Oral vaccination and protection of red foxes (Vulpes vulpes) against rabies using ONRAB®, an adenovirus-rabies recombinant vaccine

Vaccine

Volumn 32, Issue 8, 2014, Pages 984-989

  Brown, L J ^a   Rosatte, R C ^a   Fehlner Gardiner, C ^b   Bachmann, P ^a   Ellison, J A ^c   Jackson, F R ^c   Taylor, J S ^a   Davies, C ^a   Donovan, D ^a  

^a TRENT UNIVERSITY   (Canada)

^b Ottawa Laboratory Fallowfield   (Canada)

^c NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

Author keywords

Human adenovirus serotype 5; Immune response; ONRAB ; Oral rabies vaccination; Rabies control; Rabies virus challenge; Red fox; Vulpes vulpes

Indexed keywords

ADENOVIRUS RABIES RECOMBINANT VACCINE; ADENOVIRUS VACCINE; NEUTRALIZING ANTIBODY; ONRAB; RABIES VACCINE; RECOMBINANT VACCINE; UNCLASSIFIED DRUG; VIRUS RNA;

ADULT; ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; FLUORESCENT ANTIBODY TECHNIQUE; HUMORAL IMMUNITY; LONGITUDINAL STUDY; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RABIES; RABIES VIRUS; VACCINATION; VULPES VULPES;

HUMAN ADENOVIRUS SEROTYPE 5; IMMUNE RESPONSE; ONRAB(®); ORAL RABIES VACCINATION; RABIES CONTROL; RABIES VIRUS CHALLENGE; RED FOX; VULPES VULPES;

ADENOVIRIDAE; ADMINISTRATION, ORAL; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; FOXES; IMMUNITY, HUMORAL; RABIES; RABIES VACCINES; VACCINES, SYNTHETIC;

EID: 84892966160     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2013.12.015     Document Type: Article

References (69)

