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Applied and Environmental Microbiology, February 2008, p. 555-563, Vol. 74, No. 3
0099-2240/08/$08.00+0     doi:10.1128/AEM.02167-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

MINIREVIEW

Persistence of Category A Select Agents in the Environment{triangledown}

Ryan Sinclair,1* Stephanie A. Boone,2 David Greenberg,3 Paul Keim,3 and Charles P. Gerba1

Department of Soil, Water and Environmental Science, University of Arizona, Tucson, Arizona 85721,1 Southern Research Regional Research Center, Agricultural Research Service, United States Department of Agriculture, 1100 Robert E. Lee Blvd., New Orleans, Louisiana 70124,2 Department of Biological Sciences, Northern Arizona University, Flagstaff, Arizona 860113


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INTRODUCTION
 
The intentional use of biological agents as weapons could result in deaths in numbers comparable to those expected from the use of nuclear weapons. It is one of the most significant terrorism threats (16, 82) and has the potential to catalyze a general breakdown of society through a loss of human lives, food, livestock, agriculture, and economy. This form of warfare has been a threat for centuries and predates scientific understanding of microorganisms or disease (44). The biological agents used for warfare are easily produced and dispersed, have a delayed onset, cause high rates of morbidity and mortality, and present unique challenges in diagnosis, detection, and treatment (16). Biological agents are diverse and can be deployed to contaminate various environmental media including air, water, food, soil, and fomites.

The well-known global history of military biowarfare and terrorism (16, 42-44, 85) has prompted many governments to prioritize response plans for the event of a biological agent release in a bioterrorism attack (5, 74). An important component to any response plan is an understanding of the survival rate or viability of the biological agent in the surrounding environment (82). Bioterrorism events such as the "anthrax letter" attacks of 2001 (25) have highlighted that the survival and persistence of a biological agent have a significant impact on the microbial hazard and its subsequent effects. Microbial decay and injury will affect decontamination, infection rates, and encompassing geographic areas. Therefore, knowledge of microbial ecology and defensive public preparation are important factors in limiting bioterrorism-related morbidity and mortality. The Centers for Disease Control (CDC) prioritizes potential biological terrorism agents as category A if they require intensive public preparedness efforts due to the potential for mass causalities, public fear, and civil disruption (76). These category A select agents are variola major virus (smallpox), Bacillus anthracis (anthrax), Yersinia pestis (plague), Clostridium botulinum toxin (botulism), Francisella tularensis (tularemia), and the viral hemorrhagic fever agents Arenaviridae (Lassa fever, Junin-Argentine hemorrhagic fever, and Venezuelan hemorrhagic fever), Bunyaviridae (hantavirus), Filoviridae (Ebola hemorrhagic fever and Marburg hemorrhagic fever), and Flaviviridae (St. Louis encephalitis and Japanese B encephalitis).

In an intentional release, exposure may occur by routes in which the bioagent is not transmitted in nature. The potential for transmission is a function of transport and persistence in the environment, with the transport probability based upon both predicted entry ports and other portals not usually considered significant or lacking in nature. Information on the environmental persistence of these agents is limited but essential for estimating where the greatest environmental exposure may occur through a risk assessment framework.

The purpose of this review is to assess the current information on the persistence of select agents on the CDC category A agent list in the environment and its implications in a terrorism response.


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ROUTES OF EXPOSURE
 
The release of vertebrate pathogens may occur intentionally, by accident, or by natural release in the bodily fluids of those infected. All category A agents can be expected to be released in the bodily fluids of infected persons or animals (Table 1). The concentration of these agents in these materials can be significant (Table 2). Most of the agents in nature are primarily transmitted by insect vectors or through animal contact or material contaminated by infected animals. The demonstrated or suspected natural routes of transmission are shown in Table 3. For the bacteria in particular, multiple routes of transmission are possible, although some may play a minor role in nature. The agents' persistence characteristics in aerosols, fomites, and water are detailed in Tables 4, 5, and 6, respectively.


