Ovine Progressive Pneumonia Virus Is Transmitted More Effectively via Aerosol Nebulization than Oral Administration

Abstract

A new method of experimental infection of ovine progressive pneumonia virus (OPPV), aerosol nebulization (Nb), was compared to intravenous (IV) and oral (PO) methods of experimental infection. Seven month old lambs were given 3.5 × 107 TCID50 of Dubois OPPV LMH19 isolate using IV, PO, or Nb methods and were monitored for infection using cELISA and OPPV quantitative (q) PCR for 35 weeks. Four out of four sheep in the IV group, six out of six sheep in the Nb group, but only two out of six sheep in the PO group became infected by OPPV; whereas the uninoculated controls (n = 2) and a sentinel control (n = 1) remained uninfected during the course of the study. The time to a cELISA or OPPV qPCR positive result in the Nb group was quicker and statistically different from the time to a cELISA or OPPV qPCR positive result in the PO group (cELISA P value = 0.0021 and OPPV qPCR P value = 0.0007). When the Nb and IV groups were compared, sheep became cELISA and OPPV qPCR positive at similar times (cELISA P value = 0.6 and OPPV qPCR P value = 0.1). In addition, sheep became OPPV qPCR positive prior to cELISA in both the IV and Nb groups (IV P value = 0.027 and Nb P value = 0.007). Aerosol nebulization is a more natural experimental method of transmitting OPPV and may be valuable for testing potential vaccines or specific host genetics.

Share and Cite:

