Establishment of the black-tailed prairie dog (Cynomys ludovicianus) as a novel animal model for comparing smallpox vaccines administered preexposure in both high- and low-dose monkeypox virus challenges

Journal of Virology

Volumn 85, Issue 15, 2011, Pages 7683-7698

  Keckler, M S ^a   Carroll, D S ^a   Gallardo Romero, N F ^a   Lash, R R ^a   Salzer, J S ^a   Weiss, S L ^a   Patel, N ^a   Clemmons, C J ^a   Smith, S K ^a   Hutson, C L ^a   Karem, K L ^a   Damon, I K ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ACAMBIS 200; NEUTRALIZING ANTIBODY; ORTHOPOXVIRUS ANTIBODY; SMALLPOX VACCINE; UNCLASSIFIED DRUG; VIRUS ANTIBODY; VIRUS DNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; DRUG MEGADOSE; DRUG SAFETY; FEMALE; HUMORAL IMMUNITY; LOW DRUG DOSE; MALE; MONKEYPOX; MORBIDITY; MORTALITY; NONHUMAN; PRIORITY JOURNAL; PUBLIC HEALTH; SINGLE DRUG DOSE; TREATMENT PLANNING; VACCINATION; WEIGHT REDUCTION;

ANIMALS; DNA, VIRAL; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; MALE; MODELS, ANIMAL; MONKEYPOX VIRUS; NEUTRALIZATION TESTS; SCIURIDAE; SMALLPOX VACCINE;

ANIMALIA; CYNOMYS; CYNOMYS LUDOVICIANUS; MONKEYPOX VIRUS; ORTHOPOXVIRUS; VARIOLA VIRUS;

EID: 79960395676     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02174-10     Document Type: Article

References (80)

