Skip to main content
Springer Nature - PMC COVID-19 Collection logoLink to Springer Nature - PMC COVID-19 Collection
. 2009;330:73–87. doi: 10.1007/978-3-540-70617-5_4

Ferrets as a Model for Morbillivirus Pathogenesis, Complications, and Vaccines

S Pillet , N Svitek , V von Messling ‡,
Editors: Diane E Griffin*, Michael B A Oldstone6
PMCID: PMC7121116  PMID: 19203105

Abstract

The ferret is a standard laboratory animal that can be accommodated in most animal facilities. While not susceptible to measles, ferrets are a natural host of canine distemper virus (CDV), the closely related carnivore morbillivirus. CDV infection in ferrets reproduces all clinical signs associated with measles in humans, including the typical rash, fever, general immunosuppression, gastrointestinal and respiratory involvement, and neurological complications. Due to this similarity, experimental CDV infection of ferrets is frequently used to assess the efficacy of novel vaccines, and to characterize pathogenesis mechanisms. In addition, direct intracranial inoculation of measles isolates from subacute sclerosing panencephali-tis (SSPE) patients results in an SSPE-like disease in animals that survive the acute phase. Since the advent of reverse genetics systems that allow the targeted manipulation of viral genomes, the model has been used to evaluate the contribution of the accessory proteins C and V, and signalling lymphocyte activation molecule (SLAM)-binding to immunosuppression and overall pathogenesis. Similarly produced green fluorescent protein-expressing derivatives that maintain parental virulence have been instrumental in the direct visualization of systemic dissemination and neuroinvasion. As more immunological tools become available for this model, its contribution to our understanding of morbillivirus—host interactions is expected to increase.

Keywords: Measle Virus, Canine Distemper Virus, Maternal Antibody, Measle Vaccine, Subacute Sclerosing Panencephalitis

Contributor Information

Diane E. Griffin, Email: dgriffin@mail.jhmi.edu, Email: dgriffin@jhsph.edu

Michael B. A. Oldstone, Email: mbaobo@scripps.edu

V. von Messling, Email: veronika.vonmessling@iaf.inrs.ca

References

  1. Alldinger S, Wunschmann A, Baumgartner W, Voss C, Kremmer E. Up-regulation of major histocompatibility complex class II antigen expression in the central nervous system of dogs with spontaneous canine distemper virus encephalitis. Acta Neuropathol. 1996;92:273–280. doi: 10.1007/s004010050518. [DOI] [PubMed] [Google Scholar]
  2. Appel MJ, Harris WV. Antibody titers in domestic ferret jills and their kits to canine distemper virus vaccine. J Am Vet Med Assoc. 1988;193:332–333. [PubMed] [Google Scholar]
  3. Appel MJ, Shek WR, Summers BA. Lymphocyte-mediated immune cytotoxicity in dogs infected with virulent canine distemper virus. Infect Immun. 1982;37:592–600. doi: 10.1128/iai.37.2.592-600.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Appel MJ, Shek WR, Shesberadaran H, Norrby E. Measles virus and inactivated canine distemper virus induce incomplete immunity to canine distemper. Arch Virol. 1984;82:73–82. doi: 10.1007/BF01309369. [DOI] [PubMed] [Google Scholar]
  5. Appel MJ, Summers BA. Pathogenicity of morbilliviruses for terrestrial carnivores. Vet Microbiol. 1995;44:187–191. doi: 10.1016/0378-1135(95)00011-X. [DOI] [PubMed] [Google Scholar]
