoimmunity in farmed Atlantic salmon. J Immunol. 2008;181:4807–14.CrossRefGoogle Scholar
  26. 26.
    Haugarvoll E, Bjerkås I, Szabo NJ, Satoh M, Koppang EO. Manifestations of systemic autoimmunity in vaccinated salmon. Vaccine. 2010;28:4961–9.  https://doi.org/10.1016/j.vaccine.2010.05.032.CrossRefGoogle Scholar
  27. 27.
    Petrik MS, Wong MC, Tabata RC, Garry RF, Shaw CA. Aluminum adjuvant linked to Gulf War illness induces motor neuron death in mice. NeuroMolecular Med. 2007;9:83–100.CrossRefGoogle Scholar
  28. 28.
    Gherardi RK, Eidi H, Crépeaux G, Authier FJ, Cadusseau J. Biopersistence and brain translocation of aluminum adjuvants of vaccines. Front Neurol. 2015;6:4.  https://doi.org/10.3389/fneur.2015.00004.CrossRefGoogle Scholar
  29. 29.
    Schrauwen E, van Ham L. Postvaccinal acute polyradiculoneuritis in a young dog. Prog Vet Neurol. 1995;6:68–70.Google Scholar
  30. 30.
    Gehring R, Eggars B. Suspected post-vaccinal acute polyradiculoneuritis in a puppy. J S Afr Vet Assoc. 2001;72:96.Google Scholar
  31. 31.
    Quiroz-Rothe E, Ginel PJ, Pérez J, Lucena R, Rivero JLL. Vaccine-associated acute polyneuropathy resembling Guillain-Barré syndrome in a dog. Eur J Comp An Prac. 2005;15:155–9.Google Scholar
  32. 32.
    OIE-World Organization for Animal Health. OIE Technical Disease Cards: Bluetongue. http://www.oie.int/fileadmin/Home/eng/Animal_Health_in_the_World/docs/pdf/Disease_cards/BLUETONGUE.pdf. 2013; Accessed 20.06.2018.
  33. 33.
    Mellor PS, Carpenter S, Harrup L, Baylis M, Mertens PP. Bluetongue in Europe and the Mediterranean Basin: history of occurrence prior to 2006. Prev Vet Med. 2008;87:4–20.  https://doi.org/10.1016/j.prevetmed.2008.06.002.CrossRefGoogle Scholar
  34. 34.
    Carpenter S, Wilson A, Mellor PS. Culicoides and the emergence of bluetongue virus in northern Europe. Trends Microbiol. 2009;17:172–8.  https://doi.org/10.1016/j.tim.2009.01.001.CrossRefGoogle Scholar
  35. 35.
    UE Commission Decision 2008/655/EC, 24 July 2008, approving the emergency vaccination plans against bluetongue of certain Member States and fixing the level of the Community’s financial contribution for 2007 and 2008.http://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A32008D0655. 2008; Accessed 20.06.2018.
  36. 36.
    Agence Française de Sécurité Sanitaire (AFSS). Review of adverse effects observed after vaccination against bluetongue, serotype 1 and serotype 8, as of 31/05/2009. https://www.anses.fr/en/system/files/ANMV-Fi-VaccinFCOEN.pdf. 2009; Accessed 20.06.2018.
  37. 37.
    Nusinovici S, Seegers H, Joly A, Beaudeau F, Fourichon C. A side effect of decreased fertility associated with vaccination against bluetongue virus serotype 8 in Holstein dairy cows. Prev Vet Med. 2011;101:42–50.  https://doi.org/10.1016/j.prevetmed.2011.05.011.CrossRefGoogle Scholar
  38. 38.
    Questions écrites et orales - Assemblée nationale. Question n° 74498. http://questions.assemblee-nationale.fr/q14/14-74498QE.htm. 2015; Accessed 20.06.2018.
  39. 39.
    Questions écrites et orales - Assemblée nationale. Question n° 74975. http://questions.assemblee-nationale.fr/q14/14-74975QE.htm. 2015; Accessed 20.06.2018.
  40. 40.
    Tschuor AC, Kaufmann T, Strabel D, Hässig M. Investigation of abortions and other animal health problems in relation to vaccination against Bluetongue virus in 2009. Schweiz Arch Tierheilkd. 2010;152:501–6.  https://doi.org/10.1024/0036-7281/a000115 In German.CrossRefGoogle Scholar
  41. 41.
    Probst C, Gethmann JM, Höreth-Böntgen D, Cussler K, Conraths FJ. Lack of evidence for claims of farmers in south-eastern Germany regarding adverse reactions ascribed to BTV-8 vaccines. Berl Munch Tierarztl Wochenschr. 2011;124:282–7.Google Scholar
  42. 42.
    Dyer F, Brown E, Cooles S, Tait A. Suspected adverse reactions, 2008. Vet Rec. 2009;165:162–4.CrossRefGoogle Scholar
  43. 43.
    González JM, Figueras L, Ortega ME, Lozano M, de Arcaute MR, Royo R, et al. Possible adverse reactions in sheep after vaccination with inactivated BTV vaccines. Vet Rec. 2010;166:757–8.  https://doi.org/10.1136/vr.b4849.CrossRefGoogle Scholar
  44. 44.