1. Adams, M. M., A. D. Rice, and R. W. Moyer. 2007. Rabbitpox virus and vaccinia virus infection of rabbits as a model for human smallpox. J. Virol. 81:11084-11095.
2. Americo, J. L., B. Moss, and P. L. Earl. 2010. Identification of wild-derived inbred mouse strains highly susceptible to monkeypox virus infection for use as small animal models. J. Virol. 84:8172-8180.
3. Anonymous. 2003. Multistate outbreak of monkeypox-Illinois, Indiana, and Wisconsin, 2003. MMWR Morb. Mortal. Wkly. Rep. 52:537-540.
4. Anonymous. 2009. Progressive vaccinia in a military smallpox vaccinee-United States, 2009. MMWR Morb. Mortal. Wkly. Rep. 58:532-536.
5. Anonymous. 1980. World Health Organization on smallpox. J. Trop. Med. Hyg. 83:47-48.
6. Behbehani, A. M. 1983. The smallpox story: life and death of an old disease. Microbiol. Rev. 47:455-509.
7. Bray, M., and M. Buller. 2004. Looking back at smallpox. Clin. Infect. Dis. 38:882-889.
8. Croft, D. R., et al. 2007. Occupational risks during a monkeypox outbreak, Wisconsin, 2003. Emerg. Infect. Dis. 13:1150-1157.
9. Crotty, S., et al. 2003. Cutting edge: long-term B cell memory in humans after smallpox vaccination. J. Immunol. 171:4969-4973.
10. Davies, D. H., et al. 2008. Antibody profiling by proteome microarray reveals the immunogenicity of the attenuated smallpox vaccine modified vaccinia virus Ankara is comparable to that of Dryvax. J. Virol. 82:652-663.
11. Dimarco, N. M., L. Dart, and C. B. Sanborn. 2007. Modified activity-stress paradigm in an animal model of the female athlete triad. J. Appl. Physiol. 103:1469-1478.
12. Dubois, M. E., and M. K. Slifka. 2008. Retrospective analysis of monkeypox infection. Emerg. Infect. Dis. 14:592-599.
13. Earl, P. L., et al. 2004. Immunogenicity of a highly attenuated MVA smallpox vaccine and protection against monkeypox. Nature, 428:182-185.
14. Earl, P. L., et al. 2008. Rapid protection in a monkeypox model by a single injection of a replication-deficient vaccinia virus. Proc. Natl. Acad. Sci. U. S. A. 105:10889-10894.
15. Edghill-Smith, Y., et al. 2005. Smallpox vaccine-induced antibodies are necessary and sufficient for protection against monkeypox virus. Nat. Med. 11:740-747.
16. Ennis, F. A., J. Cruz, W. E. Demkowicz, Jr., A. L. Rothman, and D. J. McClain. 2002. Primary induction of human CD8 cytotoxic T lymphocytes and interferon-gamma-producing T cells after smallpox vaccination. J. Infect. Dis. 185:1657-1659.
17. Frey, S. E., et al. 2007. Clinical and immunologic responses to multiple doses of IMVAMUNE (modified vaccinia Ankara) followed by Dryvax challenge. Vaccine, 25:8562-8573.
18. Garza, N. L., et al. 2009. Evaluation of the efficacy of modified vaccinia Ankara (MVA)/IMVAMUNE against aerosolized rabbitpox virus in a rabbit model. Vaccine, 27:5496-5504.
19. Goff, A. J., et al. 2011. A novel respiratory model of infection with monkeypox virus in cynomolgus macaques. J. Virol. 85:4898-4909.
20. Guarner, J., et al. 2004. Monkeypox transmission and pathogenesis in prairie dogs. Emerg. Infect. Dis. 10:426-431.
21. Hahon, N., and B. J. Wilson. 1960. Pathogenesis of variola in Macaca irus monkeys. Am. J. Hyg. (Lond.), 71:69-80.
22. Handley, L., R. M. Buller, S. E. Frey, C. Bellone, and S. Parker. 2009. The new ACAM2000 vaccine and other therapies to control orthopoxvirus outbreaks and bioterror attacks. Expert Rev. Vaccines, 8:841-850.
23. Harkin, A., J. M. O'Donnell, and J. P. Kelly. 2002. A study of VitalView for behavioural and physiological monitoring in laboratory rats. Physiol. Behav. 77:65-77.
24. Hebert, J., et al. 2008. Thermoregulation in pronghorn antelope (Antilocapra americana, Ord) in winter. J. Exp. Biol. 211:749-756.
25. Hooper, J. W., et al. 2004. Smallpox DNA vaccine protects nonhuman primates against lethal monkeypox. J. Virol. 78:4433-4443.
26. Huggins, J., et al. 2009. Nonhuman primates are protected from smallpox virus or monkeypox virus challenges by the antiviral drug ST-246. Antimicrob. Agents Chemother. 53:2620-2625.
27. Hutson, C. L., et al. 2010. Dosage comparison of Congo Basin and West African strains of monkeypox virus using a prairie dog animal model of systemic orthopoxvirus disease. Virology, 402:72-82.
28. Hutson, C. L., et al. 2007. Monkeypox zoonotic associations: insights from laboratory evaluation of animals associated with the multi-state US outbreak. Am. J. Trop. Med. Hyg. 76:757-768.