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  		TABLE 1. Occurrence of category A select agents in bodily fluids and sewagea


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  		TABLE 2. Concentration and duration of agent release


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  		TABLE 3. Vehicles for the transmission of category A agents in nature


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  		TABLE 4. Survival of category A biological agents as aerosols


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  		TABLE 5. Survival of category A biological agents on fomites


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  		TABLE 6. Survival of category A biological agents in water


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PERSISTENCE IN THE ENVIRONMENT
 
The maintenance of infectivity by any pathogen outside the host is dependent on a number of factors including temperature, relative humidity, desiccation, and UV light. Temperature has the greatest effect, since the rates of most chemical and physical processes are dependent upon it. Temperature is also the most useful parameter for modeling microbial decay rates for microbes that cannot replicate in the environment. Relative humidity (and desiccation) is also a significant factor for survival in air and on fomites (9).

For comparative purposes and to assess long-term exposure risks, we calculated inactivation coefficients (Ki) with the following calculation for the titers per unit volume (ml, g, or cubic meter of air): [log10 reduction (initial titer – final titer/volume or weight]/total hours of viability (9). Inactivation coefficients were assumed to be linear functions and were not used to calculate T90 and T99 values, which are the times required for the initial titer to decrease by 90% (T90) and 99% (T99); these values were calculated using the survival curve, which is typically not linear. Therefore, T90 and T99 values usually underestimate viral survival compared to inactivation coefficients (Ki values). We estimated these from published data tables and/or figures if available.

Aerosols.
Research on category A pathogen survival in aerosols is limited, but it is known that most biological agents, with some exceptions, face decay once exposed to air due mainly to freezing, dehydration, and UV exposure during the daylight as well as to many other contributing environmental factors (45, 50). In general, vegetative forms are much more susceptible to open-air conditions than bacterial spores (Tables 4 and 7) (36, 73, 80).


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  		TABLE 7. Nonkinetic studies on survival of Bacillus anthracis (virulent strains) in the environment

B. anthracis in its vegetative form usually will not survive for long outside of a host and will form spores when exposed to oxygen (26, 88). Early studies on anthrax spores demonstrated very long survival times (Table 7). One limited study examined the survival of anthrax spores in outdoor air and showed that B. anthracis spores retained complete viability when exposed for several hours during the nighttime (61). This finding is expected, as spores are highly resistant structures and are at least 10-fold more resistant at night than during the day (82). Additional studies examined air for B. anthracis spores and reported viable DNA over several U.S. cites and in the upper atmosphere (15, 33, 60). Other studies of survivability in water and on fomites suggest that the aerosol survival of B. anthracis spores could be long (24). Many other modeling studies, animal dose-response models, epidemiological studies, and studies with surrogate organisms (11, 12, 30, 72, 90) that reveal qualitative information related to B. anthracis survival in air are available, but experimental evidence is lacking or is classified.

Y. pestis exhibited a constant decay rate when it was aerosolized at an rH of 50% in heart infusion broth (94). An abrupt loss of viable organisms occurs when rH rises above 50%, especially to 85%. F. tularensis responded similarly by having the lowest survival at a high rH. Additional studies found that the effect of temperature on survival is linear when the rH is above 85%.

Many of the studies on viral survival exhibited an initial log die-off within the first few minutes of aerosolization. Vaccinia virus behaved in this manner, but ultimate survival was determined by rH and temperature. The T99 was about 9 h even under the most challenging rH and temperature (40, 41). Because the Lassa fever virus can be present in pharyngeal secretions and urine for up to 3 to 4 weeks after a patient's clinical signs have subsided (65), there is a long window in which the infective virions can become airborne. An aerosol study found that 75% of the virus was infective after 4 min at 24°C (81). The Ebola and Marburg filoviruses are not typically transmitted by aerosols, but laboratory studies with monkeys demonstrate that the disease could potentially be transmitted through respirable particles (46, 47, 55). Epidemiological investigations have found that most human cases occurred due to direct contact with blood, secretions, or tissues of infected patients or nonhuman primates (6, 10, 53). The survival of Japanese B encephalitis virus was shown to be inversely related to rH (52), with longer survival times at lower levels. A study on the St. Louis encephalitis virus, another major flavivirus, found different results; no loss of titer was associated with differences in rH (71).

