Implications of limits of detection of various methods for Bacillus anthracis in computing risks to human health

Applied and Environmental Microbiology

Volumn 75, Issue 19, 2009, Pages 6331-6339

  Herzog, Amanda B ^a,b   McLennan, S Devin ^b   Pandey, Alok K ^a,b   Gerba, Charles P ^b,d   Haas, Charles N ^b,c   Rose, Joan B ^b   Hashsham, Syed A ^a,b  

^a Michigan State University   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c Drexel University   (United States)

^d UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRACIS; BACILLUS ANTHRACIS; BIOCHIP SYSTEMS; BIOLOGICAL WARFARES; CURRENT LIMITATION; DESCRIPTIVE STATISTICS; DETECTION APPROACH; DETECTION METHODS; DOSE-RESPONSE MODELS; ENVIRONMENTAL MATRIXES; ENVIRONMENTAL MONITORING; ENVIRONMENTAL SAMPLE; ENZYME LINKED IMMUNOSORBENT ASSAY; FIRST RESPONDERS; HUMAN HEALTH; JOURNAL ARTICLES; LIMIT OF DETECTION; LIMITS OF DETECTION; LITERATURE REVIEWS; QUANTITATIVE RISK ASSESSMENT; REAL-TIME PCR; SENSITIVE METHOD;

BACTERIOLOGY; HEALTH RISKS; RISK MANAGEMENT; RISK PERCEPTION; STAINLESS STEEL;

RISK ASSESSMENT;

BACTERIUM; BIOLOGICAL WEAPON; CLEANUP; DETECTION METHOD; DOSE-RESPONSE RELATIONSHIP; ENVIRONMENTAL MONITORING; HEALTH RISK; MORTALITY RISK; POLYMERASE CHAIN REACTION; PUBLIC HEALTH; RISK ASSESSMENT;

ARTICLE; BACILLUS ANTHRACIS; BACTERIUM DETECTION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FOMITE; IMMUNOASSAY; MODEL; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; RISK ASSESSMENT; SENSITIVITY AND SPECIFICITY;

BACILLUS ANTHRACIS; BACTERIOLOGICAL TECHNIQUES; ENVIRONMENTAL MICROBIOLOGY; HUMANS; POLYMERASE CHAIN REACTION; RISK ASSESSMENT; SENSITIVITY AND SPECIFICITY;

BACILLUS ANTHRACIS;

EID: 70349422227     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00288-09     Document Type: Article

References (78)