  6. Atabani SF, Byrnes AA, Jaye A, Kidd IM, Kidd xAF, Whittle H, Karp CL. Natural measles causes prolonged suppression of interleukin-12 production. J Infect Dis. 2001;184:1–9. doi: 10.1086/321009. [DOI] [PubMed] [Google Scholar]
  7. Axthelm MK, Krakowka S. Canine distemper virus: the early blood-brain barrier lesion. Acta Neuropathol. 1987;75:27–33. doi: 10.1007/BF00686789. [DOI] [PubMed] [Google Scholar]
  8. Bonami F, Rudd PA, von Messling V. Disease duration determines canine distemper virus neurovirulence. J Virol. 2007;81:12066–12070. doi: 10.1128/JVI.00818-07. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brown HR, Thormar H, Barshatzky M, Wisniewski HM. Localization of measles virus antigens in subacute sclerosing panencephalitis in ferrets. Lab Anim Sci. 1985;35:233–237. [PubMed] [Google Scholar]
  10. Bush M, Montali RJ, Brownstein D, James AE, Jr, Appel MJ. Vaccine-induced canine distemper in a lesser panda. J Am Vet Med Assoc. 1976;169:959–960. [PubMed] [Google Scholar]
  11. Cabasso VJ, Stebbins MR, Cox HR. Active immunization of ferrets by simultaneous injections of avianized canine distemper vaccine and anticanine distemper hyperimmune serum. Cornell Vet. 1953;43:179–183. [PubMed] [Google Scholar]
  12. Carpenter JW, Appel MJ, Erickson RC, Novilla MN. Fatal vaccine-induced canine distemper virus infection in black-footed ferrets. J Am Vet Med Assoc. 1976;169:961–964. [PubMed] [Google Scholar]
  13. Chalmers WS, Baxendale W. A comparison of canine distemper vaccine and measles vaccine for the prevention of canine distemper in young puppies. Vet Rec. 1994;135:349–353. doi: 10.1136/vr.135.15.349. [DOI] [PubMed] [Google Scholar]
  14. Cherpillod P, Tipold A, Griot-Wenk M, Cardozo C, Schmid I, Fatzer R, Schobesberger M, Zurbriggen R, Bruckner L, Roch F, et al. DNA vaccine encoding nucleocapsid and surface proteins of wild type canine distemper virus protects its natural host against distemper. Vaccine. 2000;18:2927–2936. doi: 10.1016/S0264-410X(00)00119-5. [DOI] [PubMed] [Google Scholar]
  15. Confer AW, Kahn DE, Koestner A, Krakowka S. Biological properties of a canine distemper virus isolate associated with demyelinating encephalomyelitis. Infect Immun. 1975;11:835–844. doi: 10.1128/iai.11.4.835-844.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dahl L, Jensen TH, Gottschalck E, Karlskov-Mortensen P, Jensen TD, Nielsen L, Andersen MK, Buckland R, Wild TF, Blixenkrone-Moller M. Immunization with plasmid DNA encoding the hemagglutinin and the nucleoprotein confers robust protection against a lethal canine distemper virus challenge. Vaccine. 2004;22:3642–3648. doi: 10.1016/j.vaccine.2004.03.016. [DOI] [PubMed] [Google Scholar]
  17. Danesh A, Seneviratne C, Cameron CM, Banner D, Devries ME, Kelvin AA, Xu L, Ran L, Bosinger SE, Rowe T, et al. Cloning, expression and characterization of ferret CXCL10. Mol Immunol. 2008;45:1288–1297. doi: 10.1016/j.molimm.2007.09.018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Devaux P, von Messling V, Songsungthong W, Springfeld C, Cattaneo R. Tyrosine 110 in the measles virus phosphoprotein is required to block STAT1 phosphorylation. Virology. 2007;360:72–83. doi: 10.1016/j.virol.2006.09.049. [DOI] [PubMed] [Google Scholar]
  19. Dorries R, ter Meulen V. Detection and identification of virus-specific, oligoclonal IgG in unconcentrated cerebrospinal fluid by immunoblot technique. J Neuroimmunol. 1984;7:77–89. doi: 10.1016/S0165-5728(84)80008-9. [DOI] [PubMed] [Google Scholar]
