Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2015, Article ID 678084, 13 pages
http://dx.doi.org/10.1155/2015/678084
Research Article

A High-Performance Multiplex Immunoassay for Serodiagnosis of Flavivirus-Associated Neurological Diseases in Horses

1UMR 1161 of Virology, ANSES, INRA, ENVA, ANSES Animal Health Laboratory, EU-RL on Equine Diseases, UPE, 94701 Maisons-Alfort, France
2UMR PIMIT (I2T Team), INSERM U1187, CNRS 9192, IRD 249, Technology Platform CYROI, University of Reunion, 97491 Saint-Clotilde, Réunion
3Department of Infections and Epidemiology, Institut Pasteur, 75724 Paris, France
4Viral Zoonoses, Emerging and Vector-Borne Infections Group, Institute of Virology, University of Veterinary Medicine Vienna, 1210 Vienna, Austria
5Department of Microbiology and Immunology, College of Medicine and Health Sciences, Sultan Qaboos University, 123 Al-Khoudh, Oman
6INRA UE 1277, Plate-Forme d’Infectiologie Expérimentale, 37380 Nouzilly, France
7Equine Research Institute, Japan Racing Association, Tochigi 329-0412, Japan

Received 11 March 2015; Accepted 12 May 2015

Academic Editor: Sulagna Das

Copyright © 2015 Cécile Beck et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. Z. Hubálek and J. Halouzka, “West Nile fever—a reemerging mosquito-borne viral disease in Europe,” Emerging Infectious Diseases, vol. 5, no. 5, pp. 643–650, 1999. View at Publisher · View at Google Scholar · View at Scopus
  2. J. Süss, “Tick-borne encephalitis 2010: epidemiology, risk areas, and virus strains in Europe and Asia-An overview,” Ticks and Tick-borne Diseases, vol. 2, no. 1, pp. 2–15, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. S. L. Hills and D. C. Phillips, “Past, present, and future of Japanese encephalitis,” Emerging Infectious Diseases, vol. 15, no. 8, p. 1333, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. M. G. Guzman, S. B. Halstead, H. Artsob et al., “Dengue: a continuing global threat,” Nature Reviews Microbiology, vol. 8, no. 12, supplement, pp. S7–S16, 2010. View at Publisher · View at Google Scholar
  5. G. Kuno, G.-J. J. Chang, K. R. Tsuchiya, N. Karabatsos, and C. B. Cropp, “Phylogeny of the genus Flavivirus,” Journal of Virology, vol. 72, no. 1, pp. 73–83, 1998. View at Google Scholar · View at Scopus
  6. C. Beck, M. A. Jimenez-Clavero, A. Leblond et al., “Flaviviruses in Europe: complex circulation patterns and their consequences for the diagnosis and control of West Nile disease,” International Journal of Environmental Research and Public Health, vol. 10, no. 11, pp. 6049–6083, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. A. T. de Madrid and J. S. Porterfield, “The flaviviruses (group B arboviruses): a cross neutralization study,” Journal of General Virology, vol. 23, no. 1, pp. 91–96, 1974. View at Publisher · View at Google Scholar · View at Scopus
  8. D. Ghosh and A. Basu, “Japanese encephalitis—a pathological and clinical perspective,” PLoS Neglected Tropical Diseases, vol. 3, no. 9, article e437, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. J. J. Sejvar, “Clinical manifestations and outcomes of West Nile virus infection,” Viruses, vol. 6, no. 2, pp. 606–623, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. E. A. Gould, “Evolution of the Japanese encephalitis serocomplex viruses,” Current Topics in Microbiology and Immunology, vol. 267, pp. 391–404, 2002. View at Google Scholar · View at Scopus
  11. S. T. Sonnleitner, J. Simeoni, R. Baumgartner et al., “The spreading of flaviviruses over the continental divide: a challenge for serological diagnostics,” Journal of Medical Microbiology & Diagnosis, vol. 3, article 002, 2013. View at Publisher · View at Google Scholar