29. Hutson, C. L., et al. 2009. A prairie dog animal model of systemic orthopoxvirus disease using West African and Congo Basin strains of monkeypox virus. J. Gen. Virol. 90:323-333.
30. Jacobs, B. L., et al. 2009. Vaccinia virus vaccines: past, present and future. Antiviral Res. 84:1-13.
31. Jahrling, P. B., et al. 2004. Exploring the potential of variola virus infection of cynomolgus macaques as a model for human smallpox. Proc. Natl. Acad. Sci. U. S. A. 101:15196-15200.
32. Jenner, E. 1801. An inquiry into the causes and effects of the variola vaccine, a disease discovered in some of the western counties of England, particularly Gloucestershire, 3rd ed. Printed for the author by D. N. Shury, London, England.
33. Johnson, M. C., I. K. Damon, and K. L. Karem. 2008. A rapid, highthroughput vaccinia virus neutralization assay for testing smallpox vaccine efficacy based on detection of green fluorescent protein. J. Virol. Methods 150:14-20.
34. Karem, K. L., et al. 2007. Monkeypox-induced immunity and failure of childhood smallpox vaccination to provide complete protection. Clin. Vaccine Immunol. 14:1318-1327.
35. Karem, K. L., M. Reynolds, V. Olson, Y. Li, and I. K. Damon. 2006. Monkeypox outbreak diagnostics and implications for vaccine protective effect. Nat. Med. 12:495-496.
36. Keckler, M. S., et al. 2010. Physiologic reference ranges for captive blacktailed prairie dogs (Cynomys ludovicianus). J. Am. Assoc. Lab. Anim. Sci. 49:274-281.
37. Kempe, C. H. 1972. The end of routine smallpox vaccination in the United States. Pediatrics 49:489-492.
38. Kile, J. C., et al. 2005. Transmission of monkeypox among persons exposed to infected prairie dogs in Indiana in 2003. Arch. Pediatr. Adolesc. Med. 159:1022-1025.
39. Kramski, M., et al. 2010. A novel highly reproducible and lethal nonhuman primate model for orthopox virus infection. PLoS One, 5:e10412.
40. Kugeler, K. J., R. Pappert, Y. Zhou, and J. M. Petersen. 2006. Real-time PCR for Francisella tularensis types A and B. Emerg. Infect. Dis. 12:1799-1801.
41. Kulesh, D. A., et al. 2004. Smallpox and pan-orthopox virus detection by real-time 3 -minor groove binder TaqMan assays on the Roche LightCycler and the Cepheid Smart Cycler platforms. J. Clin. Microbiol. 42:601-609.
42. Langohr, I. M., G. W. Stevenson, H. L. Thacker, and R. L. Regnery. 2004. Extensive lesions of monkeypox in a prairie dog (Cynomys sp). Vet. Pathol. 41:702-707.
43. Lewis, M. W., M. B. Graham, E. Hammarlund, J. Hanifin, and M. K. Slifka. 2007. Monkeypox without exanthem. N. Engl. J. Med. 356:2112-2114.
44. Li, Y., V. A. Olson, T. Laue, M. T. Laker, and I. K. Damon. 2006. Detection of monkeypox virus with real-time PCR assays. J. Clin. Virol. 36:194-203.
45. Likos, A. M., et al. 2005. A tale of two clades: monkeypox viruses. J. Gen. Virol. 86:2661-2672.
46. Mack, T. M., J. Noble, Jr., and D. B. Thomas. 1972. A prospective study of serum antibody and protection against smallpox. Am. J. Trop. Med. Hyg. 21:214-218.
47. Marriott, K. A., et al. 2008. Clonal vaccinia virus grown in cell culture fully protects monkeys from lethal monkeypox challenge. Vaccine, 26:581-588.
48. Mayr, A. 2003. Smallpox vaccination and bioterrorism with pox viruses. Comp. Immunol. Microbiol. Infect. Dis. 26:423-430.
49. Mertens, A., O. Stiedl, S. Steinlechner, and M. Meyer. 2008. Cardiac dynamics during daily torpor in the Djungarian hamster (Phodopus sungorus). Am. J. Physiol. Regul. Integr. Comp. Physiol. 294:R639-R650.
50. Meseda, C. A., et al. 2005. Enhanced immunogenicity and protective effect conferred by vaccination with combinations of modified vaccinia virus Ankara and licensed smallpox vaccine Dryvax in a mouse model. Virology, 339:164-175.
51. Moss, B. 2011. Smallpox vaccines: targets of protective immunity. Immunol. Rev. 239:8-26.
52. Moutaftsi, M., et al. 2010. Uncovering the interplay between CD8, CD4 and antibody responses to complex pathogens. Future Microbiol. 5:221-239.
53. Nedunchelliyan, S., D. S. Reddy, and K. S. Venkataraman. 1992. Buffalo pox infection in man. Indian J. Public Health, 36:57.
54. Nigam, P., et al. 2007. DNA/MVA HIV-1/AIDS vaccine elicits long-lived vaccinia virus-specific immunity and confers protection against a lethal monkeypox challenge. Virology, 366:73-83.