  20. Ek-Kommonen C, Rudback E, Anttila M, Aho M, Huovilainen A. Canine distemper of vaccine origin in European mink, Mustela lutreola — a case report. Vet Microbiol. 2003;92:289–293. doi: 10.1016/S0378-1135(02)00361-9. [DOI] [PubMed] [Google Scholar]
  21. Fischer L, Tronel JP, Pardo-David C, Tanner P, Colombet G, Minke J, Audonnet JC. Vaccination of puppies born to immune dams with a canine adenovirus-based vaccine protects against a canine distemper virus challenge. Vaccine. 2002;20:3485–3497. doi: 10.1016/S0264-410X(02)00344-4. [DOI] [PubMed] [Google Scholar]
  22. Fischer L, Tronel JP, Minke J, Barzu S, Baudu P, Audonnet JC. Vaccination of puppies with a lipid-formulated plasmid vaccine protects against a severe canine distemper virus challenge. Vaccine. 2003;21:1099–1102. doi: 10.1016/S0264-410X(02)00608-4. [DOI] [PubMed] [Google Scholar]
  23. Fontana JM, Bankamp B, Bellini WJ, Rota PA. Regulation of interferon signaling by the C and V proteins from attenuated and wild-type strains of measles virus. Virology. 2008;374:71–81. doi: 10.1016/j.virol.2007.12.031. [DOI] [PubMed] [Google Scholar]
  24. Fox JG. Biology and diseases of the ferret. New York: Wiley-Blackwell; 1998. [Google Scholar]
  25. Gans HA, Arvin AM, Galinus J, Logan L, De Hovitz R, Maldonado Y. Deficiency of the humoral immune response to measles vaccine in infants immunized at age 6 months. JAMA. 1998;280:527–532. doi: 10.1001/jama.280.6.527. [DOI] [PubMed] [Google Scholar]
  26. Gill JM, Hartley WJ, Hodgkinson NL. An outbreak of post-vaccinal suspected distemperlike encephalitis in farmed ferrets ( Mustela putorius furo) NZ Vet J. 1988;36:173–176. doi: 10.1080/00480169.1988.35525. [DOI] [PubMed] [Google Scholar]
  27. Gillespie JH, Rickard CG. Encephalitis in dogs produced by distemper virus. Am J Vet Res. 1956;17:103–108. [PubMed] [Google Scholar]
  28. Gorham JR, Leader RW, Gutierrez JC. Distemper immunization of ferrets by nebulization with egg adapted virus. Science. 1954;119:125–126. doi: 10.1126/science.119.3082.125. [DOI] [PubMed] [Google Scholar]
  29. Greenacre CB. J Am Vet Med Assoc 223:663 – 665 virology. 5 th edn. Philadelphia: Lippincott Williams Wilkins; 2003. Incidence of adverse events in ferrets vaccinated with distemper or rabies vaccine: 143 cases (1995 – 2001) pp. 1550–1585. [DOI] [PubMed] [Google Scholar]
  30. Griot C, Moser C, Cherpillod P, Bruckner L, Wittek R, Zurbriggen A, Zurbriggen R. Early DNA vaccination of puppies against canine distemper in the presence of maternally derived immunity. Vaccine. 2004;22:650–654. doi: 10.1016/j.vaccine.2003.08.022. [DOI] [PubMed] [Google Scholar]
  31. Hoover JP, Baldwin CA, Rupprecht CE. Serologic response of domestic ferrets ( Mustela puto-rius furo) to canine distemper and rabies virus vaccines. J Am Vet Med Assoc. 1989;194:234–238. [PubMed] [Google Scholar]
  32. Hsu KH, Lubeck MD, Bhat BM, Bhat RA, Kostek B, Selling BH, Mizutani S, Davis AR, Hung PP. Efficacy of adenovirus-vectored respiratory syncytial virus vaccines in a new ferret model. Vaccine. 1994;12:607–612. doi: 10.1016/0264-410X(94)90264-X. [DOI] [PubMed] [Google Scholar]
  33. Katz M, Rorke LB, Masland WS, Koprowski H, Tucker SH. Transmission of an encepha-litogenic agent from brains of patients with subacute sclerosing panencephalitis to ferrets. Preliminary report. N Engl J Med. 1968;279:793–798. doi: 10.1056/NEJM196810102791503. [DOI] [PubMed] [Google Scholar]