  12. A. Papa, D. Karabaxoglou, and A. Kansouzidou, “Acute West Nile virus neuroinvasive infections: cross-reactivity with dengue virus and tick-borne encephalitis virus,” Journal of Medical Virology, vol. 83, no. 10, pp. 1861–1865, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. G. Dauphin and S. Zientara, “West Nile virus: recent trends in diagnosis and vaccine development,” Vaccine, vol. 25, no. 30, pp. 5563–5576, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. D. Nash, F. Mostashari, A. Fine et al., “The outbreak of West Nile virus infection in the New York City area in 1999,” The New England Journal of Medicine, vol. 344, no. 24, pp. 1807–1814, 2001. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Tamba, P. Bonilauri, R. Bellini et al., “Detection of usutu virus within a west nile virus surveillance program in northern Italy,” Vector-Borne and Zoonotic Diseases, vol. 11, no. 5, pp. 551–557, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. A. Vázquez, M. Jiménez-Clavero, L. Franco et al., “Usutu virus: potential risk of human disease in Europe,” Eurosurveillance, vol. 16, no. 31, 2011. View at Google Scholar
  17. M. Calzolari, P. Gaibani, R. Bellini et al., “Mosquito, bird and human surveillance of west nile and Usutu viruses in Emilia-Romagna region (italy) in 2010,” PLoS ONE, vol. 7, no. 5, Article ID e38058, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. T. Oliphant, G. E. Nybakken, S. K. Austin et al., “Induction of epitope-specific neutralizing antibodies against West Nile virus,” Journal of Virology, vol. 81, no. 21, pp. 11828–11839, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Lobigs and M. S. Diamond, “Feasibility of cross-protective vaccination against flaviviruses of the Japanese encephalitis serocomplex,” Expert Review of Vaccines, vol. 11, no. 2, pp. 177–187, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. D. W. C. Beasley, M. R. Holbrook, A. P. A. Travassos Da Rosa et al., “Use of a recombinant envelope protein subunit antigen for specific serological diagnosis of West Nile virus infection,” Journal of Clinical Microbiology, vol. 42, no. 6, pp. 2759–2765, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. M. R. Holbrook, R. E. Shope, and A. D. T. Barrett, “Use of recombinant E protein domain III-based enzyme-linked immunosorbent assays for differentiation of tick-borne encephalitis serocomplex flaviviruses from mosquito-borne flaviviruses,” Journal of Clinical Microbiology, vol. 42, no. 9, pp. 4101–4110, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. D. Ludolfs, M. Niedrig, J. T. Paweska, and H. Schmitz, “Reverse ELISA for the detection of anti West Nile virus IgG antibodies in humans,” European Journal of Clinical Microbiology and Infectious Diseases, vol. 26, no. 7, pp. 467–473, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Bhardwaj, M. Holbrook, R. E. Shope, A. D. T. Barrett, and S. J. Watowich, “Biophysical characterization and vector-specific antagonist activity of domain III of the tick-borne flavivirus envelope protein,” Journal of Virology, vol. 75, no. 8, pp. 4002–4007, 2001. View at Publisher · View at Google Scholar · View at Scopus
  24. J. J. H. Chu, R. Rajamanonmani, J. Li, R. Bhuvananakantham, J. Lescar, and M.-L. Ng, “Inhibition of West Nile virus entry by using a recombinant domain III from the envelope glycoprotein,” Journal of General Virology, vol. 86, part 2, pp. 405–412, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. M. D. Sánchez, T. C. Pierson, M. M. DeGrace et al., “The neutralizing antibody response against West Nile virus in naturally infected horses,” Virology, vol. 359, no. 2, pp. 336–348, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. T. Oliphant, M. Engle, G. E. Nybakken et al., “Development of a humanized monoclonal antibody with therapeutic potential against West Nile virus,” Nature Medicine, vol. 11, no. 5, pp. 522–530, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. D. W. C. Beasley and A. D. T. Barrett, “Identification of neutralizing epitopes within structural domain III of the West Nile virus envelope protein,” Journal of Virology, vol. 76, no. 24, pp. 13097–13100, 2002. View at Publisher · View at Google Scholar · View at Scopus
