Oral vaccination of wildlife against rabies: Differences among host species in vaccine uptake efficiency

Vaccine

Volumn 35, Issue 32, 2017, Pages 3938-3944

  Vos, Ad ^a   Freuling, Conrad M ^b   Hundt, Boris ^a   Kaiser, Christiane ^a   Nemitz, Sabine ^b   Neubert, Andreas ^a   Nolden, Tobias ^b,c   Teifke, Jens P ^b   te Kamp, Verena ^b   Ulrich, Reiner ^b   Finke, Stefan ^b   Müller, Thomas ^b  

^a IDT Biologika GmbH   (Germany)

^b FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^c ViraTherapeutics GmbH   (Austria)

Author keywords

Fox; Oral vaccination; Rabies; Skunk; Tonsil; Vaccine uptake efficiency; Wildlife

Indexed keywords

RABIES VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG MEGADOSE; DRUG UPTAKE; INFECTION PREVENTION; LOW DRUG DOSE; MEPHITIS MEPHITIS; NONHUMAN; PALATINE TONSIL; PRIORITY JOURNAL; RABIES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEROCONVERSION; SKUNK; VACCINATION; VACCINE IMMUNOGENICITY; VIRUS DETECTION; VULPES VULPES; ANIMAL; FOX; IMMUNOLOGY; ORAL DRUG ADMINISTRATION; RABIES VIRUS; VETERINARY;

ADMINISTRATION, ORAL; ANIMALS; FOXES; MEPHITIDAE; RABIES; RABIES VACCINES; RABIES VIRUS;

EID: 85020882853     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2017.06.022     Document Type: Article

References (71)