1. Rosatte R.C., Tinline R.R., Johnston D.H. Rabies control in wild carnivores. Rabies 2007, 595-634. Academic Press, San Diego, CA. A. Jackson, W. Wunner (Eds.).
2. MacInnes C.D., Smith S.M., Tinline R.R., Ayers Neil R., Bachmann P., Ball D.G., et al. Elimination of rabies from red foxes in eastern Ontario. J Wildl Dis 2001, 37:119-132.
3. Rosatte R.C., Power M.J., Donovan D., Davies J.C., Allan M., Bachmann P., et al. Elimination of arctic variant rabies in red foxes, metropolitan Toronto. Emerg Infect Dis 2007, 13:25-27.
4. Tabel H., Corner A.H., Webster W.A., Casey C.A. History and epizootiology of rabies in Canada. Can Vet J 1974, 15:271-281.
5. Agriculture Canada Report of Rabies Diagnosed - 1958 to 1989, Ottawa 1958-1989.
6. Rosatte R., Allan M., Bachmann P., Sobey K., Donovan D., Davies J.C., et al. Prevalence of tetracycline and rabies virus antibody in raccoons, skunks, and foxes following aerial distribution of V-RG baits to control raccoon rabies in Ontario, Canada. J Wildl Dis 2008, 44:946-964.
7. Rosatte R.C., Donovan D., Allan M., Bruce L., Buchanan T., Sobey K., et al. The control of raccoon rabies in Ontario, Canada: proactive and reactive tactics, 1994-2007. J Wildl Dis 2009, 45:772-784.
8. Wandeler A.I. Raccoon rabies in eastern Ontario. Can J Vet Res 1999, 40:731.
9. Slate D., Algeo T.P., Nelson K.M., Chipman R.B., Donovan D., Blanton J.D., et al. Oral rabies vaccination in North America: opportunities, complexities, and challenges. PLoS Negl Trop Dis 2009, 3:e549.
10. ® rabies vaccine baits to control Arctic variant rabies in striped skunks in Ontario, Canada. J Wildl Dis 2011, 47:459-465.
11. Shwiff S.A., Nunan C.P., Kirkpatrick K.N., Shwiff S.S. A retrospective economic analysis of the Ontario red fox oral rabies vaccination programme. Zoonoses Public Health 2011, 58:169-177.
12. Wandeler A.I. Oral immunization against rabies: afterthoughts and foresight. Schweiz Arch Tierheilkd 2000, 142:455-462.
13. Black J.G., Lawson K.F. The safety and efficacy of immunizing foxes (Vulpes vulpes) using bait containing attenuated rabies virus vaccine. Can J Comp Med 1980, 44:169-176.
14. Artois M., Guittré C., Thomas I., Leblois H., Brochier B., Barrat J. Potential pathogenicity for rodents of vaccines intended for oral vaccination against rabies: a comparison. Vaccine 1992, 10:524-528.
15. Vos A., Neubert A., Aylan O., Schuster P., Pommerening E., Muller T., et al. An update on safety studies of SAD B19 rabies virus vaccine in target and non-target species. Epidemiol Infect 1999, 123:165-175.
16. Lawson K.F., Hertler R., Charlton K.M., Campbell J.B., Rhodes A.J. Safety and immunogenicity of ERA strain of rabies virus propagated in a BHK-21 cell line. Can J Vet Res 1989, 53:438-444.
17. Rupprecht C.E., Charlton K.M., Artois M., Casey G.A., Webster W.A., Campbell J.B., et al. Ineffectiveness and comparative pathogenicity attenuated rabies virus vaccines for the striped skunk (Mephitis mephitis). J Wildl Dis 1990, 26:99-102.
18. Fehlner-Gardiner C., Nadin-Davis S., Armstrong J., Muldoon F., Bachmann P., Wandeler A. Era vaccine-derived cases of rabies in wildlife and domestic animals in Ontario, Canada, 1989-2004. J Wildl Dis 2008, 44:71-85.
19. Müller T., Bätza H.-J., Beckert A., Bunzenthal C., Cox J.H., Freuling C.M., et al. Analysis of vaccine-virus-associated rabies cases in red foxes (Vulpes vulpes) after oral rabies vaccination campaigns in Germany and Austria. Arch Virol 2009, 154:1081-1091.
20. Winkler W.G., McLean R.G., Cowart J.C. Vaccination of foxes against rabies using ingested baits. J Wildl Dis 1975, 11:382-388.
21. Tolson N.D., Charlton K.M., Lawson K.F., Campbell J.B., Stewart R.B. Studies of ERA BHK-21 rabies vaccine in skunks and mice. Can J Vet Res 1988, 52:58-62.
22. Rupprecht C.E., Dietzschold B., Cox J.H., Schneider L.G. Oral vaccination of raccoons (Procyon lotor) with an attenuated (SAD-B19) rabies virus vaccine. J Wildl Dis 1989, 25:548-554.
23. Blancou J., Kieny M.P., Lathe R., Lecocq J.P., Pastoret P.-P., Soulebot J.P., et al. Oral vaccination of the fox against rabies using a live recombinant vaccinia virus. Nature 1986, 322:373-375.
