Persistence of category A select agents in the environment

Applied and Environmental Microbiology

Volumn 74, Issue 3, 2008, Pages 555-563

  Sinclair, Ryan ^a   Boone, Stephanie A ^b   Greenberg, David ^c   Keim, Paul ^c   Gerba, Charles P ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c NORTHERN ARIZONA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

WATER;

ENVIRONMENTAL IMPACT ASSESSMENT; ENVIRONMENTAL RISK; MICROBIAL ACTIVITY; WAR; WATER POLLUTION;

AEROSOL; BACILLUS ANTHRACIS; BACTERIAL SPORE; BACTERIAL TRANSMISSION; BIOLOGICAL WARFARE; EBOLA VIRUS; ENVIRONMENTAL EXPOSURE; FLAVIVIRUS; FOMITE; FRANCISELLA TULARENSIS; HANTAVIRUS; HUMAN; INFECTION RISK; MARBURG VIRUS; NONHUMAN; RISK ASSESSMENT; SHORT SURVEY; SMALLPOX VIRUS; SOIL; VIRUS TRANSMISSION; YELLOW FEVER FLAVIVIRUS;

BACILLUS ANTHRACIS; BACTERIA; BIOLOGICAL WARFARE AGENTS; BIOTERRORISM; CENTERS FOR DISEASE CONTROL AND PREVENTION (U.S.); CLOSTRIDIUM BOTULINUM; ENVIRONMENT; FRANCISELLA TULARENSIS; HEMORRHAGIC FEVERS, VIRAL; HUMANS; UNITED STATES; VARIOLA VIRUS; VIRUSES;

EID: 38949144492     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.02167-07     Document Type: Short Survey

References (94)