Limited studies have verified the stability of hantavirus in air, while epidemiological studies have characterized disease transmission to humans as through wounds or inhalation of aerosolized rodent excreta (78).

Fomites.
Studies detailing the survival of category A agents on fomites describe surface characteristics, rH, and temperature as major contributors to viability (Table 5) (9). Stainless steel, polyethylene, glass, and paper were assessed for Y. pestis survivability. It was found that these pneumonic plague bacteria remained viable much longer on paper, potentially due to surface roughness and hydrophobicity (75). The smallpox virus was less sensitive to differences in surface and environment; it remained viable for up to 2 weeks on fomites with various rH values, temperatures, and surface textures (58). Three Bunyaviridae hemorrhagic fever viruses, Hantaan virus, Sicilian virus, and Crimean-Congo virus, showed various survival times on aluminum discs, with the Sicilian fever virus exhibiting a T99 of up to 2.2 h (39).

Knowledge of survival of B. anthracis on fomites is fairly limited. Several studies have revived spores dried on filter paper after 35 and 41 years (67). Another study recovered anthrax spores from canvas after 22 years (37).

Water.
Most of the research on pathogen survival in water has been on waterborne pathogens, i.e., those transmitted by the fecal oral route (Tables 6 and 7). Humans and animals are the natural hosts of these pathogens, which normally cannot replicate in the environment. Of all the category A select agents, only B. anthracis and F. tularensis are capable of replication in the environment. However, all of the agents may be excreted in the feces and urine; thus, they are likely to end up in sewage systems or in water during recreational (34) activities. This appears to be the least studied area on environmental survival of category A select agents.

Waterborne outbreaks of F. tularensis have been documented (38, 68, 87). F. tularensis type A has been isolated from natural waters and mud contaminated by muskrats and beavers (69), and the organisms may be capable of multiplication in these environments (35, 69). F. tularensis type B has also been isolated from surface waters, including drinking water supplies (22, 83). An additional study found that the vaccine strain could persist for at least 40 days at 8°C in tap water (32). However, the organisms entered a viable but nonculturable (VBNC) stage, and 65% of the original inoculum remained viable after 140 days. The VBNC organisms were not capable of causing tularemia in mice. The organism is also known to replicate intracellularly in protozoa similarly to the water-based pathogen Legionella, and this could act to serve as a reservoir in aquatic environments or at least prolong its persistence (1).

Y. pestis is also capable of transmission by inhalation of aerosol (48). It has been reported to enter the VBNC state when added to deionized water at 28 and 37°C (4) and may be capable of persisting in cysts of amoebas (3). It was reported to survive 16 days in tap water and well water (64) and has been detected in sewage (31).

Early studies show that vegetative B. anthracis dies after only 72 h in distilled water (17) or has a maximum survival of 6 days in water (64). There is a controversy as to the life cycle of B. anthracis in water (26, 63, 88, 89). Contrarily, B. anthracis spores can survive for a much longer time in water. Some suggest that because large herbivores can become infected through ingestion of spores at drying water holes in Africa, it is possible that humans could also contract the illness via water (19). Unfortunately, most information describing the longevity of spores in water is from the early 1900s and lacks detailed descriptions of procedures or lacks data on initial and final concentrations. Recent data extrapolation calculates that B. anthracis spores will survive for 620 years at room temperature; however, this assumes a linear relation to survival at decreasing temperatures (23, 24). There are also data on spore survival in water for species taxonomically close to B. anthracis, and this information can be used to extrapolate the behavior of B. anthracis (64, 80); however, actual experimental evidence using B. anthracis is very limited. Table 7 shows some of the limited data available on B. anthracis survival.

Hantavirus is excreted in the urine and saliva of rodents and may contaminate water, although waterborne transmission is unproven. A recent study investigated the survival of hantavirus and related arthropod-borne members of the Bunyaviridae family in cell culture media at various temperatures (39). A 99.9% decrease in virus titer at 20°C required about 20 days. The most stable of the viruses studied was the Sicilian virus, carried by the sand fly; this virus showed little inactivation after 10 days at 20°C.