1. Steck, F., Wandeler, A., Bichsel, P., Capt, S., Hafliger, U., Schneider, L., Oral immunization of foxes against rabies. Laboratory and field studies. Comp Immunol Microbiol Infect Dis 5:1–3 (1982), 165–171.
2. Nyberg, M., Kulonen, K., Neuvonen, E., Ek-Kommonen, C., Nuorgam, M., Westerling, B., An Epidemic of sylvatic rabies in Finland – descriptive epidemiology and results of oral vaccination. Acta Vet Scand 33:1 (1992), 43–57.
3. Rupprecht, C.E., Wiktor, T.J., Johnston, D.H., Hamir, A.N., Dietzschold, B., Wunner, W.H., et al. Oral immunization and protection of raccoons (Procyon lotor) with a vaccinia-rabies glycoprotein recombinant virus vaccine. Proc Natl Acad Sci U S A Biol Sci 83 (1986), 7947–7950.
4. 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 25:4 (1989), 548–554.
5. Meehan, S.K., Rabies epizootic in coyotes combated with oral vaccination program. J Am Vet Med Assoc 206:8 (1995), 1097–1099.
6. Fearneyhough, M.G., Wilson, P.J., Clark, K.A., Smith, D.R., Johnston, D.H., Bradley, N., et al. Results of an oral rabies vaccination program for coyotes. J Am Vet Med Assoc 212:4 (1998), 498–502.
7. Sidwa, T.J., Wilson, P.J., Moore, G.M., Oertli, E.H., Hicks, B.N., Rohde, R.E., et al. Evaluation of oral rabies vaccination programs for control of rabies epizootics in coyotes and gray foxes: 1995–2003. J Am Vet Med Assoc 227:5 (2005), 785–792.
8. Rosatte, R.C., Power, M.J., MacInnes, C.D., Campbell, J.B., Trap-vaccinate-release and oral vaccination for rabies control in urban skunks, raccoons and foxes. J Wildl Dis 28:4 (1992), 562–571, 10.7589/0090-3558-28.4.562 PubMed PMID: 1474654.
9. Blanton, J.D., Meadows, A., Murphy, S., Manangan, J.S., Hanlon, C.A., Faber, M.L., et al. Vaccination of small asian mongoose (herpestes javanicus) against rabies. J Wildl Dis 42:3 (2006), 663–666.
10. Vos, A., Kretzschmar, A., Ortmann, S., Lojkic, I., Habla, C., Muller, T., et al. Oral vaccination of captive small Indian mongoose (Herpestes auropunctatus) against rabies. J Wildl Dis 49:4 (2013), 1033–1036, 10.7589/2013-02-035 Epub 2014/02/08. PubMed PMID: 24502736.
11. Haddad, N., Khelifa, R.B., Matter, H., Kharmachi, H., Aubert, M.F.A., Wandeler, A., et al. Assay of oral vaccination of dogs against rabies in Tunisia with the vaccinal strain Sad(Bern). Vaccine 12:4 (1994), 307–309.
12. Aylan O, Vos A. Efficacy studies with SAD B19 in Turkish dogs. J ETLIK Veterin Microbiol 1998;9(Special Issue Oral vaccination of dogs against rabies):93–102.
13. Rupprecht, C.E., Hanlon, C.A., Blanton, J.D., Manangan, J.S., Morrill, P., Murphy, S., et al. Oral vaccination of dogs with recombinant rabies virus vaccines. Virus Res 111:1 (2005), 101–105.
14. Brown, L.J., Rosatte, R.C., Fehlner-Gardiner, C., Ellison, J.A., Jackson, F.R., Bachmann, P., et al. Oral vaccination and protection of striped skunks (Mephitis mephitis) against rabies using ONRAB(R). Vaccine 32:29 (2014), 3675–3679, 10.1016/j.vaccine.2014.04.029 PubMed PMID: 24814554.
15. 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 123 (1992), 169–179.
16. Grosenbaugh, D.A., Maki, J.L., Rupprecht, C.R., Wall, D.K., Rabies challenge of captive striped skunks (mephitis mephitis) following oral administration of a live vaccinia-vectored rabies vaccine. J Wildl Dis 43:1 (2007), 124–128.
17. Rupprecht, C.E., Charlton, K.M., Artois, M., Casey, G.A., Webster, W.A., Campbell, J.B., et al. Ineffectiveness and comparative pathogenicity of attenuated rabies virus-vaccines for the striped skunk (mephitis-mephitis). J Wildl Dis 26:1 (1990), 99–102.
18. 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 52:1 (1988), 58–62.
19. Tolson, N.D., Charlton, K.M., Stewart, R.B., Casey, G.A., Webster, W.A., MacKenzie, K., et al. Mutants of rabies viruses in skunks: immune response and pathogenicity. Can J Vet Res 54:1 (1990), 178–183.
20. Vos, A., Pommerening, E., Neubert, L., Kachel, S., Neubert, A., Safety studies of the oral rabies vaccine SAD B19 in striped skunk (Mephitis mephitis). J Wildl Dis 38:2 (2002), 428–431.
