Considerations in the Use of Nonhuman Primate Models of Ebola Virus and Marburg Virus Infection

Journal of Infectious Diseases

Volumn 212, Issue , 2015, Pages S91-S97

  Geisbert, Thomas W ^a,b   Strong, James E ^d,e,f   Feldmann, Heinz ^c  

^a UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^b University of Texas Medical Branch School of Medicine   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^e University of Manitoba ^*  (Canada)

^f UNIVERSITY OF MANITOBA   (Canada)

Author keywords

animal model; Ebola virus; filovirus; Marburg virus; nonhuman primate; treatment; vaccine

Indexed keywords

ANIMAL EUTHANASIA; BIOSAFETY; BUNDIBUGYO EBOLAVIRUS; CALLITHRIX JACCHUS; CHLOROCEBUS AETHIOPS; EBOLA HEMORRHAGIC FEVER; EBOLAVIRUS; EXPERIMENTAL INFECTION; GENETIC DIFFERENCE; GOOD LABORATORY PRACTICE; IVORY COAST EBOLAVIRUS; MACACA FASCICULARIS; MARBURG HEMORRHAGIC FEVER; NONHUMAN; PAPIO HAMADRYAS; PRIMATE MODEL; PRIORITY JOURNAL; RESTON EBOLAVIRUS; REVIEW; RHESUS MONKEY; SUDAN EBOLAVIRUS; VIRUS LOAD; VIRUS STRAIN; ZAIRE EBOLAVIRUS; AFRICA; ANIMAL; DISEASE MODEL; EPIDEMIC; HEMORRHAGIC FEVER, EBOLA; HUMAN; IMMUNOLOGY; MARBURG VIRUS DISEASE; MARBURGVIRUS; PRIMATE; VIROLOGY;

GLYCOPROTEIN; LIVE VACCINE; VIRUS VACCINE;

AFRICA, WESTERN; ANIMALS; DISEASE MODELS, ANIMAL; DISEASE OUTBREAKS; EBOLAVIRUS; GLYCOPROTEINS; HEMORRHAGIC FEVER, EBOLA; HUMANS; MACACA FASCICULARIS; MACACA MULATTA; MARBURG VIRUS DISEASE; MARBURGVIRUS; PRIMATES; VACCINES, ATTENUATED; VIRAL VACCINES;

EID: 84943270748     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiv284     Document Type: Review

References (41)