1. Acharya, G., D. D. Doorneweerd, C. L. Chang, W. A. Henne, P. S. Low, and C. A. Savran. 2007. Label-free optical detection of anthrax-causing spores. J. Am. Chem. Soc. 129:732-733.
2. Agarwal, G. S., D. V. Kamboj, S. I. Alam, M. Dixit, and L. Singh. 2002. Environmental detection of Bacillus anthracis spores. Curr. Sci. 83:697-699.
3. Baeumner, A. J., J. Pretz, and S. Fang. 2004. A universal nucleic acid sequence biosensor with nanomolar detection limits. Anal. Chem. 76:888-894.
4. Bartrand, T. A., M. H. Weir, and C. N. Haas. 2008. Dose-response models for inhalation of Bacillus anthracis spores: interspecies comparisons. Risk Anal. 28:1115-1124.
5. Belgrader, P., W. Benett, D. Hadley, G. Long, R. Mariella, F. Milanovich, S. Nasarabadi, W. Nelson, J. Richards, and P. Stratton. 1998. Rapid pathogen detection using a microchip PCR array instrument. Clin. Chem. 44:2191-2194.
6. Belgrader, P., C. J. Elkin, S. B. Brown, S. N. Nasarabadi, R. G. Langlois, F. P. Milanovich, B. W. Colston, and G. D. Marshall. 2003. A reusable flow-through polymerase chain reaction instrument for the continuous monitoring of infectious biological agents. Anal. Chem. 75:3446-3450.
7. Bell, C. A., J. R. Uhl, T. L. Hadfield, J. C. David, R. F. Meyer, T. F. Smith, and F. R. Cockerill. 2002. Detection of Bacillus anthracis DNA by Light-Cycler PCR. J. Clin. Microbiol. 40:2897-2902.
8. Beverly, M. B., F. Basile, K. J. Voorhees, and T. L. Hadfield. 1996. A rapid approach for the detection of dipicolinic acid in bacterial spores using pyrolysis mass spectrometry. Rapid Commun. Mass Spectrom. 10:455-458.
9. Beverly, M. B., K. J. Voorhees, and T. L. Hadfield. 1999. Direct mass spectrometric analysis of Bacillus spores. Rapid Commun. Mass Spectrom. 13:2320-2326.
10. Beyer, W., S. Pocivalsek, and R. Bohm. 1999. Polymerase chain reaction-ELISA to detect Bacillus anthracis from soil samples - limitations of present published primers. J. Appl. Microbiol. 87:229-236.
11. Bode, E., W. Hurtle, and D. Norwood. 2004. Real-time PCR assay for a unique chromosomal sequence of Bacillus anthracis. J. Clin. Microbiol. 42:5825-5831.
12. Borthwick, K. A. J., T. E. Love, M. B. McDonnell, and W. T. Coakley. 2005. Improvement of immunodetection of bacterial spore antigen by ultrasonic cavitation. Anal. Chem. 77:7242-7245.
13. Brightwell, C., M. Pearce, and D. Leslie. 1998. Development of internal controls for PCR detection of Bacillus anthracis. Mol. Cell. Probes 12:367-377.
14. Brown, G. S., R. G. Betty, J. E. Brockmann, D. A. Lucero, C. A. Souza, K. S. Walsh, R. M. Boucher, M. Tezak, and M. C. Wilson. 2007. Evaluation of vacuum filter sock surface sample collection method for Bacillus spores from porous and non-porous surfaces. J. Environ. Monit. 9:666-671.
15. Brown, G. S., R. G. Betty, J. E. Brockmann, D. A. Lucero, C. A. Souza, K. S. Walsh, R. M. Boucher, M. Tezak, M. C. Wilson, and T. Rudolph. 2007. Evaluation of a wipe surface sample method for collection of Bacillus spores from nonporous surfaces. Appl. Environ. Microbiol. 73:706-710.
16. Brown, G. S., R. G. Betty, J. E. Brockmann, D. A. Lucero, C. A. Souza, K. S. Walsh, R. M. Boucher, M. Tezak, M. C. Wilson, T. Rudolph, H. D. A. Lindquist, and K. F. Martinez. 2007. Evaluation of rayon swab surface sample collection method for Bacillus spores from nonporous surfaces. J. Appl. Microbiol. 103:1074-1080.
17. Bruno, J. G., and J. L. Kiel. 1999. In vitro selection of DNA aptamers to anthrax spores with electrochemiluminescence detection. Biosens. Bioelectron. 14:457-464.
18. Bruno, J. G., and H. Yu. 1996. Immunomagnetic-electrochemiluminescent detection of Bacillus anthracis spores in soil matrices. Appl. Environ. Microbiol. 62:3474-3476.