21. Freuling, C., Hampson, K., Selhorst, T., Schröder, R., Meslin, F.X., Mettenleiter, T.C., et al. The elimination of fox rabies from Europe: determinants of success and lessons for the future. Philos Trans R Soc Lond B Biol Sci, 368, 2013.
22. Müller, T.F., Schroder, R., Wysocki, P., Mettenleiter, T.C., Freuling, C.M., Spatio-temporal use of oral rabies vaccines in fox rabies elimination programmes in Europe. PLOS Negl Trop Dis, 9(8), 2015, e0003953, 10.1371/journal.pntd.0003953 PubMed PMID: 26280895; PubMed Central PMCID: PMC4539187.
23. Fehlner-Gardiner, C., Rudd, R., Donovan, D., Slate, D., Kempf, L., Badcock, J., Comparing ONRAB(R) AND RABORAL V-RG(R) oral rabies vaccine field performance in raccoons and striped skunks, New Brunswick, Canada, and Maine, USA. J Wildl Dis 48:1 (2012), 157–167, 10.7589/0090-3558-48.1.157 Epub 2012/01/17. PubMed PMID: 22247384.
24. Mainguy, J., Fehlner-Gardiner, C., Slate, D., Rudd, R.J., Oral rabies vaccination in raccoons: comparison of ONRAB(R) and RABORAL V-RG(R) vaccine-bait field performance in Quebec, Canada and Vermont, USA. J Wildl Dis 49:1 (2013), 190–193, 10.7589/2011-11-342 Epub 2013/01/12. PubMed PMID: 23307388.
25. MacInnes, C.D., Smith, S.M., Tinline, R.R., Ayers, N.R., Bachmann, P., Ball, D.G., et al. Elimination of rabies from red foxes in eastern Ontario. J Wildl Dis 37:1 (2001), 119–132, 10.7589/0090-3558-37.1.119 PubMed PMID: 11272485.
26. 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 13:1 (2007), 25–27, 10.3201/eid1301.060622 Epub 2007/03/21. PubMed PMID: 17370512; PubMed Central PMCID: PMC2725809.
27. 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, 3(12), 2009, e549, 10.1371/journal.pntd.0000549 Epub 2009/12/23, PubMed PMID: 20027214; PubMed Central PMCID: PMC2791170.
28. 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 31:17 (2013), 2207–2213, 10.1016/j.vaccine.2013.02.057 Epub 2013/03/19, PubMed PMID: 23499602.
29. Kaden, V., Lange, E., Fischer, U., Strebelow, G., Oral immunisation of wild boar against classical swine fever: evaluation of the first field study in Germany. Vet Microbiol 73:2–3 (2000), 239–252 PubMed PMID: 10785331.
30. Romelt, M., Klingelhefer, I., Konig, A., Braun, B., Reiner, G., Classical swine fever in wild boar in rhineland-palatinate: evaluation of the official control measures from 2005–2011. Berl Munch Tierarztl Wochenschr 128:11–12 (2015), 507–516 PubMed PMID: 26697717.
31. Moennig, V., The control of classical swine fever in wild boar. Front Microbiol, 6, 2015, 1211, 10.3389/fmicb.2015.01211 PubMed PMID: 26594202; PubMed Central PMCID: PMC4635204.
32. von Ruden, S., Staubach, C., Kaden, V., Hess, R.G., Blicke, J., Kuhne, S., et al. Retrospective analysis of the oral immunisation of wild boar populations against classical swine fever virus (CSFV) in region Eifel of Rhineland-Palatinate. Vet Microbiol 132:1–2 (2008), 29–38, 10.1016/j.vetmic.2008.04.022 PubMed PMID: 18534790.
33. Rocke, T.E., Kingstad-Bakke, B., Berlier, W., Osorio, J.E., A recombinant raccoon poxvirus vaccine expressing both yersinia pestis F1 and truncated V antigens protects animals against lethal plague. Vaccines 2:4 (2014), 772–784, 10.3390/vaccines2040772 PubMed PMID: 26344891; PubMed Central PMCID: PMC4494250.
34. Rocke, T.E., Pussini, N., Smith, S.R., Williamson, J., Powell, B., Osorio, J.E., Consumption of baits containing raccoon pox-based plague vaccines protects black-tailed prairie dogs (Cynomys ludovicianus). Vector Borne Zoonotic Dis 10:1 (2010), 53–58, 10.1089/vbz.2009.0050 PubMed PMID: 20158332.
35. Mencher, J.S., Smith, S.R., Powell, T.D., Stinchcomb, D.T., Osorio, J.E., Rocke, T.E., Protection of black-tailed prairie dogs (Cynomys ludovicianus) against plague after voluntary consumption of baits containing recombinant raccoon poxvirus vaccine. Infect Immun 72:9 (2004), 5502–5505, 10.1128/IAI.72.9.5502-5505.2004 PubMed PMID: 15322054; PubMed Central PMCID: PMC517477.
36. Baer, G.M., Broderson, J.R., Yager, P.A., Determination of the site of oral rabies vaccination. Am J Epidemiol 101:2 (1975), 160–164.