1. Bray M, Davis K, Geisbert T, Schmaljohn C, Huggins J. A mouse model for evaluation of prophylaxis and therapy of Ebola hemorrhagic fever. J Infect Dis 1998; 178:651-61.
2. Connolly BM, Steele KE, Davis KJ, et al. Pathogenesis of experimental Ebola virus infection in guinea pigs. J Infect Dis 1999; 179(suppl 1): S203-17.
3. Warfield KL, Bradfute SB,Wells J, et al. Development and characterization of a mouse model for Marburg hemorrhagic fever. J Virol 2009; 83:6404-15.
4. Lofts LL, Ibrahim MS, Negley DL, Hevey MC, Schmaljohn AL. Genomic differences between guinea pig lethal and nonlethal Marburg virus variants. J Infect Dis 2007; 196(suppl 2):S305-12.
5. Ebihara H, Zivcec M, Gardner D, et al. A Syrian golden hamster model recapitulating Ebola hemorrhagic fever. J Infect Dis 2013; 207:306-18.
6. Rasmussen AL, Okumura A, Ferris MT, et al. Host genetic diversity enables Ebola hemorrhagic fever pathogenesis and resistance. Science 2014; 346:987-91.
7. Bray M, Hatfill S, Hensley L, Huggins JW. Haematological, biochemical and coagulation changes in mice, guinea-pigs and monkeys infected with a mouse-adapted variant of Ebola Zaire virus. J Comp Pathol 2001; 125:243-53.
8. Geisbert TW, Pushko P, Anderson K, Smith J, Davis KJ, Jahrling PB. Evaluation in nonhuman primates of vaccines against Ebola virus. Emerg Infect Dis 2002; 8:503-7.
9. Cross RW, Fenton KA, Geisbert JB, Mire CE, Geisbert TW. Modeling the disease course of Zaire ebolavirus infection in the outbred guinea pig. J Infect Dis 2015; 212(suppl 2):S305-15.
10. Cross RW, Fenton KA, Geisbert JB, Ebihara H, Mire CE, Geisbert TW. Comparison of the pathogenesis of the Angola and Ravn strains of Marburg virus in the outbred guinea pig model. J Infect Dis 2015; 212(suppl 2):S258-70.
11. Feldmann H, Sanchez A, Geisbert TW. Filoviridae: Marburg and Ebola viruses. In: Knipe DM, Howley PM, eds. Fields virology. 6th ed. Philadelphia: Lippincott Williams and Wilkins, 2013:923-56.
12. Geisbert TW, Jahrling PB, Larsen T, Davis KJ, Hensley LE. Filovirus pathogenesis in nonhuman primates. In: Klenk H-D, Feldmann H, eds. Ebola and Marburg viruses: molecular and cellular biology. Norfolk, UK: Horizon Bioscience, 2004:203-38.
13. Davis KJ, Anderson AO, Geisbert TW, et al. Pathology of experimental Ebola virus infection in African green monkeys. Involvement of fibroblastic reticular cells. Arch Pathol Lab Med 1997; 121:805-19.
14. Reed DS, Lackemeyer MG, Garza NL, Sullivan LJ, Nichols DK. Aerosol exposure to Zaire ebolavirus in three nonhuman primate species: differences in disease course and clinical pathology. Microbes Infect 2011; 13:930-6.
15. Carrion R Jr, Ro Y, Hoosien K, et al. A small nonhuman primate model for filovirus-induced disease. Virology 2011; 420:117-24.
16. Volchkova VA, Dolnik O, Martinez MJ, Reynard O, Volchkov VE. Genomic RNA editing and its impact on Ebola virus adaptation during serial passages in cell culture and infection of guinea pigs. J Infect Dis 2011; 204(suppl 3):S941-6.
17. Kugelman JR, Lee MS, Rossi CA, et al. Ebola virus genome plasticity as a marker of its passaging history: A comparison of in vitro passaging to non-human primate infection. PLoS One 2012; 7:e50316.
18. Sanchez A, Yang ZY, Xu L, Nabel GJ, Crews T, Peters CJ. Biochemical analysis of the secreted and virion glycoproteins of Ebola virus. J Virol 1998; 72:6442-7.
19. Volchkov VE, Becker S, Volchkova VA, et al. GP mRNA of Ebola virus is edited by the Ebola virus polymerase and by T7 and vaccinia virus polymerases. Virology 1995; 214:421-30.
20. Mehedi M, Hoenen T, Robertson S, et al. Ebola virus RNA editing depends on the primary editing site sequence and an upstream secondary structure. PLoS Pathog 2013; 9:e1003677.
21. Mohan GS, Li W, Ye L, Compans RW, Yang C. Antigenic subversion: A novel mechanism of host immune evasion by Ebola virus. PLoS Pathog 2012; 8:e1003065.
22. Trefry JC, Wollen SE, Kugelman JR, Palacios GF, Honko AN, Pitt LM. In vivo pathological consequences of Ebola virus genome plasticity: is a 7U virus more lethal? Presented at: 2015 ASM Biodefense and Emerging Diseases Research Meeting, Washington, D. C., 2015.
23. Hirschberg R, Ward LA, Kilgore N, et al. Challenges, progress, and opportunities: proceedings of the filovirus medical countermeasures workshop. Viruses 2014; 6:2673-97.
24. Geisbert TW, Daddario-DiCaprio KM, Geisbert JB, et al. Marburg virus Angola infection of rhesus macaques: pathogenesis and treatment with recombinant nematode anticoagulant protein c2. J Infect Dis 2007; 196(suppl 2):S372-81.
25. Fernando L, Qiu X, Melito PL, et al. Immune response to Marburg virus Angola infection in nonhuman primates. J Infect Dis 2015212(suppl 2): S234-41.
26. Sullivan NJ, Sanchez A, Rollin PE, Yang ZY, Nabel GJ. Development of a preventive vaccine for Ebola virus infection in primates. Nature 2000; 408:605-9.
27. Sullivan NJ, Geisbert TW, Geisbert JB, et al. Accelerated vaccination for Ebola virus haemorrhagic fever in non-human primates. Nature 2003; 424:681-4.
28. Alves DA, Glynn AR, Steele KE, et al. Aerosol exposure to the Angola strain of Marburg virus causes lethal viral hemorrhagic fever in cynomolgus macaques. Vet Pathol 2010; 47:831-51.
29. World Health Organization. Ebola haemorrhagic fever in Zaire, 1976. Bull World Health Organ 1978; 56:271-93.
30. Jaax NK, Davis KJ, Geisbert TJ, et al. Lethal experimental infection of rhesus monkeys with Ebola-Zaire (Mayinga) virus by the oral and conjunctival route of exposure. Arch Pathol Lab Med 1996; 120:140-55.
31. Kortepeter MG, Bausch DG, Bray M. Basic clinical and laboratory features of filoviral hemorrhagic fever. J Infect Dis 2011; 204(suppl 3): S810-6.
32. US Department of Health and Human Services (DHHS). Guidance for industry: product development under the animal rule. Silver Spring, MD: DHHS, 2014.
33. Qiu X, Wong G, Audet J, et al. Reversion of advanced Ebola virus disease in nonhuman primates with ZMapp. Nature 2014; 514:47-53.
34. Thi EP, Mire CE, Lee ACH, et al. Lipid nanoparticle siRNA treatment of Ebola-virus-Makona-infected nonhuman primates. Nature 2015; 521:362-5.
35. Lyon GM, Mehta AK, Varkey JP, et al. Clinical care of two patients with Ebola virus disease in the United States. N Engl J Med 2014; 371: 2402-9.
36. Kraft CS, Hewlett AL, Koepsell S, et al. The use of TKM-100802 and convalascent plasma in 2 patients with Ebola virus disease in the United States. Clin Infect Dis 2015; 61:496-502.
37. Ledgerwood JE, DeZure AD, Stanley DA, et al. Chimpanzee adenovirus vector Ebola vaccine-preliminary report. N Engl J Med 2014; doi:10.1056/NEJMoa1410863.
38. Rampling T, Ewer K, Bowyer G, et al. A monovalent chimpanzee adenovirus Ebola vaccine-preliminary report. N Engl J Med 2015; doi:10.1056/NEJMoa1411627.
39. Regules JA, Beigel JH, Paolino KM, et al. A recombinant vesicular stomatitis virus Ebola vaccine-preliliminary report. N Engl J Med 2015; doi:10.1056/NEJMoa1414216.
40. Agnandji ST, Huttner A, Zinser ME, et al. Phase 1 trials of rVSV Ebola vaccine in Africa and Europe-preliminary report. N Engl J Med 2015; doi:10.1056/NEJMoa1502924.
41. Mire CE, Mattassov D, Geisbert JB, et al. Single-dose attenuated Vesiculovax vaccines protect primates against Ebola Makona virus. Nature 2015; 520:688-91.