    Luján L, Pérez M, Salazar E, Álvarez N, Gimeno M, Pinczowski P, et al. Autoimmune/autoinflammatory syndrome induced by adjuvants (ASIA syndrome) in commercial sheep. Immunol Res. 2013;56:317–24.  https://doi.org/10.1007/s12026-013-8404-0.CrossRefGoogle Scholar
  45. 45.
    The Ministry of Agriculture, Food and Environment, Spanish: Ministerio de Agricultura, Alimentación y Medio Ambiente (MAGRAMA). CRESA-Estudio de brotes de enfermedad en granjas de ovino en Cataluña y de su posible relación con la vacunación frente a la Lengua Azul [In Spanish]. http://rasve.magrama.es/Publica/Noticias/ficheros/Infome_CRESA_%20Posibles_Reacciones_Adversas_Vacunaci%C3%B3n_de_LenguaAzul.pdf. 2009; Accessed 12.12.2016. Now only available at https://www.oviespana.com/extras/pdf/gana156_2.pdf.
  46. 46.
    The Ministry of Agriculture, Food and Environment, Spanish: Ministerio de Agricultura, Alimentación y Medio Ambiente (MAGRAMA). VISAVET-Informe sobre el estudio del aumento de mortalidad en el ganado ovino y su posible relación con la vacunación de Lengua Azul [In Spanish]. http://rasve.magrama.es/Publica/Noticias/ficheros/Informe_VISAVET_Posibles_Reacciones_Adversas_Vacunaci%C3%B3n_de_LenguaAzul.pdf. 2009; Accessed 12.12.2016. Now only available at https://www.oviespana.com/extras/pdf/gana156_3.pdf.
  47. 47.
    European Medicines Agency (EMA)-Committee for Medicinal Products for Veterinary Use (CVMP). An overview of field safety data from the EU for Bluetongue virus vaccines serotype 8 emerging from the 2008 national vaccination campaigns. http://www.ema.europa.eu/docs/en_GB/document_library/Other/2009/12/WC500017480.pdf. 2009; Accessed 20.06.2018.
  48. 48.
    Perricone C, Colafrancesco S, Mazor RD, Soriano A, Agmon-Levin N, Shoenfeld Y. Autoimmune/inflammatory syndrome induced by adjuvants (ASIA) 2013: unveiling the pathogenic, clinical and diagnostic aspects. J Autoimmun. 2013;47:1–16.  https://doi.org/10.1016/j.jaut.2013.10.004.CrossRefGoogle Scholar
  49. 49.
    Li XB, Zheng H, Zhang ZR, Li M, Huang ZY, Schluesener HJ, et al. Glia activation induced by peripheral administration of aluminum oxide nanoparticles in rat brains. Nanomedicine. 2009;5(4):473–9.  https://doi.org/10.1016/j.nano.2009.01.013.CrossRefGoogle Scholar
  50. 50.
    Caito S, Aschner M. Neurotoxicity of metals. Handb Clin Neurol. 2015;131:169–89.  https://doi.org/10.1016/b978-0-444-62627-1.00011-153.CrossRefGoogle Scholar
  51. 51.
    Khan Z, Combadière C, Authier FJ, Itier V, Lux F, Exley C, et al. Slow CCL2-dependent translocation of biopersistent particles from muscle to brain. BMC Med. 2013;11:99.  https://doi.org/10.1186/1741-7015-11-99.CrossRefGoogle Scholar
  52. 52.
    Crépeaux G, Eidi H, David MO, Tzavara E, Giros B, Exley C, et al. Highly delayed systemic translocation of aluminum-based adjuvant in CD1 mice following intramuscular injections. J Inorg Biochem. 2015;152:199–205.  https://doi.org/10.1016/j.jinorgbio.2015.07.004.CrossRefGoogle Scholar
  53. 53.
    Crépeaux G, Eidi H, David MO, Baba-Amer Y, Tzavara E, Giros B, et al. Non-linear dose-response of aluminium hydroxide adjuvant particles: selective low dose neurotoxicity. Toxicology. 2016;375:4857.  https://doi.org/10.1016/j.tox.2016.11.018.CrossRefGoogle Scholar
  54. 54.
    Eisenbarth SC, Colegio OR, O'Connor W, Sutterwala FS, Flavell RA. Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature. 2008;453:1122–6.  https://doi.org/10.1038/nature06939.CrossRefGoogle Scholar
  55. 55.
    European Comission. Map showing showing the location of the restriction zones for different BTV serotypes in Europe until 16-04-2018; https://ec.europa.eu/food/sites/food/files/animals/docs/ad_control-measures_bt_restrictedzones-map.jpg. 2018; Accessed 20.06.2018.

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • J. Asín
    • 1
  • M. Pérez
    • 2
  • P. Pinczowski
    • 1
  • M. Gimeno
    • 1
  • L. Luján
    • 1
    Email author
  1. 1.Department of Animal Pathology, Veterinary FacultyUniversity of ZaragozaZaragozaSpain
  2. 2.Department of Anatomy, Embryology and Genetics, Veterinary FacultyUniversity of ZaragozaZaragozaSpain

Personalised recommendations