37. Rupprecht, C.E., Hamir, A.N., Johnston, D.H., Koprowski, H., Efficacy of a vaccinia-rabies glycoprotein recombinant virus vaccine in raccoons (procyon lotor). Rev Infect Dis 10:4 (1988), 803–809.
38. Thomas, I., Brochier, B., Languet, B., Blancou, J., Peharpe, D., Kieny, M.P., et al. Primary multiplication site of the vaccinia - rabies glycoprotein recombinant virus administered to foxes by the oral route. J Gen Virol 71 (1990), 37–42.
39. Orciari, L.A., Niezgoda, M., Hanlon, C.A., Shaddock, J.H., Sanderlin, D.W., Yager, P.A., et al. Rapid clearance of SAG-2 rabies virus from dogs after oral vaccination. Vaccine 19:31 (2001), 4511–4518.
40. Vos, A., Neubert, A., Aylan, O., Schuster, P., Pommerening, E., Müller, T., et al. An update on safety studies of SAD B 19 rabies virus vaccine in target and non-target species. Epidemiol Infect 123:1 (1999), 165–175.
41. Zhou, M., Wang, L., Zhou, S., Wang, Z., Ruan, J., Tang, L., et al. Recombinant rabies virus expressing dog GM-CSF is an efficacious oral rabies vaccine for dogs. Oncotarget. 6:36 (2015), 38504–38516, 10.18632/oncotarget.5904 PubMed PMID: 26436700.
42. Koenig, P., Hoffmann, B., Depner, K.R., Reimann, I., Teifke, J.P., Beer, M., Detection of classical swine fever vaccine virus in blood and tissue samples of pigs vaccinated either with a conventional C-strain vaccine or a modified live marker vaccine. Vet Microbiol 120:3–4 (2007), 343–351, 10.1016/j.vetmic.2006.10.034 PubMed PMID: 17147979.
43. Tignon, M., Kulcsar, G., Haegeman, A., Barna, T., Fabian, K., Levai, R., et al. Classical swine fever: comparison of oronasal immunisation with CP7E2alf marker and C-strain vaccines in domestic pigs. Vet Microbiol 142:1–2 (2010), 59–68, 10.1016/j.vetmic.2009.09.044 PubMed PMID: 19857935.
44. Drager, C., Petrov, A., Beer, M., Teifke, J.P., Blome, S., Classical swine fever virus marker vaccine strain CP7_E2alf: Shedding and dissemination studies in boars. Vaccine 33:27 (2015), 3100–3103, 10.1016/j.vaccine.2015.04.103 PubMed PMID: 25980427.
45. Zimmermann, G., Über den Waldeyer'schen lymphatischen Rachenring. Arch Wiss Prakt Tierheilk, 67(141–153), 1934.
46. Vollmerhaus, B., Zur vergleichenden Nomenklatur des lymphoepithelialen Rachenringes der Haussäugetiere und des Menschen. Zbl Vet Med 6 (1959), 82–89.
47. Graff, S., Descriptive anatomy of the pharyngeal tonsil and its place in Waldemyer's fauces. Anat Anz. 100:8–10 (1954), 120–133 PubMed PMID: 13148631.
48. Schummer, A., Wilkens, H., Vollmerhaus, B., Habermehl, K.H., The circulatory system, the skin, and the cutaneous organs of the domestic mammals. 1981, Springer, US.
49. Faber, M., Pulmanausahakul, R., Hodawadekar, S.S., Spitsin, S., McGettigan, J.P., Schnell, M.J., et al. Overexpression of the rabies virus glycoprotein results in enhancement of apoptosis and antiviral immune response. J Virol 76:7 (2002), 3374–3381 PubMed PMID: 11884563; PubMed Central PMCID: PMC136034.
50. Faber, M., Bette, M., Preuss, M.A.R., Pulmanausahakul, R., Rehnelt, J., Schnell, M.J., et al. Overexpression of tumor necrosis factor alpha by a recombinant rabies virus attenuates replication in neurons and prevents lethal infection in mice. J Virol 79:24 (2005), 15405–15416, 10.1128/Jvi.79.24.15405-15416.2005 PubMed PMID: WOS:000234276700042.
51. Vos A, Neumann G, Hundt B, Neubert A. Attenuated vaccines for veterinary use. In: Rupprecht CE, Nagarajan T, editors. Current laboratory techniques in rabies diagnosis, research and prevention, vol. 1. San Diego: Elsevier Academic Press; 2015. p. 237–44.
52. Neubert, A., Schuster, P., Muller, T., Vos, A., Pommerening, E., Immunogenicity and efficacy of the oral rabies vaccine SAD B19 in foxes. J Veter Med Ser B-Infect Dis Veterin Public Health 48:3 (2001), 179–183.
53. Dean, D.J., Abelseth, M.K., Athanasiu, P., The fluorescence antibody test. Meslin, F.X., Kaplan, M.M., Koprowski, H., (eds.) Laboratory techniques in rabies, 4th ed., 1996, World Health Organization, Geneva, 88–93.
