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Volume 12, Number 4—April 2006
Research

Animals as Sentinels of Bioterrorism Agents

Peter Rabinowitz*Comments to Author , Zimra Gordon*†, Daniel Chudnov*, Matthew Wilcox*, Lynda Odofin*, Ann Liu*, and Joshua Dein‡
Author affiliations: *Yale University School of Medicine, New Haven, Connecticut, USA; †Rippowam Animal Hospital, Stamford, Connecticut, USA; ‡US Geological Survey National Wildlife Health Center, Madison, Wisconsin, USA

Main Article

Table

Evidence for animals as sentinels of bioterrorism agents*

Agent/disease Animals provide early warning of acute bioterrorism attack Animals could be markers for ongoing exposure risk Animals can propagate/maintain epidemic
Category A
Anthrax Yes: sheep, cattle (level 3 evidence [6])
No: dogs and pigs (level 1 evidence [7]) Yes: sheep, cattle (level 3 evidence [6,8]) –
Plague Yes: cats (level 1 evidence [9]) Yes: dogs, cats (level 1 evidence [9]), multiple species (level 2 evidence [10]) Yes: cats, camels, goats (level 3 evidence [11,12])
Tularemia No (level 3 evidence [13]) Yes: rodents (level 2 evidence [14])
No: horses, cows (level 2 evidence [13]) Yes: ticks, rodents, prairie dogs (level 2 evidence [15])
Botulism No (level 3 evidence [16]) No (level 3 evidence [16]) No (level 3 evidence [16)
Filovirus infection – – Yes: wildlife (level 3 evidence [17])
Category B
Q fever No: sheep (level 1 evidence [18]) Yes: wild hogs, goats (level 2 evidence [19,20]) Yes: cats, sheep, goat, cattle (level 3 evidence [21])
Brucellosis No (level 3 evidence [3]) Yes: cattle (level 2 [22]) Yes: wildlife, cattle, dogs (level 3 evidence [23])
Foodborne illness: Salmonella spp; Shigella spp.; Cryptosporidium spp, etc. Yes: cattle (level 3 evidence [24]) – –
Glanders – Yes: horses (level 2 evidence [25]) Yes: horses (level 3 evidence [26])
Alphaviruses (VEE/EEE) Yes: horses (level 3 evidence [26])) Yes: birds (level 1 evidence [27]) Yes: wild birds (level 2 evidence [27])
Rift valley fever Yes: cattle, sheep (level 3 evidence [23]) Yes: sheep (level 1 evidence [28]) Yes: mosquitoes, rodents (level 1 evidence [29])
Ricin toxin – – –
Epsilon toxin – – –
Category C (emerging diseases)
Nipah virus – Yes: multiple species (level 3 evidence [30]) Yes: pigs (level 1 evidence [31])
Hantavirus No (level 2 evidence [32]) Yes: multiple species (level 2 evidence [32]) Yes: rodents (level 2 evidence [33])
Flavivirus (WN, JE) Yes: wild birds (level 3 evidence [34]) Yes: mosquitoes, birds (level 2 evidence [35]) Yes: birds (level 1 evidence [36])

*Level 1 evidence, experimental or cohort study or randomized clinical trial; level 2 evidence, case-control or cross-sectional study; level 3 evidence, case reports or case series, expert opinion; .–, insufficient evidence found; VEE/EEE, Venezuelan equine encephalitis /eastern equine encephalitis; WN, West Nile; JE, Japanese encephalitis.