1. Abd, H., T. Johansson, I. Golovliov, G. Sandstrom, and M. Forsman. 2003. Survival and growth of Francisella tularensis in Acanthamoeba castellanii. Appl. Environ. Microbiol. 69:600-606.
2. Adebayo, A. A., J. W. Sim-Brandenburg, H. Emmel, D. O. Olaleye, and M. Niedrig. 1998. Stability of 17D yellow fever virus vaccine using different stabilizers. Biologicals 26:309-316.
3. Anisimov, A. P. 2002. Factors of Yersinia pestis providing circulation and persistence of plague pathogen in ecosystems of natural foci. Communication 2. Mol. Gen. Mikrobiol. Virusol. 2002:3-11. (In Russian.)
4. Anisimov, A. P. 2002. Yersinia pestis factors, assuring circulation and maintenance of the plague pathogen in natural foci ecosystems. Report 1. Mol. Gen. Mikrobiol. Virusol. 2002:3-23. (In Russian.)
5. Atlas, R. M. 2002. Responding to the threat of bioterrorism: a microbial ecology perspective - a case of anthrax. Int. Microbiol. 5:161-167.
6. Baron, R. C., J. B. McCormick, and O. A. Zubeir. 1983. Ebola virus disease in southern Sudan: hospital dissemination and intrafamilial spread. Bull. W. H. O. 61:997-1003.
7. Belanov, E. F., V. P. Muntianov, V. D. Kriuk, A. V. Sokolov, N. I. Bormotov, O. V. P'Iankov, and A. N. Sergeev. 1996. Survival of Marburg virus infectivity on contaminated surfaces and in aerosols. Vopr. Virusol. 41:32-34. (In Russian.)
8. Blawat, F., U. Potajallo, J. Dabrowski, A. Towianska, and I. Jarnuskiewicz. 1976. Survival of some viruses in the sea-water samples collected from the Gulf of Gdansk. Preliminary studies. Bull. Inst. Marit. Trop. Med. Gdynia 27:331-339.
9. Boone, S. A., and C. P. Gerba. 2007. Significance of fomites in the spread of respiratory and enteric viral disease. Appl. Environ. Microbiol. 73:1687-1696.
10. Borio, L., T. Inglesby, C. J. Peters, A. L. Schmaljohn, J. M. Hughes, P. B. Jahrling, T. Ksiazek, K. M. Johnson, A. Meyerhoff, T. O'Toole, M. S. Ascher, J. Bartlett, J. G. Breman, E. M. Eitzen, Jr., M. Hamburg, J. Hauer, D. A. Henderson, R. T. Johnson, G. Kwik, M. Layton, S. Lillibridge, G. J. Nabel, M. T. Osterholm, T. M. Perl, P. Russell, and K. Tonat. 2002. Hemorrhagic fever viruses as biological weapons: medical and public health management. JAMA 287:2391-2405.
11. Brachman, P. S., A. F. Kaufman, and F. G. Dalldorf. 1966. Industrial inhalation anthrax. Bacteriol. Rev. 30:646-659.
12. Braithwaite, R. S., D. Fridsma, and M. S. Roberts. 2006. The cost-effectiveness of strategies to reduce mortality from an intentional release of aerosolized anthrax spores. Med. Decis. Making 26:182-193.
13. Breneva, N. V., A. S. Maramovich, and V. T. Klimov. 2005. Ecological regularities of the existence of pathogenic Yersinia in soil ecosystems. Zh. Mikrobiol. Epidemiol. Immunobiol. November/December:82- 88. (In Russian.)
14. Breneva, N. V., A. S. Maramovich, and V. T. Klimov. 2006. The population variability of Yersinia pestis in soil samples from the natural focus of plague. Zh. Mikrobiol. Epidemiol. Immunobiol. March/April:7-11. (In Russian.)
15. Brodie, E. L., T. Z. DeSantis, J. P. Parker, I. X. Zubietta, Y. M. Piceno, and G. L. Andersen. 2007. Urban aerosols harbor diverse and dynamic bacterial populations. Proc. Natl. Acad. Sci. USA 104:299-304.
16. Broussard, L. A. 2001. Biological agents: weapons of warfare and bioterrorism. Mol. Diagn. 6:323-333.
17. Busson, B. 1911. Ein Beitrag zur Kenntnis der Lebensdauer von Bacterium coli und Milzbrandsporen. Zentralbl. Bakteriol. Parasitenkd. Infektionskr. 58:505-509.
18. Chupurnova, T. S., V. A. Pisanko, L. F. Bakulina, V. A. Zhukov, and A. A. Chepurnov. 2000. Assay for level of Marburg virus in blood and isolates from experimentally infected animals. Vopr. Virusol. 45(2):18-20. (In Russian.)
19. Clegg, S., et al. July 2006. Preparedness for anthrax epizootics in wildlife areas. http://www.cdc.gov/ncidod/EID/vol12no07/06-0458.htm.
20. Cox, C. S. 1971. Aerosol survival of Pasteurella tularensis disseminated from the wet and dry states. Appl. Microbiol. 21:482-486.
21. Cox, C. S., and L. J. Goldberg. 1972. Aerosol survival of Pasteurella tularensis and the influence of relative humidity. Appl. Microbiol. 23:1-3.