  34. Kauffman CA, Bergman AG, O'Connor RP. Distemper virus infection in ferrets: an animal model of measles-induced immunosuppression. Clin Exp Immunol. 1982;47:617–625. [PMC free article] [PubMed] [Google Scholar]
  35. Krakowka S. Mechanisms of in vitro immunosuppression in canine distemper virus infection. J Clin Lab Immunol. 1982;8:187–196. [PubMed] [Google Scholar]
  36. Krakowka S, Cockerell G, Koestner A. Effects of canine distemper virus infection on lym-phoid function in vitro and in vivo. Infect Immun. 1975;11:1069–1078. doi: 10.1128/iai.11.5.1069-1078.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Krakowka S, Axthelm MK, Johnsen GC. Canine distemper virus. In: Olsen RG, Krakowka S, Blakeslee JR, editors. Comparative pathobiology of viral diseases. FL, CRC: Boca Raton; 1985. pp. 137–164. [Google Scholar]
  38. Krakowka S, Ringler SS, Lewis M, Olsen RG, Axthelm MK. Immunosuppression by canine distemper virus: modulation of in vitro immunoglobulin synthesis, interleukin release and prostaglandin E2 production. Vet Immunol Immunopathol. 1987;15:181–201. doi: 10.1016/0165-2427(87)90082-1. [DOI] [PubMed] [Google Scholar]
  39. Loeffler IK, Howard J, Montali RJ, Hayek LA, Dubovi E, Zhang Z, Yan Q, Guo W, Wildt DE. Serosurvey of ex situ giant pandas ( Ailuropoda melanoleuca) and red pandas ( Ailurus fulgens) in China with implications for species conservation. J Zoo Wildl Med. 2007;38:559–566. doi: 10.1638/2006-0008R.1. [DOI] [PubMed] [Google Scholar]
  40. Maher JA, DeStefano J. The ferret: an animal model to study influenza virus. Lab Anim (NY) 2004;33:50–53. doi: 10.1038/laban1004-50. [DOI] [PubMed] [Google Scholar]
  41. McCullough B, Krakowka S, Koestner A. Experimental canine distemper virus-induced lymphoid depletion. Am J Pathol. 1974;74:155–170. [PMC free article] [PubMed] [Google Scholar]
  42. McKenna MC, Bell SK. Classification of mammals above the species level. New York: Columbia University Press; 1997. [Google Scholar]
  43. McQuaid S, Cosby SL, Koffi K, Honde M, Kirk J, Lucas SB. Distribution of measles virus in the central nervous system of HIV-seropositive children. Acta Neuropathol. 1998;96:637–642. doi: 10.1007/s004010050945. [DOI] [PubMed] [Google Scholar]
  44. Mehta PD, Thormar H. Immunological studies of subacute measles encephalitis in ferrets: similarities to human subacute sclerosing panencephalitis. J Clin Microbiol. 1979;9:601–604. doi: 10.1128/jcm.9.5.601-604.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Moody KD, Bowman TA, Lang CM. Laboratory management of the ferret for biomedical research. Lab Anim Sci. 1985;35:272–279. [PubMed] [Google Scholar]
  46. Morris JA, Coburn DR, O'Connor JR. Rapid protection of ferrets against fully virulent distemper virus with nebulized attenuated distemper virus. Cornell Vet. 1954;44:198–207. [PubMed] [Google Scholar]
  47. Moss WJ, Ryon JJ, Monze M, Griffin DE. Differential regulation of interleukin (IL)-4, IL-5, and IL-10 during measles in Zambian children. J Infect Dis. 2002;186:879–887. doi: 10.1086/344230. [DOI] [PubMed] [Google Scholar]
  48. Nagano I, Nakamura S, Yoshioka M, Kogure K. Immunocytochemical analysis of the cellular infiltrate in brain lesions in subacute sclerosing panencephalitis. Neurology. 1991;41:1639–1642. doi: 10.1212/wnl.41.10.1639. [DOI] [PubMed] [Google Scholar]