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References
  1. Centers for Disease Control and Prevention. Biological and chemical terrorism: strategic plan for preparedness and response. Recommendations of the CDC Strategic Planning Workgroup. MMWR Morb Mortal Wkly Rep. 2000;49:1–14.PubMedGoogle Scholar
  2. Cottrell  TS, Morgan  ER. Animal surveillance in NBC defensive operations. J R Army Med Corps. 2003;149:225–30.
  3. Davis  RG. The ABCs of bioterrorism for veterinarians, focusing on Category A agents. J Am Vet Med Assoc. 2004;224:1084–95. DOIPubMedGoogle Scholar
  4. Kortepeter  M, Eitzen  E Jr, Mckee  K Jr, eds. USAMRIID's medical management of biological casualties handbook. 4th ed. McLean (VA): International Medical Publishing Inc; 2001.
  5. Phillips  B, Ball  C, Sackett  D, Badenoch  D, Straus  S, Haynes  B, Levels of evidence and grades of recommendation. Oxford Centre for Evidence Based Medicine; 2001 [cited 2005 Nov 28]. Available from http://www.cebm.net/levels_of_evidence.asp#levels
  6. Meselson  M, Guillemin  J, Hugh-Jones  M, Langmuir  A, Popova  I, Shelokov  A, The Sverdlovsk anthrax outbreak of 1979. Science. 1994;266:1202–8. DOIPubMedGoogle Scholar
  7. Gleiser  CA, Gochenour  WS Jr, Ward  MK. Pulmonary lesions in dogs and pigs exposed to a cloud of anthrax spores. J Comp Pathol. 1968;78:445–8. DOIPubMedGoogle Scholar
  8. McGee  ED, Fritz  DL, Ezzell  JW, Newcomb  HL, Brown  RJ, Jaax  NK. Anthrax in a dog. Vet Pathol. 1994;31:471–3. DOIPubMedGoogle Scholar
  9. Rust  JH Jr, Cavanaugh  DC, O'Shita  R, Marshall  JD Jr. The role of domestic animals in the epidemiology of plague. I. Experimental infection of dogs and cats. J Infect Dis. 1971;124:522–6. DOIPubMedGoogle Scholar
  10. Kilonzo  BS, Mbise  TJ, Makundi  RH. Plague in Lushoto district, Tanzania, 1980-1988. Trans R Soc Trop Med Hyg. 1992;86:444–5. DOIPubMedGoogle Scholar
  11. Eidson  M, Thilsted  JP, Rollag  OJ. Clinical, clinicopathologic, and pathologic features of plague in cats: 119 cases (1977–1988). J Am Vet Med Assoc. 1991;199:1191–7.PubMedGoogle Scholar
  12. Christie  AB, Chen  TH, Elberg  SS. Plague in camels and goats: their role in human epidemics. J Infect Dis. 1980;141:724–6. DOIPubMedGoogle Scholar
  13. Dahlstrand  S, Ringertz  O, Zetterberg  B. Airborne tularemia in Sweden. Scand J Infect Dis. 1971;3:7–16.PubMedGoogle Scholar
  14. Feldman  KA, Enscore  RE, Lathrop  SR, Matyas  BT, McGuill  M, Schriefer  ME, An outbreak of primary pneumonic tularemia on Martha's Vineyard. N Engl J Med. 2001;345:1601–6. DOIPubMedGoogle Scholar
  15. Avashia  SB, Peterson  JM, Lindley  CM, Schriefer  ME, Gage  KL, Cetron  M, First reported prairie dog-to-human tularemia transmission, Texas, 2002. Emerg Infect Dis. 2004;10:483–6.PubMedGoogle Scholar
  16. Arnon  SS, Schechter  R, Inglesby  TV, Henderson  DA, Bartlett  JG, Ascher  MS, Botulinum toxin as a biological weapon: medical and public health management. [Erratum in: JAMA 2001;285:2081]. JAMA. 2001;285:1059–70. DOIPubMedGoogle Scholar
  17. Leroy  EM, Rouquet  P, Formenty  P, Souquiere  S, Kilbourne  A, Forment  J, Multiple Ebola virus transmission events and rapid decline of central African wildlife. Science. 2004;303:387–90. DOIPubMedGoogle Scholar
  18. Martinov  SP, Neikov  P, Popov  GV. Experimental Q fever in sheep. Eur J Epidemiol. 1989;5:428–31. DOIPubMedGoogle Scholar
  19. Clark  RK, Jessup  DA, Hird  DW, Ruppanner  R, Meyer  ME. Serologic survey of California wild hogs for antibodies against selected zoonotic disease agents. J Am Vet Med Assoc. 1983;183:1248–51.PubMedGoogle Scholar
  20. Scrimgeour  EM, Al-Ismaily  SI, Rolain  JM, Al-Dhahry  SH, El-Khatim  HS, Raoult  D. Q fever in human and livestock populations in Oman. Ann N Y Acad Sci. 2003;990:221–5. DOIPubMedGoogle Scholar