Data on the stability of smallpox virus come largely from studies of scabs, vesicles, and bodily fluids (29, 93). Most of the useful studies have been conducted with vaccinia virus, a genetically related virus in the smallpox vaccine. The genus Orthopoxvirus is a very stable group of viruses. Little is known about the stability of the arenaviruses and flaviviruses in water or other liquids because they are not known to be naturally transmitted by this route. The flavivirus yellow fever virus, when reconstituted from a vaccine, was able to survive for several days at 37°C (2).

Soil.
Bacillus species spores have been found and revived from sediments perhaps as old as 1,000 years and some have claimed from Paleozoic salt beds (80). Viable spores of B. anthracis have been found after 40 years on Gruinard Island (59), and Lewis reported on recovered viable spores from sealed soil samples stored for 60 and 68 years (56). As soil is part of the organism's ecological life cycle, it is expected that spores persist in particular types of soil for many years, where they may germinate and multiply (26, 88, 89). Table 7 shows that some spores can remain viable in soil for many decades.

Soil moisture and organic matter content are important to the survival of Y. pestis. In soil, Y. pestis may multiply under favorable soil conditions and will survive for more than 10 months in soil at 4 to 8°C and for 3.5 months at room temperature (13, 14, 64).


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DISCUSSION
 
Exposure is critical to estimating the risk posed by pathogens capable of environmental transmission and creates the greatest amount of uncertainty in estimating the risk of infection to exposed populations (34). Models can be developed to predict exposure after the release of a pathogen in the environment, but die-off or decay rates are critical in this estimation. To have the greatest utility, die-off rates (Ki) need to be as quantitative as possible. This review reveals that information appears to be very limited for select agents in category A. Because no investigators have appeared to use similar methods, data comparison between groups of organisms is of limited value. The development of standardized testing methods and conditions for assessing survival would be of the most value. Consideration must also be given to the usual multiphasic die-off rates, or otherwise they may be underestimated. For example, die-off of organisms is usually most rapid during aerosolization or drying on fomites.

With the limited database, it is difficult to make generalizations; however, it appears overall that the greatest stability of the select agents was seen for liquid environments (Table 6) and the least for aerosols. Desiccation during aerosolization and drying on fomites were major factors contributing to the steep initial die-off trends for fomite and aerosol environments. The viruses were generally more stable in aerosols than were the other agents, except for the spores of B. anthracis. F. tularensis was the most stable non-spore-forming organism in water, reflecting its potential to grow in this environment. Vaccinia virus and B. anthracis were the most environmentally stable agents overall.

The available data would suggest that the greater long-term exposure to agents once released into the environment would be from water or fomites. In these media, agents will persist longer than in aerosols and present the greater hazard. Also, aerosols are usually only a transitory medium for these agents in nature, as the organisms quickly settle out. The potential for resuspension into the aerosol state is largely governed by the potential for survival on a fomite or in a liquid that may be aerosolized. Overall, further survival studies need to be conducted on all category A select agents within the context of human exposure to liquid, soil, fomites, and aerosols.


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ACKNOWLEDGMENTS
 
This study was supported by the Center for Advancing Microbial Risk Assessment funded by the U.S. Environmental Protection Agency Science to Achieve Results program and U.S. Department of Homeland Security University Programs grant number R3236201. Ryan Sinclair was supported through the National Research Council's Research Associate Program with funding from the U.S. Department of Homeland Security.


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FOOTNOTES
 
* Corresponding author. Mailing address: University of Arizona, 2601 E. Airport Drive, Tucson, AZ 85706. Phone: (520) 626-2656. Fax: (520) 573-0852. E-mail: ryans{at}email.arizona.edu Back