  49. Ochi A, Danesh A, Seneviratne C, Banner D, Devries ME, Rowe T, Xu L, Ran L, Czub M, Bosinger SE, et al. Cloning, expression and immunoassay detection of ferret IFN-gamma. Dev Comp Immunol. 2008;32:890–897. doi: 10.1016/j.dci.2007.12.008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Ohno S, Ono N, Takeda M, Takeuchi K, Yanagi Y. Dissection of measles virus V protein in relation to its ability to block alpha/beta interferon signal transduction. J Gen Virol. 2004;85:2991–2999. doi: 10.1099/vir.0.80308-0. [DOI] [PubMed] [Google Scholar]
  51. Osterhaus AD, Fouchier RA, Kuiken T. The aetiology of SARS: Koch's postulates fulfilled. Philos Trans R Soc Lond B Biol Sci. 2004;359:1081–1082. doi: 10.1098/rstb.2004.1489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Palosaari H, Parisien JP, Rodriguez JJ, Ulane CM, Horvath CM. STAT protein interference and suppression of cytokine signal transduction by measles virus V protein. J Virol. 2003;77:7635–7644. doi: 10.1128/JVI.77.13.7635-7644.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Pardo MC, Bauman JE, Mackowiak M. Protection of dogs against canine distemper by vaccination with a canarypox virus recombinant expressing canine distemper virus fusion and hemagglutinin glycoproteins. Am J Vet Res. 1997;58:833–836. [PubMed] [Google Scholar]
  54. Pardo MC, Tanner P, Bauman J, Silver K, Fischer L. Immunization of puppies in the presence of maternally derived antibodies against canine distemper virus. J Comp Pathol. 2007;137(1):S72–S75. doi: 10.1016/j.jcpa.2007.04.015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Pearson GL. Vaccine-induced canine distemper virus in black-footed ferrets. J Am Vet Med Assoc. 1977;170:103:106–109. [PubMed] [Google Scholar]
  56. Pollock RV, Carmichael LE. Maternally derived immunity to canine parvovirus infection: transfer, decline, and interference with vaccination. J Am Vet Med Assoc. 1982;180:37–42. [PubMed] [Google Scholar]
  57. Qin Q, Wei F, Li M, Dubovi EJ, Loeffler IK. Serosurvey of infectious disease agents of carnivores in captive red pandas ( Ailurus fulgens) in China. J Zoo Wildl Med. 2007;38:42–50. doi: 10.1638/06-048.1. [DOI] [PubMed] [Google Scholar]
  58. Quesenberry KE. Basic approach to veterinary care. In: Hillyer E V, Quesenberry KE, editors. Ferrets, rabbits, and rodents: clinical medicine and surgery. Philadelphia: W.B. Saunders; 1996. pp. 14–25. [Google Scholar]
  59. Rockborn G, Norrby E, Lannek N. Comparison between the immunizing effect in dogs and ferrets of living distemper vaccines, attenuated in dog tissue cultures and embryonated eggs. Res Vet Sci. 1965;6:423–427. [PubMed] [Google Scholar]
  60. Rudd PA, Cattaneo R, von Messling V. Canine distemper virus uses both the anterograde and the hematogenous pathway for neuroinvasion. J Virol. 2006;80:9361–9370. doi: 10.1128/JVI.01034-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Schluederberg A, Lamm SH, Landrigan PJ, Black FL. Measles immunity in children vaccinated before one year of age. Am J Epidemiol. 1973;97:402–409. doi: 10.1093/oxfordjournals.aje.a121521. [DOI] [PubMed] [Google Scholar]
  62. Schneider-Schaulies J, Niewiesk S, Schneider-Schaulies S, ter Meulen V. Measles virus in the CNS: the role of viral and host factors for the establishment and maintenance of a persistent infection. J Neurovirol. 1999;5:613–622. doi: 10.3109/13550289909021290. [DOI] [PubMed] [Google Scholar]
  63. Schobesberger M, Summerfield A, Doherr MG, Zurbriggen A, Griot C. Canine distemper virus-induced depletion of uninfected lymphocytes is associated with apoptosis. Vet Immunol Immunopathol. 2005;104:33–44. doi: 10.1016/j.vetimm.2004.09.032. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Senchak AJ, Sato AK, Vazquez R, Keller CE, Cable BB. Characterization of transforming growth factors beta1 and 2 in ferrets ( Mustela putorius furo) Comp Med. 2007;57:594–596. [PubMed] [Google Scholar]