  28. G. E. Nybakken, T. Oliphant, S. Johnson, S. Burke, M. S. Diamond, and D. H. Fremont, “Structural basis of West Nile virus neutralization by a therapeutic antibody,” Nature, vol. 437, no. 7059, pp. 764–769, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. W. M. P. B. Wahala, A. A. Kraus, L. B. Haymore, M. A. Accavitti-Loper, and A. M. de Silva, “Dengue virus neutralization by human immune sera: role of envelope protein domain III-reactive antibody,” Virology, vol. 392, no. 1, pp. 103–113, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. P. Danecek, W. Lu, and C. H. Schein, “PCP consensus sequences of flaviviruses: correlating variance with vector competence and disease phenotype,” Journal of Molecular Biology, vol. 396, no. 3, pp. 550–563, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. G. Añez, R. Men, K. H. Eckels, and C.-J. Lai, “Passage of dengue virus type 4 vaccine candidates in fetal rhesus lung cells selects heparin-sensitive variants that result in loss of infectivity and immunogenicity in rhesus macaques,” Journal of Virology, vol. 83, no. 20, pp. 10384–10394, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Nickells and T. J. Chambers, “Neuroadapted yellow fever virus 17D: determinants in the envelope protein govern neuroinvasiveness for SCID mice,” Journal of Virology, vol. 77, no. 22, pp. 12232–12242, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. C. W. Mandl, S. L. Allison, H. Holzmann, T. Meixner, and F. X. Heinz, “Attenuation of tick-borne encephalitis virus by structure-based site-specific mutagenesis of a putative flavivirus receptor binding site,” Journal of Virology, vol. 74, no. 20, pp. 9601–9609, 2000. View at Publisher · View at Google Scholar · View at Scopus
  34. K. Hiramatsu, M. Tadano, R. Men, and C.-J. Lai, “Mutational analysis of a neutralization epitope on the dengue type 2 virus (DEN2) envelope protein: monoclonal antibody resistant DEN2/DEN4 chimeras exhibit reduced mouse neurovirulence,” Virology, vol. 224, no. 2, pp. 437–445, 1996. View at Publisher · View at Google Scholar · View at Scopus
  35. F. J. van der Wal, R. P. Achterberg, S. M. de Boer et al., “Bead-based suspension array for simultaneous detection of antibodies against the Rift Valley fever virus nucleocapsid and Gn glycoprotein,” Journal of Virological Methods, vol. 183, no. 2, pp. 99–105, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. S. J. Wong, V. L. Demarest, R. H. Boyle et al., “Detection of human anti-flavivirus antibodies with a west nile virus recombinant antigen microsphere immunoassay,” Journal of Clinical Microbiology, vol. 42, no. 1, pp. 65–72, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. T.-H. Chen, F. Lee, Y.-L. Lin et al., “Development of a Luminex assay for the detection of swine antibodies to non-structural proteins of foot-and-mouth disease virus,” Journal of Immunological Methods, vol. 396, no. 1-2, pp. 87–95, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Sánchez-Matamoros, C. Beck, D. Kukielka et al., “Development of a microsphere-based immunoassay for serological detection of african horse sickness virus and comparison with other diagnostic techniques,” Transboundary and Emerging Diseases, 2015. View at Publisher · View at Google Scholar
  39. P. Koraka, H. Zeller, M. Niedrig, A. D. M. E. Osterhaus, and J. Groen, “Reactivity of serum samples from patients with a flavivirus infection measured by immunofluorescence assay and ELISA,” Microbes and Infection, vol. 4, no. 12, pp. 1209–1215, 2002. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Hirota, H. Nishi, H. Matsuda, H. Tsunemitsu, and S. Shimizu, “Cross-reactivity of Japanese encephalitis virus-vaccinated horse sera in serodiagnosis of West Nile Virus,” Journal of Veterinary Medical Science, vol. 72, no. 3, pp. 369–372, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. J. O. Rushton, S. Lecollinet, Z. Hubálek, P. Svobodová, H. Lussy, and N. Nowotny, “Tick-borne encephalitis virus in horses, Austria, 2011,” Emerging Infectious Diseases, vol. 19, no. 4, pp. 635–637, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. C. Klaus, U. Hörügel, B. Hoffmann, and M. Beer, “Tick-borne encephalitis virus (TBEV) infection in horses: clinical and laboratory findings and epidemiological investigations,” Veterinary Microbiology, vol. 163, no. 3-4, pp. 368–372, 2013. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Šikutová, S. Hornok, Z. Hubálek, I. Doležálková, Z. Juřicová, and I. Rudolf, “Serological survey of domestic animals for tick-borne encephalitis and Bhanja viruses in northeastern Hungary,” Veterinary Microbiology, vol. 135, no. 3-4, pp. 267–271, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. A.-C. Bréhin, L. Rubrecht, M. E. Navarro-Sanchez et al., “Production and characterization of mouse monoclonal antibodies reactive to Chikungunya envelope E2 glycoprotein,” Virology, vol. 371, no. 1, pp. 185–195, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. M. Faresjö, “A useful guide for analysis of immune markers by fluorochrome (Luminex) technique,” in Cytokine Bioassays, vol. 1172 of Methods in Molecular Biology, pp. 87–96, Springer, New York, NY, USA, 2014. View at Publisher · View at Google Scholar
  46. C. Klaus, U. Ziegler, D. Kalthoff, B. Hoffmann, and M. Beer, “Tick-borne encephalitis virus (TBEV)—findings on cross reactivity and longevity of TBEV antibodies in animal sera,” BMC Veterinary Research, vol. 10, article 78, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. A. Arnal, E. Gómez-Díaz, M. Cerdà-Cuéllar et al., “Circulation of a Meaban-like virus in yellow-legged gulls and seabird ticks in the Western Mediterranean Basin,” PLoS ONE, vol. 9, no. 3, Article ID e89601, 2014. View at Publisher · View at Google Scholar · View at Scopus
  48. R. Bargaoui, S. Lecollinet, and R. Lancelot, “Mapping the serological prevalence rate of west nile Fever in equids, Tunisia,” Transboundary and Emerging Diseases, vol. 62, no. 1, pp. 55–66, 2015. View at Publisher · View at Google Scholar · View at Scopus
  49. J. A. Farfán-Ale, B. J. Blitvich, N. L. Marlenee et al., “Antibodies to West Nile virus in asymptomatic mammals, birds, and reptiles in the Yucatan Peninsula of Mexico,” The American Journal of Tropical Medicine and Hygiene, vol. 74, no. 5, pp. 908–914, 2006. View at Google Scholar
  50. J. Y. Yeh, J. H. Lee, J. Y. Park et al., “A diagnostic algorithm to serologically differentiate West Nile virus from Japanese encephalitis virus infections and its validation in field surveillance of poultry and horses,” Vector-Borne and Zoonotic Diseases, vol. 12, no. 5, pp. 372–379, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Zohaib, M. Saqib, C. Beck, and et al, “High prevalence of West Nile virus in equines from the two provinces of Pakistan,” Epidemiology and Infection, pp. 1–5, 2014. View at Publisher · View at Google Scholar
  52. S. Pradier, A. Sandoz, M. C. Paul et al., “Importance of wetlands management for West Nile Virus circulation risk, Camargue, Southern France,” International Journal of Environmental Research and Public Health, vol. 11, no. 8, pp. 7740–7754, 2014. View at Google Scholar
  53. J. H. Chávez, J. R. Silva, A. A. Amarilla, and L. T. Moraes Figueiredo, “Domain III peptides from flavivirus envelope protein are useful antigens for serologic diagnosis and targets for immunization,” Biologicals, vol. 38, no. 6, pp. 613–618, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. L. Mathengtheng and F. J. Burt, “Use of envelope domain III protein for detection and differentiation of flaviviruses in the Free State Province, South Africa,” Vector-Borne and Zoonotic Diseases, vol. 14, no. 4, pp. 261–271, 2014. View at Publisher · View at Google Scholar
  55. S. J. Wong, R. H. Boyle, V. L. Demarest et al., “Immunoassay targeting nonstructural protein 5 to differentiate West Nile virus infection from dengue and St. Louis encephalitis virus infections and from flavivirus vaccination,” Journal of Clinical Microbiology, vol. 41, no. 9, pp. 4217–4223, 2003. View at Publisher · View at Google Scholar · View at Scopus