{triangledown} Published ahead of print on 7 December 2007. Back


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REFERENCES
 
    1
  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.[Abstract/Free Full Text]
    2. 2
  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.[CrossRef][Medline]
    3. 3
  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. 4
  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. 5
  5. Atlas, R. M. 2002. Responding to the threat of bioterrorism: a microbial ecology perspective—a case of anthrax. Int. Microbiol. 5:161-167.[CrossRef][Medline]
    6. 6
  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.[Medline]
    7. 7
  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.)[Medline]
    8. 8
  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.[Medline]
    9. 9
  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.[Free Full Text]
    10. 10
  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.[Abstract/Free Full Text]
    11. 11
  11. Brachman, P. S., A. F. Kaufman, and F. G. Dalldorf. 1966. Industrial inhalation anthrax. Bacteriol. Rev. 30:646-659.[Free Full Text]
    12. 12
  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.[Abstract/Free Full Text]
    13. 13
  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. 14
  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. 15
  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.[Abstract/Free Full Text]
    16. 16
  16. Broussard, L. A. 2001. Biological agents: weapons of warfare and bioterrorism. Mol. Diagn. 6:323-333.[CrossRef][Medline]
    17. 17
  17. Busson, B. 1911. Ein Beitrag zur Kenntnis der Lebensdauer von Bacterium coli und Milzbrandsporen. Zentralbl. Bakteriol. Parasitenkd. Infektionskr. 58:505-509.
    18. 18
  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.)[Medline]
    19. 19
  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. 20
  20. Cox, C. S. 1971. Aerosol survival of Pasteurella tularensis disseminated from the wet and dry states. Appl. Microbiol. 21:482-486.[Medline]
    21. 21
  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.[Medline]
    22. 22
  22. Dahlstrand, S., O. Ringertz, and B. Zetterberg. 1971. Airborne tularemia in Sweden. Scand. J. Infect. Dis. 3:7-16.[Medline]
    23. 23
  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.[Free Full Text]
    24. 24
  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.[Medline]
    25. 25
  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. Inhalational anthrax outbreak among postal workers, Washington, D.C., 2001. Emerg. Infect. Dis. 8:1066-1072.[Medline]
    26. 26
  26. Dragon, D. C., and R. P. Rennie. 1995. The ecology of anthrax spores: tough but not invincible. Can. Vet. J. 36:295-301.[Medline]
    27. 27
  27. Ehrlich, R., and S. Miller. 1973. Survival of airborne Pasteurella tularensis at different atmospheric temperatures. Appl. Microbiol. 25:369-372.[Medline]
    28. 28
  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.[Medline]
    29. 29
  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.[CrossRef][Medline]
    30. 30
  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.[Medline]
    31. 31
  31. Filipkowska, Z. 2003. Sanitary and bacteriological aspects of sewage treatment. Acta Microbiol. Pol. 52(Suppl.):57-66.[Medline]
    32. 32
  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.[CrossRef][Medline]
    33. 33
  33. Fulton, J. D. 1966. Microorganisms of the upper atmosphere. 3. Relationship between altitude and micropopulation. Appl. Microbiol. 14:237-240.[Medline]
    34. 34
  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.[CrossRef]
    35. 35
  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.[Free Full Text]
    36. 36
  36. Gould, G. W. 1977. Recent advances in the understanding of resistance and dormancy in bacterial spores. J. Appl. Bacteriol. 42:297-309.[Medline]
    37. 37
  37. Graham-Smith, G. S. 1930. The longevity of dry spores of B. anthracis. J. Hyg. 30:213-215.
    38. 38
  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.[CrossRef][Medline]
    39. 39
  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.[Abstract/Free Full Text]
    40. 40
  40. Harper, G. J. 1961. Airborne micro-organisms: survival tests with four viruses. J. Hyg. (London) 59:479-486.[Medline]
    41. 41
  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.[CrossRef][Medline]
    42. 42
  42. Henderson, D. A. 2002. Bioweapons preparedness chief discusses priorities in world of 21st-century biology. Interview by Rebecca Voelker. JAMA 287:573-575.[Free Full Text]
    43. 43
  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.[Abstract/Free Full Text]
    44. 44
  44. Holdstock, D. 2000. Biotechnology and biological warfare. Peace Rev. 12:549-553.[CrossRef]
    45. 45
  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. 46