54. Hoffmann, B., Freuling, C.M., Wakeley, P.R., Rasmussen, T.B., Leech, S., Fooks, A.R., et al. Improved safety for molecular diagnosis of classical rabies Viruses by use of a TaqMan real-time reverse transcription-PCR “Double Check” Strategy. J Clin Microbiol 48:11 (2010), 3970–3978, 10.1128/Jcm.00612-10 PubMed PMID: ISI:000283588500021.
55. Webster, W.A., A tissue culture infection test in routine rabies diagnosis. Can J Vet Res 51 (1987), 367–369.
56. Webster, W.A., Casey, G.A., Virus isolation in neuroblastoma cell culture. Meslin, F.X., Kaplan, M.M., Koprowski, H., (eds.) Laboratory techniques in rabies, 4th ed., 1996, World Health Organization, Geneva, 93–104.
57. Smith, J.S., Yager, P.A., Baer, G.M., A rapid reproducible test for determining rabies neutralizing antibody. Bull World Health Organ 48 (1973), 535–541.
58. Cox, J.H., Schneider, L.G., Prophylactic immunization of humans against rabies by intradermal inoculation of human diploid cell culture vaccine. J Clin Microbiol 3:2 (1976), 96–101.
59. Schneider, C.A., Rasband, W.S., Eliceiri, K.W., NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:7 (2012), 671–675 PubMed PMID: 22930834.
60. Blanton, J.D., Self, J., Niezgoda, M., Faber, M.L., Dietzschold, B., Rupprecht, C., Oral vaccination of raccoons (Procyon lotor) with genetically modified rabies virus vaccines. Vaccine 25:42 (2007), 7296–7300.
61. 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 27:51 (2009), 7194–7197, 10.1016/j.vaccine.2009.09.030 PubMed PMID: 19925952.
62. Cliquet, F., Guiot, A.L., Munier, M., Bailly, J., Rupprecht, C.E., Barrat, J., Safety and efficacy of the oral rabies vaccine SAG2 in raccoon dogs. Vaccine 24:20 (2006), 4386–4392.
63. Schuster, P., Müller, T., Vos, A., Selhorst, T., Neubert, L., Pommerening, E., Comparative immunogenicity and efficacy studies with oral rabies virus vaccine SAD P5/88 in raccoon dogs and red foxes. Acta Vet Hung 49:3 (2001), 285–290.
64. Wright, N., Jackson, F.R., Niezgoda, M., Ellison, J.A., Rupprecht, C.E., Nel, L.H., High prevalence of antibodies against canine adenovirus (CAV) type 2 in domestic dog populations in South Africa precludes the use of CAV-based recombinant rabies vaccines. Vaccine 31:38 (2013), 4177–4182, 10.1016/j.vaccine.2013.06.089 Epub 2013 Jul 16.
65. Rosatte, R.C., Howard, D.R., Campbell, J.B., MacInnes, C.D., Intramuscular vaccination of skunks and raccoons against rabies. J Wildl Dis 26:2 (1990), 225–230.
66. Nittayananta, W., Transmission of HIV-1 via oral route: why is it difficult?. J Dent Assoc Thai 59:4 (2009), 201–212.
67. Kraan, H., Vrieling, H., Czerkinsky, C., Jiskoot, W., Kersten, G., Amorij, J.P., Buccal and sublingual vaccine delivery. J Control Release: Off J Control Release Soc 190 (2014), 580–592, 10.1016/j.jconrel.2014.05.060 PubMed PMID: 24911355.
68. Casteleyn, C., Breugelmans, S., Simoens, P., Van den Broeck, W., The tonsils revisited: review of the anatomical localization and histological characteristics of the tonsils of domestic and laboratory animals. Clin Dev Immunol, 2011, 2011, 472460, 10.1155/2011/472460 PubMed PMID: 21869895; PubMed Central PMCID: PMC3159307.
69. Cho, K.A., Kim, J.Y., Kim, H.S., Ryu, K.H., Woo, S.Y., Tonsil-derived mesenchymal progenitor cells acquire a follicular dendritic cell phenotype under cytokine stimulation. Cytokine 59:2 (2012), 211–214, 10.1016/j.cyto.2012.04.016 PubMed PMID: 22578801.
70. Bernstein, J.M., Yamanaka, N., Nadal, D., Immunology of the tonsils and adenoids. Ogra, P.L., Mestecky, J., Lamm, M.E., Strober, W., McGhee, J.R., Bienenstock, J., (eds.) Handbook of mucosal immunology, 1994, Academic Press Inc., San Diego, 625–640.
71. Zhou, M., Zhang, G., Ren, G., Gnanadurai, C.W., Li, Z., Chai, Q., et al. Recombinant rabies viruses expressing GM-CSF or flagellin are effective vaccines for both intramuscular and oral immunizations. PLoS ONE, 8(5), 2013, e63384, 10.1371/journal.pone.0063384 PubMed PMID: 23700422; PubMed Central PMCID: PMC3658976.