M. Herrmann-Hoesing, L. , N. White, S. , E. Broughton-Neiswanger, L. , C. Johnson, W. , M. Noh, S. , A. Schneider, D. , Li, H. , S. Taus, N. , Reynolds, J. , Truscott, T. , P. Dassanayake, R. and P. Knowles, D. (2012) Ovine Progressive Pneumonia Virus Is Transmitted More Effectively via Aerosol Nebulization than Oral Administration. Open Journal of Veterinary Medicine, 2, 113-119. doi: 10.4236/ojvm.2012.23019.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] D. De Andres, D. Klein, N. J. Watt, E. Barriatua, S. Torsteinsdottir, B. A. Blacklaws and G. D. Harkiss, “Diagnostic Tests for Small Ruminant Lentiviruses,” Vet Microbiol, Vol. 107, No. 1-2, 2005, pp. 49-62. doi:10.1016/j.vetmic.2005.01.012
[2] M. Pepin, C. Vitu, P. Russo, J. F. Mornex and E. Peterhans, “Maedi-Visna Virus Infection in Sheep: A Review,” Vet Res, Vol. 29, No. 3-4, 1998, pp. 341-367.
[3] L.M. Herrmann-Hoesing, “Diagnostic assays used to control small ruminant lentiviruses,” J Vet Diagn Invest, Vol. 22, No. 6, 2010, pp. 843-855. doi:10.1177/104063871002200602
[4] G.F. De Boer, C. Terpstra, D.J. Houwers, and J. Hendriks, “Studies in epidemiology of maedi/visna in sheep,” Res Vet Sci, Vol. 26, No. 2, 1979, pp. 202-208.
[5] D.J. Houwers, C.D. Konig, G.F. De Boer, and J. Schaake, “Maedi-visna control in sheep. I. Artificial rearing of colostrum-deprived lambs,” Vet Microbiol, Vol. 8, No. 2, 1983, pp. 179-185. doi:10.1016/0378-1135(83)90064-0
[6] R.C. Cutlip, H.D. Lehmkuhl, and T.A. Jackson, “Intrauterine transmission of ovine progressive pneumonia virus,” Am J Vet Res, Vol. 42, No. 10, 1981, pp. 1795-1797.
[7] I. Leginagoikoa, R.A. Juste, J. Barandika, B. Amorena, D. De Andres D, L. Lujan, J. Badiola, and E. Berriatua, “Extensive rearing hinders Maedi-Visna Virus (MVV) infection in sheep,” Vet Res, Vol. 37, No. 6, 2006, pp. 767-78. doi:10.1051/vetres:2006034
[8] I. Leginagoikoa, E. Minguijon, R.A. Juste, J. Barandika, B. Amorena, D. de Andres, J.J. Badiola, L. Lujan, and E. Berriatua, “Effects of housing on the incidence of visna/maedi virus infection in sheep flocks,” Res Vet Sci, Vol. 88, No. 3, 2010, pp. 415-421. doi:10.1016/j.rvsc.2009.11.006
[9] L.E. Broughton-Neiswanger, S.N. White, D.P. Knowles, M.R. Mousel, G.S. Lewis, D.R. Herndon, and L.M. Herrmann-Hoesing, “Non-maternal transmission is the major mode of ovine lentivirus transmission in a ewe flock: a molecular epidemiology study,” Infect Genet Evol, Vol. 10, No. 7, 2010, pp. 998-1007. doi:10.1016/j.meegid.2010.06.007
[10] D.S. Adams, P. Klevjer-Anderson, J.L. Carlson, T.C. McGuire, and J.R. Gorham, “Transmission and control of caprine arthritis-encephalitis virus,” Am J Vet Res, Vol. 44, No. 9, 1983, pp. 1670-1675.
[11] V. Alvarez, J. Arranz, M. Daltabuit-Test, I. Leginagoikoa, R.A. Juste, B. Amorena, D. de Andres, L.Lujan, J.J. Badiola, and E. Berriatua, “Relative contribution of colostrum from Maedi-Visna virus (MVV) infected ewes to MVV-seroprevalence in lambs,” Res Vet Sci, Vol. 78, No. 3, 2005, pp. 237-243. doi:10.1016/j.rvsc.2004.09.006
[12] S.J. Brodie, L.D. Pearson, M.C. Zink, H.M. Bickle, B.C. Anderson, K.A. Marcom, and J.C. DeMartini, “Ovine lentivirus expression and disease. Virus replication, but not entry, is restricted to macrophages of specific tissues,” Am J Pathol, Vol. 146, No. 1, 1995, pp. 250-263.
[13] L.M. Herrmann-Hoesing, G.H. Palmer and D.P. Knowles, “Evidence of proviral clearance following postpartum transmission of an ovine lentivirus,” Virology, Vol. 362, No. 1, 2007, pp. 226-234. doi:10.1016/j.virol.2006.12.021
[14] C. Lerondelle and R. Ouzrout, “Expression of maedi-visna virus in mammary secretions of a seropositive ewe,” Dev Biol Stand, Vol. 72, 1990, pp. 223-227.