  65. Shen DT, Gorham JR, Evermann JF, McKeirnan AJ. Comparison of subcutaneous and intramuscular administration of a live attenuated distemper virus vaccine in ferrets. Vet Rec. 1984;114:42–43. doi: 10.1136/vr.114.2.42. [DOI] [PubMed] [Google Scholar]
  66. Sips GJ, Chesik D, Glazenburg L, Wilschut J, De Keyser J, Wilczak N. Involvement of morbilliviruses in the pathogenesis of demyelinating disease. Rev Med Virol. 2007;17:223–244. doi: 10.1002/rmv.526. [DOI] [PubMed] [Google Scholar]
  67. Stephensen CB, Welter J, Thaker SR, Taylor J, Tartaglia J, Paoletti E. Canine distemper virus (CDV) infection of ferrets as a model for testing Morbillivirus vaccine strategies: NYVAC- and ALVAC-based CDV recombinants protect against symptomatic infection. J Virol. 1997;71:1506–1513. doi: 10.1128/jvi.71.2.1506-1513.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Strating A. Measles vaccine in dogs: efficacy against aerosol challenge with virulent canine distemper virus. J Am Vet Med Assoc. 1975;167:59–62. [PubMed] [Google Scholar]
  69. Summers BA, Greisen HA, Appel MJ. Early events in canine distemper demyelinating encephalomyelitis. Acta Neuropathol. 1979;46:1–10. doi: 10.1007/BF00684797. [DOI] [PubMed] [Google Scholar]
  70. Summers BA, Greisen HA, Appel MJ. Canine distemper encephalomyelitis: variation with virus strain. J Comp Pathol. 1984;94:65–75. doi: 10.1016/0021-9975(84)90009-4. [DOI] [PubMed] [Google Scholar]
  71. Svitek N, von Messling V. Early cytokine mRNA expression profiles predict Morbillivirus disease outcome in ferrets. Virology. 2007;362:404–410. doi: 10.1016/j.virol.2007.01.002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Tetteh JK, Addae MM, Ishiwada N, Yempewu SM, Yamaguchi S, Ofori-Adjei D, Kamiya H, Komada Y, Akanmori BD. Plasma levels of Th1 and Th2 cytokines in Ghanaian children with vaccine-modified measles. Eur Cytokine Netw. 2003;14:109–113. [PubMed] [Google Scholar]
  73. Thormar H, Mehta PD, Lin FH, Brown HR, Wisniewski HM. Presence of oligoclonal immunoglobulin G bands and lack of matrix protein antibodies in cerebrospinal fluids and sera of ferrets with measles virus encephalitis. Infect Immun. 1983;41:1205–1211. doi: 10.1128/iai.41.3.1205-1211.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Thormar H, Mehta PD, Barshatzky MR, Brown HR. Measles virus encephalitis in ferrets as a model for subacute sclerosing panencephalitis. Lab Anim Sci. 1985;35:229–232. [PubMed] [Google Scholar]
  75. Thormar H, Brown HR, Goller NL, Barshatzky MR, Wisniewski HM. Transmission of measles virus encephalitis to ferrets by intracardiac inoculation of a cell-associated SSPE virus strain. APMIS. 1988;96:1125–1128. doi: 10.1111/j.1699-0463.1988.tb00990.x. [DOI] [PubMed] [Google Scholar]
  76. van Moll P, Alldinger S, Baumgartner W, Adami M. Distemper in wild carnivores: an epidemiological, histological and immunocytochemical study. Vet Microbiol. 1995;44:193–199. doi: 10.1016/0378-1135(95)00012-Y. [DOI] [PubMed] [Google Scholar]
  77. Vandevelde M, Zurbriggen A. Demyelination in canine distemper virus infection: a review. Acta Neuropathol. 2005;109:56–68. doi: 10.1007/s00401-004-0958-4. [DOI] [PubMed] [Google Scholar]