22. Dahlstrand, S., O. Ringertz, and B. Zetterberg. 1971. Airborne tularemia in Sweden. Scand. J. Infect. Dis. 3:7-16.
23. Dearmon, I. A., Jr., D. H. Lively, and N. G. Roth. 1956. Survival time as a rapid method of determining virulence with Bacillus anthracis. J. Bacteriol. 72:666-672.
24. Dearmon, I. A., Jr., M. D. Orlando, A. J. Rosenwald, F. Klein, A. L. Fernelius, R. E. Lincoln, and P. R. Middaugh. 1962. Viability and estimation of shelf-life of bacterial populations. Appl. Microbiol. 10:422-427.
25. Dewan, P. K., A. M. Fry, K. Laserson, B. C. Tierney, C. P. Quinn, J. A. Hayslett, L. N. Broyles, A. Shane, K. L. Winthrop, I. Walks, L. Siegel, T. Hales, V. A. Semenova, S. Romero-Steiner, C. Elie, R. Khabbaz, A. S. Khan, R. A. Hajjeh, and A. Schuchat. 2002. Inhal ational anthrax outbreak among postal workers, Washington, D.C., 2001. Emerg. Infect. Dis. 8:1066-1072.
26. Dragon, D. C., and R. P. Rennie. 1995. The ecology of anthrax spores: tough but not invincible. Can. Vet. J. 36:295-301.
27. Ehrlich, R., and S. Miller. 1973. Survival of airborne Pasteurella tularensis at different atmospheric temperatures. Appl. Microbiol. 25:369-372.
28. El-Olemy, G. M., A. A. Atta, W. H. Mahmoud, and E. G. Hamzah. 1984. Brucellosis in man. II. Isolation of the causative organisms with special reference to blood picture and urine constituents. Dev. Biol. Stand. 56:573-578.
29. Essbauer, S., H. Meyer, M. Porsch-Ozcurumez, and M. Pfeffer. 2007. Long-lasting stability of vaccinia virus (Orthopoxvirus) in food and environmental samples. Zoonoses Public Health 54:118-124.
30. Fennelly, K. P., A. L. Davidow, S. L. Miller, N. Connell, and J. J. Ellner. 2004. Airborne infection with Bacillus anthracis - from mills to mail. Emerg. Infect. Dis. 10:996-1002.
31. Filipkowska, Z. 2003. Sanitary and bacteriological aspects of sewage treatment. Acta Microbiol. Pol. 52(Suppl.):57-66.
32. Forsman, M., E. W. Henningson, E. Larsson, T. Johansson, and G. Sandstrom. 2000. Francisella tularensis does not manifest virulence in viable but non-culturable state. FEMS Microbiol. Ecol. 31:217-224.
33. Fulton, J. D. 1966. Microorganisms of the upper atmosphere. 3. Relationship between altitude and micropopulation. Appl. Microbiol. 14:237-240.
34. Gerba, C. P. 2000. Assessment of enteric pathogens shedding by bathers during recreational activity and its impact on water quality. Quant. Microbiol. 2:55-68.
35. Gibby, I. W., P. S. Nicholes, J. T. Tamura, and L. Foshay. 1948. The effects of an extract of blood cells upon the cultivation of Bacterium tularense in liquid media. J. Bacteriol. 55:855-863.
36. Gould, G. W. 1977. Recent advances in the understanding of resistance and dormancy in bacterial spores. J. Appl. Bacteriol. 42:297-309.
37. Graham-Smith, G. S. 1930. The longevity of dry spores of B. anthracis. J. Hyg. 30:213-215.
38. Greco, D., G. Allegrini, T. Tizzi, E. Ninu, A. Lamanna, and S. Luzi. 1987. A waterborne tularemia outbreak. Eur. J. Epidemiol. 3:35-38.
39. Hardestam, J., M. Simon, K. O. Hedlund, A. Vaheri, J. Klingstrom, and A. Lundkvist. 2007. Ex vivo stability of the rodent-borne Hantaan virus in comparison to that of arthropod-borne members of the Bunyaviridae family. Appl. Environ. Microbiol. 73:2547-2551.
40. Harper, G. J. 1961. Airborne micro-organisms: survival tests with four viruses. J. Hyg. (London) 59:479-486.
41. Harper, G. J. 1963. The influence of environment on the survival of airborne virus particles in the laboratory. Arch. Gesamte Virusforsch. 13:64-71.
42. Henderson, D. A. 2002. Bioweapons preparedness chief discusses priorities in world of 21st-century biology. Interview by Rebecca Voelker. JAMA 287:573-575.
43. Henderson, D. A., T. V. Inglesby, J. G. Bartlett, M. S. Ascher, E. Eitzen, P. B. Jahrling, J. Hauer, M. Layton, J. McDade, M. T. Osterholm, T. O'Toole, G. Parker, T. Perl, P. K. Russell, K. Tonat, et al. 1999. Smallpox as a biological weapon: medical and public health management. JAMA 281:2127-2137.
44. Holdstock, D. 2000. Biotechnology and biological warfare. Peace Rev. 12:549-553.