24. Brochier B., Blancou J., Thomas I., Languet B., Artois M., Kieny M.-P., et al. Use of recombinant vaccinia-rabies glycoprotein virus for oral vaccination of wildlife against rabies: innocuity to several non-target bait consuming species. J Wildl Dis 1989, 25:540-547.
25. Brochier B., Costy F., Pastoret P.-P. Elimination of fox rabies from Belgium using a recombinant vaccinia-rabies vaccine: an update. Vet Microbiol 1995, 46:269-279.
26. Masson E., Aubert M.F.A., Barrat J., Vuillaume P. Comparison of the efficacy of the antirabies vaccines used for foxes in France. Vet Res 1996, 27:255-266.
27. Grosenbaugh D.A., Maki J.L., Rupprecht C.E., Wall D.K. Rabies challenge of captive striped skunks (Mephitis mephitis) following oral administration of a live vaccinia-vectored rabies vaccine. J Wildl Dis 2007, 43:124-128.
28. Brown L.J., Rosatte R.C., Fehlner-Gardiner C., Knowles M.K., Bachmann P., Davies J.C., et al. Immunogenicity and efficacy of two rabies vaccines in wild-caught, captive raccoons. J Wildl Dis 2011, 47:182-194.
29. ® oral rabies vaccine field performance in raccoons and striped skunks, New Brunswick, Canada, and Maine, USA. J Wildl Dis 2012, 48:157-167.
30. ® vaccine-bait field performance in Québec, Canada and Vermont, USA. J Wildl Dis 2013, 49:190-193.
31. Prevec L., Campbell J.B., Christie B.S., Belbeck L., Graham F.L. A recombinant human adenovirus vaccine against rabies. J Infect Dis 1990, 161:27-30.
32. Charlton K.M., Artois M., Prevec L., Campbell J.B., Casey G.A., Wandeler A.I., et al. Oral rabies vaccination of skunks and foxes with a recombinant human adenovirus vaccine. Arch Virol 1992, 123:169-179.
33. Yarosh O.K., Wandeler A.I., Graham F.L., Campbell J.B., Prevec L. Human adenovirus type 5 vectors expressing rabies glycoprotein. Vaccine 1996, 14:1257-1264.
34. Li J., Faber M., Papaneri A., Faber M.-L., McGettigan J.P., Schnell M.J., et al. A single immunization with a recombinant canine adenovirus expressing the rabies virus G protein confers protective immunity against rabies in mice. Virology 2006, 356:147-154.
35. Chawla T., Khanna N., Swaminathan S. Adenovirus-vectored vaccines. Expert Opin Ther Pat 2008, 18:293-307.
36. Tordo N., Foumier A., Jallet C., Szelechowski M., Klonjkowski B., Eloit M. Canine adenovirus based rabies vaccines. Developmental biology 2008, vol. 131:467-476. Karger, Basel.
37. Henderson H., Jackson F., Bean K., Panasuk B., Niezgoda M., Slate D., et al. Oral immunization of raccoons and skunks with a canine adenovirus recombinant rabies vaccine. Vaccine 2009, 27:7194-7197.
38. ® baits as a tactic to control rabies in raccoons and striped skunks in Ontario, Canada. J Wildl Dis 2009, 45:363-374.
39. ®, a human adenovirus rabies glycoprotein recombinant vaccine. J Wildl Dis 2012, 48:1010-1020.
40. Canadian Council on Animal Care (CCAC) Guidelines on: the care and use of wildlife 2003, Canadian Council on Animal Care, Ottawa.
41. Institute for Laboratory Animal Research Guide for the care and use of laboratory animals 2011, National Academies Press, Washington. 8th ed.
42. Kuzmin I.V., Shi M., Orciari L.A., Yager P.A., Velasco-Villa A., Kuzmina N.A., et al. Molecular inferences suggest multiple host shifts of rabies viruses from bats to mesocarnivores in Arizona during 2001-2009. PLoS Pathog 2012, 8:e1002786.
43. Dean D.J., Abelseth M.K., Atanasiu P. The fluorescent antibody test. Laboratory techniques in rabies 1996, 88-95. World Health Organization, Geneva, Switzerland. F.X. Meslin, M.M. Kaplan, H. Koprowski (Eds.).
44. Knowles M.K., Nadin-Davis S.A., Sheen M., Rosatte R., Mueller R., Beresford A. Safety studies on an adenovirus recombinant vaccine for rabies (AdRG1.3-ONRAB) in target and non-target species. Vaccine 2009, 27:6619-6626.
45. Lorenz R.J., Bogel K. Method of calculation. Laboratory techniques in rabies 1973, 321-335. World Health Organization, Geneva, Switzerland. M.M. Kaplan, H. Koprowski (Eds.).
46. Smith J.S., Yager P.A., Baer G.M. A rapid fluorescent focus inhibition test (RFFIT) for determining RVNA. Laboratory techniques in rabies 1996, 181-192. World Health Organization, Geneva, Switzerland. F.X. Meslin, M.M. Kaplan, H. Koprowski (Eds.).