[15] L. Lujan, I. Begara, D. Collie, N.J. Watt, “Ovine lentivirus (maedi-visna virus) protein expression in sheep alveolar macrophages,” Vet Pathol, Vol. 31, No. 6, 1994, pp. 695-703. doi:10.1177/030098589403100610
[16] T.N. McNeilly, A. Baker, J.K. Brown, D. Collie, G. Maclachlan, S.M. Rhind, and G.D. Harkiss, “Role of alveolar macrophages in respiratory transmission of visna/maedi virus,” J Virol, Vol. 82, No. 3, 2008, pp. 1526-1536. doi:10.1128/JVI.02148-07
[17] H.E. Gendelman, O. Narayan, S. Kennedy-Stoskopf, P.G. Kennedy, Z. Ghotbi, J.E. Clements, J. Stanley, and G. Pezeshkpour, “Tropism of sheep lentiviruses for monocytes: susceptibility to infection and virus gene expression increase during maturation of monocytes to macrophages,” J Virol, Vol. 58, No. 1, 1986, pp. 67-74.
[18] M.D. Gorrell, M.R. Brandon, D. Sheffer, R.J. Adams and O. Narayan, “Ovine lentivirus is macrophagetropic and does not replicate productively in T lymphocytes,” J Virol, Vol. 66, No. 5, 1992, pp. 2679-2688.
[19] A. De la Concha-Bermejillo, S. Magnus-Corral, S.J. Brodie, and J.C. De Martini, “Venereal shedding of ovine lentivirus in infected rams, “Am J Vet Res, Vol. 57, No. 5, 1996, pp. 684-688.
[20] K. Peterson, J. Brinkhof, D.J. Houwers, B. Colenbrander, B.M. Gadella, “Presence of pro-lentiviral DNA in male sexual organs and ejaculates of small ruminants,” Theriogenology, Vol. 69, No. 4, 2008, pp. 433-442. doi:10.1016/j.theriogenology.2007.10.013
[21] I. Begara, L. Lujan, D.D. Collie, H.R. Miller and N.J. Watt, “Early pulmonary cell response during experimental maedi-visna virus infection,” Vet Immunol Immunopathol, Vol. 55, No. 1-3, 1996, pp. 115-126. doi:10.1016/S0165-2427(96)05623-1
[22] J.L. Cadore, F. Guiguen, G. Cordier, R. Loire, M. Lyon, J. Chastang, T. Greenland, I. Court-Fortune, D. Revel, and J. F. Mornex, “Early events in the experimental interstitial lung disease induced in sheep by the Visna-maedi virus,” Immunol Lett, Vol. 39, No. 1, 1993, pp. 39-43. doi:10.1016/0165-2478(93)90162-U
[23] P. Deng, R.C. Cutlip, H.D. Lehmkuhl, and K.A. Brogden, “Ultrastructure and frequency of mastitis caused by ovine progressive pneumonia virus infection in sheep,” Vet Pathol, Vol 23, No. 2, 1986, pp. 184-189. doi:10.1177/030098588602300212
[24] M. Gudnadottir and P.A. Palsson, “Successful transmission of visna by intrapulmonary inoculation,” J Infect Dis, Vol. 115, 1965, pp. 217-225. doi:10.1093/infdis/115.3.217
[25] T.N. McNeilly, P. Tennant, L. Lujan, M. Perez, and G.D. Harkiss, “Differential infection efficiencies of peripheral lung and tracheal tissues in sheep infected with Visna/maedi virus via the respiratory tract,” J Gen Virol, Vol. 88, Pt. 2, 2007, pp. 670-679. doi:10.1099/vir.0.82434-0
[26] S. Preziuso, E. Taccini, G. Rossi, G. Renzoni, and G. Braca, “Experimental Maedi Visna Virus Infection in sheep: a morphological, immunohistochemical and PCR study after three years of infection,” Eur J Histochem, Vol. 47, No. 4, 2003, pp. 373-378.
[27] B. Sigurdsson, P.A. Palsson, and A. Tryggvaddottir, “Transmission experiments with maedi,” J Infect Dis, Vol. 93, No. 2, 1953, pp. 166-175. doi:10.1093/infdis/93.2.166
[28] S. Torsteinsdottir, S. Matthiasdottir, N. Vidarsdottir, V. Svansson, and G. Petursson, “Intratracheal inoculation as an efficient route of experimental infection with maedi-visna virus,” Res Vet Sci, Vol. 75, No. 3, 2003, pp. 245-247. doi:10.1016/S0034-5288(03)00098-5
[29] L.M. Herrmann-Hoesing, H.D. Lehmkuhl and R.C. Cutlip, “Minimum intravenous infectious dose of ovine progressive pneumonia virus (OPPV),” Res Vet Sci, Vol. 87, No. 2, 2009, pp. 329-331. doi:10.1016/j.rvsc.2009.01.006