  21. McQuiston  JH, Childs  JE, Thompson  HA. Q fever. J Am Vet Med Assoc. 2002;221:796–9. DOIPubMedGoogle Scholar
  22. Kubuafor  DK, Awumbila  B, Akanmori  BD. Seroprevalence of brucellosis in cattle and humans in the Akwapim-South district of Ghana: public health implications. Acta Trop. 2000;76:45–8. DOIPubMedGoogle Scholar
  23. Radostits  OMG, Gay  CC, Blood  DC, Hinchcliff  KW, eds. Veterinary medicine: a textbook of the diseases of cattle, sheep, pigs, goats and horses. 9th ed. London: Harcourt Publishers Ltd; 2000.
  24. Cupp  OS, Walker  DE II, Hillison  J. Agroterrorism in the U.S.: key security challenge for the 21st century. Biosecur Bioterror. 2004;2:97–105. DOIPubMedGoogle Scholar
  25. Arun  S, Neubauer  H, Gurel  A, Ayyildiz  G, Kuscu  B, Yesidere  T, Equine glanders in Turkey. Institute for Animal Pathology. 1999;144:255–8.PubMedGoogle Scholar
  26. Greene  CE. Infectious diseases of the dog and cat. 2nd ed. Philadelphia: W.B. Saunders; 1998.
  27. Howard  JJ, Grayson  MA, White  DJ, Oliver  J. Evidence for multiple foci of eastern equine encephalitis virus (Togaviridae:Alphavirus) in central New York State. J Med Entomol. 1996;33:421–32.PubMedGoogle Scholar
  28. Olaleye  OD, Tomori  O, Schmitz  H. Rift Valley fever in Nigeria: infections in domestic animals. Rev Sci Tech. 1996;15:937–46.PubMedGoogle Scholar
  29. Gargan  TP II, Clark  GG, Dohm  DJ, Turell  MJ, Bailey  CL. Vector potential of selected North American mosquito species for Rift Valley fever virus. Am J Trop Med Hyg. 1988;38:440–6.PubMedGoogle Scholar
  30. Bunning  M. Nipah virus outbreak in Malaysia, 1998–1999. Journal of Swine Health Products. 2001;9:295–9.
  31. Middleton  DJ, Westbury  HA, Morrissy  CJ, van der Heide  BM, Russell  GM, Braun  MA, Experimental Nipah virus infection in pigs and cats. J Comp Pathol. 2002;126:124–36. DOIPubMedGoogle Scholar
  32. Mills  JN, Yates  TL, Ksiazek  TG, Peters  CJ, Childs  JE. Long-term studies of Hantavirus reservoir populations in the southwestern United States: rationale, potential, and methods. Emerg Infect Dis. 1999;5:95–101. DOIPubMedGoogle Scholar
  33. Traavik  T, Sommer  A, Mehl  R, Berdal  BP, Stavem  K, Hunderi  OH, Nephropathia epidemica in Norway: antigen and antibodies in rodent reservoirs and antibodies in selected human populations. J Hyg (Camb). 1984;93:139–46. DOIPubMedGoogle Scholar
  34. Mostashari  F, Kulldorff  M, Hartman  JJ, Miller  JR, Kulasekera  V. Dead bird clusters as an early warning system for West Nile virus activity. Emerg Infect Dis. 2003;9:641–6.PubMedGoogle Scholar
  35. Komar  O, Robbins  MB, Klenk  K, Blitvich  BJ, Marlenee  NL, Burkhalter  KL, West Nile virus transmission in resident birds, Dominican Republic. Emerg Infect Dis. 2003;9:1299–302.PubMedGoogle Scholar
  36. Komar  N, Langevin  S, Hinten  S, Nemeth  N, Edwards  E, Hettler  D, Experimental infection of North American birds with the New York 1999 strain of West Nile virus. Emerg Infect Dis. 2003;9:311–22.PubMedGoogle Scholar
  37. Jernigan  JA, Stephen  DS, Ashford  DA, Omenaca  C, Topiel  MS, Galbraith  M, Bioterrorism-related inhalational anthrax: the first 10 cases reported in the United States. Emerg Infect Dis. 2001;7:933–44. DOIPubMedGoogle Scholar
  38. Grant  S, Olsen  CW. Preventing zoonotic diseases in immunocompromised persons: the role of physicians and veterinarians. Emerg Infect Dis. 1999;5:159–63. DOIPubMedGoogle Scholar
  39. Dauphin  G, Zientara  S, Zeller  H, Murgue  B. West Nile: worldwide current situation in animals and humans. Comp Immunol Microbiol Infect Dis. 2004;27:343–55. DOIPubMedGoogle Scholar

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