45. Israeli, E., J. Gitelman, and B. Lighthart. 1994. Death mechanism in microbial bioaerosols with special reference to the freeze-dried analog, p. 166-191. In B. Lighthart and A. J. Mohr (ed.), Atmospheric microbial aerosols. Chapman and Hall, New York, NY.
46. Jaax, N. K., K. J. Davis, T. J. Geisbert, P. Vogel, G. P. Jaax, M. Topper, and P. B. Jahrling. 1996. Lethal experimental infection of rhesus monkeys with Ebola-Zaire (Mayinga) virus by the oral and conjunctival route of exposure. Arch. Pathol. Lab. Med. 120:140-155.
47. Johnson, E., N. Jaax, J. White, and P. Jahrling. 1995. Lethal experimental infections of rhesus monkeys by aerosolized Ebola virus. Int. J. Exp. Pathol. 76:227-236.
48. Josko, D. 2004. Yersinia pestis: still a plague in the 21st century. Clin. Lab. Sci. 17:25-29.
49. Kallio, E. R., J. Klingstrom, E. Gustafsson, T. Manni, A. Vaheri, H. Henttonen, O. Vapalahti, and A. Lundkvist. 2006. Prolonged survival of Puumala hantavirus outside the host: evidence for indirect transmission via the environment. J. Gen. Virol. 87:2127-2134.
50. Kim, J. 1994. Atmospheric environment of bioaerosols, p. 28-67. In B. Lighthart and A. J. Mohr (ed.), Atmospheric microbial aerosols. Chapman and Hall, New York, NY.
51. Langeland, G. 1983. Yersinia enterocolitica and Yersinia enterocolitica-like bacteria in drinking water and sewage sludge. Acta Pathol. Microbiol. Immunol. Scand. Sect. B 91:179-185.
52. Larson, E. W., J. W. Dominik, and T. W. Slone. 1980. Aerosol stability and respiratory infectivity of Japanese B encephalitis virus. Infect. Immun. 30:397-401.
53. LeDuc, J. W. 1989. Epidemiology of hemorrhagic fever viruses. Rev. Infect. Dis. 11(Suppl. 4):S730-S735.
54. Lee, P. W., R. Yanagihara, C. J. Gibbs, Jr., and D. C. Gajdusek. 1986. Pathogenesis of experimental Hantaan virus infection in laboratory rats. Arch. Virol. 88:57-66.
55. Leffel, E. K., and D. S. Reed. 2004. Marburg and Ebola viruses as aerosol threats. Biosecur. Bioterror. 2:186-191.
56. Lewis, J. C. 1969. Dormancy, p. 301-358. In A. Hurst and G. W. Gould (ed.), The bacterial spore, vol. 1. Academic Press, London, United Kingdom.
57. Leyssen, P., A. Van Lommel, C. Drosten, H. Schmitz, E. De Clercq, and J. Neyts. 2001. A novel model for the study of the therapy of flavivirus infections using the Modoc virus. Virology 279:27-37.
58. Mahl, M. C., and C. Sadler. 1975. Virus survival on inanimate surfaces. Can. J. Microbiol. 21:819-823.
59. Manchee, R. J., M. G. Broster, J. Melling, R. M. Henstridge, and A. J. Stagg. 1981. Bacillus anthracis on Gruinard Island. Nature 294:254-255.
60. Mandell, G. L., R. G. Douglas, J. E. Bennett, and R. Dolin. 2005. Mandell, Douglas, and Bennett's principles and practice of infectious diseases, 6th ed. Elsevier/Churchill Livingstone, New York, NY.
61. May, K. R., H. A. Druett, and L. P. Packman. 1969. Toxicity of open air to a variety of microorganisms. Nature 221:1146-1147.
62. Miller, W. S., and M. S. Artenstein. 1967. Aerosol stability of three acute respiratory disease viruses. Proc. Soc. Exp. Biol. Med. 125:222-227.
63. Minett, F. C., and M. R. Dhanda. 1941. Multiplication of B. anthracis and Cl. chauvei in soil and water. Indian J. Vet. Sci. Anim. Husb. 11:308-328.
64. Mitscherlich, E., and E. H. Marth. 1984. Microbial survival in the environment: bacteria and rickettsiae important in human and animal health. Springer-Verlag, Berlin, Germany.
65. Monath, T. P. 1974. Lassa fever and Marburg virus disease. WHO Chron. 28:212-219.
66. Montville, T. J., R. Dengrove, T. De Siano, M. Bonnet, and D. W. Schaffner. 2005. Thermal resistance of spores from virulent strains of Bacillus anthracis and potential surrogates. J. Food Prot. 68:2362-2366.
67. Novel, R., and T. Reh. 1947. De la longevite des spores du Bacillus anthracis et de la conservation des pouvoirs pathogene et antigene. Schweiz. Z. Pathol. Bakteriol. 10:180-192.
68. Ozdemir, D., I. Sencan, A. N. Annakkaya, A. Karadenizli, E. Guclu, E. Sert, M. Emeksiz, and A. Kafali. 2007. Comparison of the 2000 and 2005 outbreaks of tularemia in the Duzce region of Turkey. Jpn. J. Infect. Dis. 60:51-52.