[30] S. Preziuso, G. Renzoni, T.E. Allen, E. Taccini, G. Rossi, J.C. DeMartini and G. Braca, “Colostral transmission of maedi visna virus: sites of viral entry in lambs born from experimentally infected ewes,” Vet Microbiol, Vol. 104, No. 3-4, 2004, pp.157-164. doi:10.1016/j.vetmic.2004.09.010
[31] I.A. Schipper, A. Misek, L. Ludemann, M. Light, and W. Limesand, “Ovine progressive pneumonia infection via the oral route,” Veterinary Medicine, Small Animal Clinician, Vol. 78, 1983, pp. 417-417.
[32] P. Klevjer-Anderson and W.P. Cheevers, “Characterization of the infection of caprine synovial membrane cells by the retrovirus caprine arthritis-encephalitis virus,” Virology, Vol. 110, No. 1, 1981, pp. 113-119. doi:10.1016/0042-6822(81)90012-X
[33] N.S. Taus, D.L. Traul, J.L. Oaks, T.B. Crawford, G.S. Lewis, and H. Li, “Experimental infection of sheep with ovine herpesvirus 2 via aerosolization of nasal secretions,” J Gen Virol, Vol. 86, Pt. 3, 2005, pp. 575-579. doi:10.1099/vir.0.80707-0
[34] L.M. Herrmann, W.P. Cheevers, K.L. Marshall, T.C. McGuire, M.M. Hutton, G.S. Lewis, D.P. Knowles, “Detection of serum antibodies to ovine progressive pneumonia virus in sheep by using a caprine arthritis-encephalitis virus competitive-inhibition enzyme-linked immunosorbent assay,” Clin Diagn Lab Immunol, Vol. 10, No. 5, 2003, pp. 862-865.
[35] L.M. Herrmann-Hoesing, S.N. White, G.S. Lewis, M.R. Mousel, D.P. Knowles, “Development and validation of an ovine progressive pneumonia virus quantitative PCR,” Clin Vac Immunol, Vol. 14, No. 10, 2007, pp. 1274-1278. doi:10.1128/CVI.00095-07
[36] D.K. Myers-Evert and L.M. Herrmann-Hoesing, “Ovine progressive pneumonia virus capsid is B-cell immunodominant using Western blot analysis: a comparison of sensitivity between Western blot analysis and immunoprecipitation,” J Virol Methods, Vol. 137, No. 2, 2006, pp. 339-342. doi:10.1016/j.jviromet.2006.06.025
[37] H.J. Larsen, B. Hyllseth, and J. Krogsrud, “Experimental maedi virus infection in sheep: Cellular and humoral immune response during three years following intranasal inoculation,” Am J Vet Res, Vol. 43, No. 3, 1982, pp. 384-389.
[38] S. Ryan, L. Tiley, I. McConnell, and B. Blacklaws, “Infection of dendritic cells by the Maedi-Visna lentivirus,” J Virol, Vol. 74, No. 21, 2000, pp. 10096-10103. doi:10.1128/JVI.74.21.10096-10103.2000
[39] N.S. Taus, D.A. Schneider, J. L. Oaks, H. Yan, K.L. Gailbreath, D.K. Knowles, H. Li, “Sheep (Ovis aries) airway epithelial cells support ovine herpesvirus 2 lytic replication in vivo,” Vet Microbiol, Vol. 145, No. 1-2, 2010, pp. 47-53. doi:10.1016/j.vetmic.2010.03.013
[40] S.G. Campbell, M.J. Siegel, and B.J. Knowlton, “Sheep immunoglobulins and their transmission to the neonatal lamb,” N Z Vet J, Vol. 25, No. 12, 1977, pp. 361-365. doi:10.1080/00480169.1977.34458
[41] R. Halliday, “The transfer of antibodies from ewes to their lambs,” J Immunol, Vol. 95, No. 3, 1965, pp. 510-516.
[42] K.L. Schnorr and L.D. Pearson, “Intestinal absorption of maternal leucocytes by newborn lambs,” J Reprod Immunol, Vol. 6, No. 5, 1984, pp. 329-337. doi:10.1016/0165-0378(84)90031-7
[43] N.E. East, J.D. Rowe, J.E. Dahlberg, G.H. Theilen, and N.C. Pedersen NC, “Modes of transmission of caprine arthritis-encephalitis virus infection,” Small Rum Res, Vol. 10, 1993, pp. 251-262. doi:10.1016/0921-4488(93)90130-A
[44] W.P. Cheevers, D.P. Knowles, T.C. McGuire, D.R. Cunningham, D.S. Adams, and J.R. Gorham, “Chronic disease in goats orally infected with two isolates of the caprine arthritis-encephalitis lentivirus,” Lab Invest, Vol. 58, No. 5, 1988, pp. 510-517.

Journals Menu
Follow SCIRP
Contact us
+1 323-425-8868
customer@scirp.org
WhatsApp +86 18163351462(WhatsApp)
Click here to send a message to me 1655362766
Paper Publishing WeChat

Copyright © 2024 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.

  翻译：