55. Paran, N., et al. 2009. Postexposure immunization with modified vaccinia virus Ankara or conventional Lister vaccine provides solid protection in a murine model of human smallpox. J. Infect. Dis. 199:39-48.
56. Parrino, J., et al. 2007. Safety, immunogenicity and efficacy of modified vaccinia Ankara (MVA) against Dryvax challenge in vaccinia-naive and vaccinia-immune individuals. Vaccine 25:1513-1525.
57. Reynolds, M. G., et al. 2007. Spectrum of infection and risk factors for human monkeypox, United States, 2003. Emerg. Infect. Dis. 13:1332-1339.
58. Reynolds, M. G., et al. 2006. Clinical manifestations of human monkeypox influenced by route of infection. J. Infect. Dis. 194:773-780.
59. Richard, J. L., and D. E. Grimes. 2008. Bioterrorism: class A agents and their potential presentations in immunocompromised patients. Clin. J. Oncol. Nurs. 12:295-302.
60. Rimoin, A. W., et al. 2010. Major increase in human monkeypox incidence 30 years after smallpox vaccination campaigns cease in the Democratic Republic of Congo. Proc. Natl. Acad. Sci. U. S. A. 107:16262-16267.
61. Ryan, C. P. 2008. Zoonoses likely to be used in bioterrorism. Public Health Rep. 123:276-281.
62. Sackal, C., et al. 2008. Bartonella spp. and Rickettsia felis in fleas, Democratic Republic of Congo. Emerg. Infect. Dis. 14:1972-1974.
63. Sakhatskyy, P., et al. 2008. Immunogenicity and protection efficacy of subunit-based smallpox vaccines using variola major antigens. Virology, 371:98-107.
64. Sale, T. A., J. W. Melski, and E. J. Stratman. 2006. Monkeypox: an epidemiologic and clinical comparison of African and US disease. J. Am. Acad. Dermatol. 55:478-481.
65. Schultz, D. A., J. E. Sagartz, D. L. Huso, and R. M. Buller. 2009. Experimental infection of an African dormouse (Graphiurus kelleni) with monkeypox virus. Virology, 383:86-92.
66. Serkova, N. J., J. C. Rose, L. E. Epperson, H. V. Carey, and S. L. Martin. 2007. Quantitative analysis of liver metabolites in three stages of the circannual hibernation cycle in 13-lined ground squirrels by NMR. Physiol. Genomics, 31:15-24.
67. Sinclair, R., S. A. Boone, D. Greenberg, P. Keim, and C. P. Gerba. 2008. Persistence of category A select agents in the environment. Appl. Environ. Microbiol. 74:555-563.
68. Singh, R. K., et al. 2007. Buffalopox: an emerging and re-emerging zoonosis. Anim. Health Res. Rev. 8:105-114.
69. Sivapalasingam, S., et al. 2007. Immunological memory after exposure to variola virus, monkeypox virus, and vaccinia virus. J. Infect. Dis. 195:1151-1159.
70. Smith, S. K., et al. 2009. In vitro efficacy of ST246 against smallpox and monkeypox. Antimicrob. Agents Chemother. 53:1007-1012.
71. Stabenow, J., et al. 2010. A mouse model of lethal infection for evaluating prophylactics and therapeutics against monkeypox virus. J. Virol. 84:3909-3920.
72. Stevenson, H. L., et al. 2003. Detection of novel Bartonella strains and Yersinia pestis in prairie dogs and their fleas (Siphonaptera: Ceratophyllidae and Pulicidae) using multiplex polymerase chain reaction. J. Med. Entomol. 40:329-337.
73. Terajima, M., et al. 2008. Vaccinia virus-specific CD8(+) T-cell responses target a group of epitopes without a strong immunodominance hierarchy in humans. Hum. Immunol. 69:815-825.
74. Tesh, R. B., et al. 2004. Experimental infection of ground squirrels (Spermophilus tridecemlineatus) with monkeypox virus. Emerg. Infect. Dis. 10: 1563-1567.
75. Tian, T., et al. 2009. Overexpression of IL-1 in skin differentially modulates the immune response to scarification with vaccinia virus. J. Investig. Dermatol. 129:70-78.
76. Trindade, G. S., G. L. Emerson, D. S. Carroll, E. G. Kroon, and I. K. Damon. 2007. Brazilian vaccinia viruses and their origins. Emerg. Infect. Dis. 13:965-972.
77. Vorou, R. M., V. G. Papavassiliou, and I. N. Pierroutsakos. 2008. Cowpox virus infection: an emerging health threat. Curr. Opin. Infect. Dis. 21:153-156.
78. Wells, T. S., et al. 2008. Self-reported adverse health events following smallpox vaccination in a large prospective study of US military service members. Hum. Vaccin. 4:127-133.
79. Wyatt, L. S., P. L. Earl, L. A. Eller, and B. Moss. 2004. Highly attenuated smallpox vaccine protects mice with and without immune deficiencies against pathogenic vaccinia virus challenge. Proc. Natl. Acad. Sci. U. S. A. 101:4590-4595.
80. Xiao, S. Y., et al. 2005. Experimental infection of prairie dogs with monkeypox virus. Emerg. Infect. Dis. 11:539-545.