  78. Vandevelde M, Kristensen F, Kristensen B, Steck AJ, Kihm U. Immunological and pathological findings in demyelinating encephalitis associated with canine distemper virus infection. Acta Neuropathol. 1982;56:1–8. doi: 10.1007/BF00691174. [DOI] [PubMed] [Google Scholar]
  79. Vandevelde M, Zurbriggen A, Steck A, Bichsel P. Studies on the intrathecal humoral immune response in canine distemper encephalitis. J Neuroimmunol. 1986;11:41–51. doi: 10.1016/0165-5728(86)90073-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. von Messling V, Springfeld C, Devaux P, Cattaneo R. A ferret model of canine distemper virus virulence and immunosuppression. J Virol. 2003;77:12579–12591. doi: 10.1128/JVI.77.23.12579-12591.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. von Messling V, Milosevic D, Cattaneo R. Tropism illuminated: lymphocyte-based pathways blazed by lethal morbillivirus through the host immune system. Proc Natl Acad Sci U S A. 2004;101:14216–14221. doi: 10.1073/pnas.0403597101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. von Messling V, Svitek N, Cattaneo R. Receptor (SLAM [CD150]) recognition and the V protein sustain swift lymphocyte-based invasion of mucosal tissue and lymphatic organs by a morbillivirus. J Virol. 2006;80:6084–6092. doi: 10.1128/JVI.00357-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Welter J, Taylor J, Tartaglia J, Paoletti E, Stephensen CB. Mucosal vaccination with recom-binant poxvirus vaccines protects ferrets against symptomatic CDV infection. Vaccine. 1999;17:308–318. doi: 10.1016/S0264-410X(98)00211-4. [DOI] [PubMed] [Google Scholar]
  84. Welter J, Taylor J, Tartaglia J, Paoletti E, Stephensen CB. Vaccination against canine distemper virus infection in infant ferrets with and without maternal antibody protection, using recombinant attenuated poxvirus vaccines. J Virol. 2000;74:6358–6367. doi: 10.1128/JVI.74.14.6358-6367.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Wilkins J, Wehrle PF. Additional evidence against measles vaccine administration to infants less than 12 months of age: altered immune response following active/passive immunization. J Pediatr. 1979;94:865–869. doi: 10.1016/S0022-3476(79)80203-6. [DOI] [PubMed] [Google Scholar]
  86. Williams ES, Anderson SL, Cavender J, Lynn C, List K, Hearn C, Appel MJ. Vaccination of black-footed ferret ( Mustela nigripes) x Siberian polecat ( M. eversmanni) hybrids and domestic ferrets ( M. putorius furo)against canine distemper. J Wildl Dis. 1996;32:417–423. doi: 10.7589/0090-3558-32.3.417. [DOI] [PubMed] [Google Scholar]
  87. Wimsatt J, Jay MT, Innes KE, Jessen M, Collins JK. Serologic evaluation, efficacy, and safety of a commercial modified-live canine distemper vaccine in domestic ferrets. Am J Vet Res. 2001;62:736–740. doi: 10.2460/ajvr.2001.62.736. [DOI] [PubMed] [Google Scholar]
  88. Wimsatt J, Biggins D, Innes K, Taylor B, Garell D. Evaluation of oral and subcutaneous delivery of an experimental canarypox recombinant canine distemper vaccine in the Siberian polecat ( Mustela eversmanni) J Zoo Wildl Med. 2003;34:25–35. doi: 10.1638/1042-7260(2003)34[0025:EOOASD]2.0.CO;2. [DOI] [PubMed] [Google Scholar]
  89. Zilliox MJ, Moss WJ, Griffin DE. Gene expression changes in peripheral blood mononu-clear cells during measles virus infection. Clin Vaccine Immunol. 2007;14:918–923. doi: 10.1128/CVI.00031-07. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Measles are provided here courtesy of Nature Publishing Group

RESOURCES