  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.[Medline]
    47. 47
  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.[Medline]
    48. 48
  48. Josko, D. 2004. Yersinia pestis: still a plague in the 21st century. Clin. Lab. Sci. 17:25-29.[Medline]
    49. 49
  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.[Abstract/Free Full Text]
    50. 50
  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. 51
  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.[Medline]
    52. 52
  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.[Abstract/Free Full Text]
    53. 53
  53. LeDuc, J. W. 1989. Epidemiology of hemorrhagic fever viruses. Rev. Infect. Dis. 11(Suppl. 4):S730-S735.[Medline]
    54. 54
  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.[CrossRef][Medline]
    55. 55
  55. Leffel, E. K., and D. S. Reed. 2004. Marburg and Ebola viruses as aerosol threats. Biosecur. Bioterror. 2:186-191.[CrossRef][Medline]
    56. 56
  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. 57
  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.[CrossRef][Medline]
    58. 58
  58. Mahl, M. C., and C. Sadler. 1975. Virus survival on inanimate surfaces. Can. J. Microbiol. 21:819-823.[Medline]
    59. 59
  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.[CrossRef][Medline]
    60. 60
  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. 61
  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.[CrossRef][Medline]
    62. 62
  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.[CrossRef][Medline]
    63. 63
  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. 64
  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. 65
  65. Monath, T. P. 1974. Lassa fever and Marburg virus disease. WHO Chron. 28:212-219.[Medline]
    66. 66
  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.[Medline]
    67. 67
  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.[CrossRef]
    68. 68
  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.[Medline]
    69. 69
  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.[Medline]
    70. 70
  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.)[Medline]
    71. 71
  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.[Medline]
    72. 72
  72. Reshetin, V. P., and J. L. Regens. 2003. Simulation modeling of anthrax spore dispersion in a bioterrorism incident. Risk Anal. 23:1135-1145.[CrossRef][Medline]
    73. 73
  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. 74
  74. Rose, J. B. 2002. Water quality security. Environ. Sci. Technol. 36:246A-250A.[Medline]
    75. 75
  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.[Abstract/Free Full Text]
    76. 76
  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.[Medline]
    77. 77
  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.[Medline]
    78. 78
  78. Schmaljohn, C., and B. Hjelle. 1997. Hantaviruses: a global disease problem. Emerg. Infect. Dis. 3:95-104.[Medline]
    79. 79
  79. Sirena, S., and G. Scagliosi. 1894. Lavori e lezioni originali. Riforma Med. 2:340-343.
    80. 80
  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. 81
  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.[Medline]
    82. 82
  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.[Medline]
    83. 83
  83. Syrjala, H., P. Kujala, V. Myllyla, and A. Salminen. 1985. Airborne transmission of tularemia in farmers. Scand. J. Infect. Dis. 17:371-375.[Medline]
    84. 84
  84. Szekely, A. V. 1903. Beitrag zur Lebensdauer der Milzbrandsporen. Z. Hyg. Infectionskrankh. 44:359-363.[CrossRef]
    85. 85
  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.[Medline]
    86. 86
  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.[Medline]
    87. 87
  87. Tarnvik, A., H. S. Priebe, and R. Grunow. 2004. Tularaemia in Europe: an epidemiological overview. Scand. J. Infect. Dis. 36:350-355.[CrossRef][Medline]
    88. 88
  88. Turnbull, P. C. B. 2002. Anthrax history, disease and ecology. Curr. Top. Microbiol. Immunol. 271:1-19.[Medline]
    89. 89
  89. Van Ness, G. B. 1971. Ecology of anthrax. Science 172:1303-1307.[Free Full Text]
    90. 90
  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.[CrossRef][Medline]
    91. 91
  91. Wilkinson, T. R. 1966. Survival of bacteria on metal surfaces. Appl. Microbiol. 14:303-307.[Medline]
    92. 92
  92. Wilson, J. B., and K. E. Russell. 1964. Isolation of Bacillus anthracis from soil stored 60 years. J. Bacteriol. 87:237-238.[Free Full Text]
    93. 93
  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.[Medline]
    94. 94
  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.[Medline]

Applied and Environmental Microbiology, February 2008, p. 555-563, Vol. 74, No. 3
0099-2240/08/$08.00+0     doi:10.1128/AEM.02167-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.



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