47. Reed L.J., Muench H. A simple method of estimating fifty percent endpoints. Am J Hyg 1938, 27:493-497.
48. Zar J.H. Biostatistical analysis 1999, Prentice-Hall, Inc., Upper Saddle River, NJ. 4th ed.
49. Artois M., Masson E., Barrat J., Aubert M.F.A. Efficacy of three oral rabies vaccine-baits in the red fox: a comparison. Vet Microbiol 1993, 38:167-172.
50. Cliquet F., Barrat J., Guiot A.L., Caël N., Boutrand S., Maki J., et al. Efficacy and bait acceptance of vaccinia vectored rabies glycoprotein vaccine in captive foxes (Vulpes vulpes), raccoon dogs (Nyctereutes procyonoides) and dogs (Canis familiaris). Vaccine 2008, 26:4627-4638.
51. Tolson N.D., Charlton K.M., Casey G.A., Knowles M.K., Rupprecht C.E., Lawson K.F., et al. Immunization of foxes against rabies with a vaccinia recombinant virus expressing the rabies glycoprotein. Arch Virol 1988, 102:297-301.
52. Lawson K.F., Chiu H., Matson M., Bachmann P., Campbell J.B. Studies on efficacy and stability of a vaccine bait containing ERA strain of rabies virus propagated in a BHK-21 cell line. Can J Vet Res 1992, 56:135-141.
53. Lawson K.F., Chiu H., Crosgrey S.J., Matson M., Casey G.A., Campbell J.B. Duration of immunity in foxes vaccinated orally with ERA vaccine in a bait. Can J Vet Res 1997, 61:39-42.
54. Neubert A., Schuster P., Muller T., Vos A., Pommerening E. Immunogenicity and efficacy of the oral rabies vaccine SAD B19 in foxes. J Vet Med B 2001, 48:179-183.
55. ®. Vaccine 2013.
56. Sobey K.G., Walpole A.A., Rosatte R., Fehlner-Gardiner C., Donovan D., Bachmann P., et al. An assessment of ONRAB oral rabies vaccine persistence in free-ranging mammal populations in Ontario, Canada. Vaccine 2013, 31:2207-2213.
57. ® in select non-target wildlife. Vaccine 2013, 31:3839-3842.
58. Vuillaume P., Bruyère V., Aubert M. Comparison of the effectiveness of two protocols of antirabies bait distribution for foxes (Vulpes vulpes). Vet Res 1998, 29:537-546.
59. Bruyère V., Vuillaume P., Cliquet F., Aubert M. Oral rabies vaccination of foxes with one or two delayed distributions of SAG2 baits during the spring. Vet Res 2000, 31:339-345.
60. Brochier B., Dechamps P., Costy F., Hallet L., Leuris J., Villers M., et al. Elimination de la rage en Belgique par la vaccination du renard roux (Vulpes vulpes). Ann Med Vet 2001, 145:293-305.
61. Bugnon P., Breitenmoser U., Peterhans E., Zanoni R. Efficacy of oral vaccination in the final stage of fox rabies elimination in Switzerland. J Vet Med B 2004, 51:433-437.
62. Cliquet F., Combes B., Barrat J. Means used for terrestrial rabies elimination in France and policy for rabies surveillance in case of re-emergence. Developmental biology 2006, vol. 125:119-126. Karger, Basel.
63. Lambot M., Blasco E., Barrat J., Cliquet F., Brochier B., Renders C., et al. Humoral and cell-mediated immune responses of foxes (Vulpes vulpes) after experimental primary and secondary oral vaccination using SAG2 and V-RG vaccines. Vaccine 2001, 19:1827-1835.
64. Johnston D.H., Voigt D.R. A baiting system for the oral rabies vaccination of wild foxes and skunks. Comp Immunol Microbiol Infect Dis 1982, 5:185-186.
65. Bachmann P., Bramwell R.N., Fraser S.J., Gilmore D.A., Johnston D.H., Lawson K.F., et al. Wild carnivore acceptance of baits for delivery of liquid rabies vaccine. J Wildl Dis 1990, 26:486-501.
66. Black J.G., Lawson K.F. Further studies of sylvatic rabies in the fox (Vulpes vulpes), vaccination by the oral route. Can Vet J 1973, 14:206-211.
67. Winkler W.G., Baer G.M. Rabies immunization of red foxes (Vulpes fulva) with vaccine in sausage baits. Am J Epidemiol 1976, 103:408-415.
68. Kieny M.P., Blancou J., Lathe R., Pastoret P.-P., Soulebot J.-P., Desmettre P., et al. Development of animal recombinant DNA vaccine and its efficacy in foxes. Rev Infect Dis 1988, 10:S799-S802.
69. Brochier B.M., Languet B., Artois M., Zanker S., Guittré C., Blancou J., et al. Efficacy of a baiting system for vaccinating foxes against rabies with vaccinia-rabies recombinant virus. Vet Rec 1990, 127:165-167.