69. Parker, R. R., E. A. Steinhaus, G. M. Kohls, and W. L. Jellison. 1951. Contamination of natural waters and mud with Pasteurella tularensis and tularemia in beavers and muskrats in the northwestern United States. Bull. Natl. Inst. Health 193:1-161.
70. Perone, A., and L. Gelosa. 1982. Findings on the spread of anthrax spores in the provincial territory of Milan with tanneries. G. Batteriol. Virol. Immunol. 75:322-336. (In Italian.)
71. Rabey, F., R. J. Janssen, and L. M. Kelley. 1969. Stability of St. Louis encephalitis virus in the airborne state. Appl. Microbiol. 18:880-882.
72. Reshetin, V. P., and J. L. Regens. 2003. Simulation modeling of anthrax spore dispersion in a bioterrorism incident. Risk Anal. 23:1135-1145.
73. Roberts, T. A., and A. D. Hitchins. 1969. Resistance of spores, p. 611-670. In G. W. Gould and A. Hurst (ed.), The bacterial spore, vol 1. Academic Press, London, United Kingdom.
74. Rose, J. B. 2002. Water quality security. Environ. Sci. Technol. 36:246A-250A.
75. Rose, L. J., R. Donlan, S. N. Banerjee, and M. J. Arduino. 2003. Survival of Yersinia pestis on environmental surfaces. Appl. Environ. Microbiol. 69:2166-2171.
76. Rotz, L. D., A. S. Khan, S. R. Lillibridge, S. M. Ostroff, and J. M. Hughes. 2002. Public health assessment of potential biological terrorism agents. Emerg. Infect. Dis. 8:225-230.
77. Sarkar, J. K., A. C. Mitra, M. K. Mukherjee, and S. K. De. 1973. Virus excretion in smallpox. 2. Excretion in the throats of household contacts. Bull. W. H. O. 48:523-527.
78. Schmaljohn, C., and B. Hjelle. 1997. Hantaviruses: a global disease problem. Emerg. Infect. Dis. 3:95-104.
79. Sirena, S., and G. Scagliosi. 1894. Lavori e lezioni originali. Riforma Med. 2:340-343.
80. Slepecky, R. A., and E. R. Leadbetter. 1983. On the prevalence and roles of spore-forming bacteria and their spores in nature, p. 79-101. In A. Hurst and G. W. Gould (ed.), The bacterial spore, vol. 2. Academic Press, London, United Kingdom.
81. Stephenson, E. H., E. W. Larson, and J. W. Dominik. 1984. Effect of environmental factors on aerosol-induced Lassa virus infection. J. Med. Virol. 14:295-303.
82. Stuart, A. L., and D. A. Wilkening. 2005. Degradation of biological weapons agents in the environment: implications for terrorism response. Environ. Sci. Technol. 39:2736-2743.
83. Syrjala, H., P. Kujala, V. Myllyla, and A. Salminen. 1985. Airborne transmission of tularemia in farmers. Scand. J. Infect. Dis. 17:371-375.
84. Szekely, A. V. 1903. Beitrag zur Lebensdauer der Milzbrandsporen. Z. Hyg. Infectionskrankh. 44:359-363.
85. Takahashi, H., P. Keim, A. F. Kaufmann, K. L. Smith, C. Keys, K. Taniguchi, S. Inouye, and T. Kurata. 2004. Epidemiological and laboratory investigation of a Bacillus anthracis bioterrorism incident, Kameido, Tokyo, 1993. Emerg. Infect. Dis. 10:117-120.
86. Tarnvik, A., S. Lofgren, L. Ohlund, and G. Sandstrom. 1987. Detection of antigen in urine of a patient with tularemia. Eur. J. Clin. Microbiol. 6:318-319.
87. Tarnvik, A., H. S. Priebe, and R. Grunow. 2004. Tularaemia in Europe: an epidemiological overview. Scand. J. Infect. Dis. 36:350-355.
88. Turnbull, P. C. B. 2002. Anthrax history, disease and ecology. Curr. Top. Microbiol. Immunol. 271:1-19.
89. Van Ness, G. B. 1971. Ecology of anthrax. Science 172:1303-1307.
90. Vasconcelos, D., R. Barnewall, M. Babin, R. Hunt, J. Estep, C. Nielsen, R. Carnes, and J. Carney. 2003. Pathology of inhalation anthrax in cynomolgus monkeys (Macaca fascicularis). Lab. Investig. 83:1201-1209.
91. Wilkinson, T. R. 1966. Survival of bacteria on metal surfaces. Appl. Microbiol. 14:303-307.
92. Wilson, J. B., and K. E. Russell. 1964. Isolation of Bacillus anthracis from soil stored 60 years. J. Bacteriol. 87:237-238.
93. Wolff, H. L., and J. J. Croon. 1968. The survival of smallpox virus (variola minor) in natural circumstances. Bull. W. H. O. 38:492-493.
94. Won, W. D., and H. Ross. 1966. Effect of diluent and relative humidity on apparent viability of airborne Pasteurella pestis. Appl. Microbiol. 14:742-745.