19. Burton, J. E., J. Oshota, E. North, M. J. Hudson, N. Polyanskaya, J. Brehm, G. Lloyd, and N. J. Silman. 2005. Development of a multipathogen oligonucleotide microarray for detection of Bacillus anthracis. Mol. Cell. Probes 19:349-357.
20. Buttner, M. P., P. Cruz, L. D. Stetzenbach, A. K. Klima-Comba, V. L. Stevens, and P. A. Emanuel. 2004. Evaluation of the biological sampling kit (BiSKit) for large-area surface sampling. Appl. Environ. Microbiol. 70:7040-7045.
21. Campbell, G. A., and R. Mutharasan. 2007. Method of measuring Bacillus anthracis spores in the presence of copious amounts of Bacillus thuringiensis and Bacillus cereus. Anal. Chem. 79:1145-1152.
22. Campbell, G. A., and R. Mutharasan. 2006. Piezoelectric-excited millimeter-sized cantilever (PEMC) sensors detect Bacillus anthracis at 300 spores/mL. Biosens. Bioelectron. 21:1684-1692.
23. Charrel, R. N., B. La Scola, and D. Raoult. 2004. Multi-pathogens sequence containing plasmids as positive controls for universal detection of potential agents of bioterrorism. BMC Microbiol. 4:21.
24. Cheun, H. I., S. I. Makino, M. Watarai, J. Erdenebaatar, K. Kawamoto, and I. Uchida. 2003. Rapid and effective detection of anthrax spores in soil by PCR. J. Appl. Microbiol. 95:728-733.
25. Christensen, D. R., L. J. Hartman, B. M. Loveless, M. S. Frye, M. A. Shipley, D. L. Bridge, M. J. Richards, R. S. Kaplan, J. Garrison, C. D. Baldwin, D. A. Kulesh, and D. A. Norwood. 2006. Detection of biological threat agents by real-time PCR: comparison of assay performance on the RAPID, the Light-Cycler, and the smart cycler platforms. Clin. Chem. 52:141-145.
26. Dang, J. L., K. Heroux, J. Kearney, A. Arasteh, M. Gostomski, and P. A. Emanuel. 2001. Bacillus spore inactivation methods affect detection assays. Appl. Environ. Microbiol. 67:3665-3670.
27. Ellerbrok, H., H. Nattermann, M. Ozel, L. Beutin, B. Appel, and G. Pauli. 2002. Rapid and sensitive identification of pathogenic and apathogenic Bacillus anthracis by real-time PCR. FEMS Microbiol. Lett. 214:51-59.
28. English, R. D., B. Warscheid, C. Fenselau, and R. J. Cotter. 2003. Bacillus spore identification via proteolytic peptide mapping with a miniaturized MALDI TOF mass spectrometer. Anal. Chem. 75:6886-6893.
29. Farrell, S., H. B. Halsall, and W. R. Heineman. 2005. Bacillus globigii bugbeads: a model simulant of a bacterial spore. Anal. Chem. 77:549-555.
30. Farrell, S., H. B. Halsall, and W. R. Heineman. 2005. Immunoassay for B-globigii spores as a model for detecting B-anthracis spores in finished water. Analyst 130:489-497.
31. Fasanella, A., S. Losito, R. Adone, F. Ciuchini, T. Trotta, S. A. Altamura, D. Chiocco, and G. Ippolito. 2003. PCR assay to detect Bacillus anthracis spores in heat-treated specimens. J. Clin. Microbiol. 41:896-899.
32. Floriano, P. N., N. Christodoulides, D. Romanovicz, B. Bernard, G. W. Simmons, M. Cavell, and J. T. McDevitt. 2005. Membrane-based on-line optical analysis system for rapid detection of bacteria and spores. Biosens. Bioelectron. 20:2079-2088.
33. Fujinami, Y., Y. Hirai, I. Sakai, M. Yoshino, and J. Yasuda. 2007. Sensitive detection of Bacillus anthracis using a binding protein originating from gammaphage. Microbiol. Immunol. 51:163-169.
34. Gatto-Menking, D. L., H. Yu, J. G. Bruno, M. T. Goode, M. Miller, and A. W. Zulich. 1995. Sensitive detection of biotoxoids and bacterial spores using an immunomagnetic electrochemiluminescence sensor. Biosens. Bioelectron. 10:501-507.
35. Haas, C. N., J. B. Rose, and C. P. Gerba. 1999. Quantitative microbial risk assessment. John Wiley & Sons Inc., New York, NY.
36. Hartley, H. A., and A. J. Baeumner. 2003. Biosensor for the specific detection of a single viable B-anthracis spore. Anal. Bioanal. Chem. 376:319-327.
37. Haynes, C. L., C. R. Yonzon, X. Y. Zhang, and R. P. Van Duyne. 2005. Surface-enhanced Raman sensors: early history and the development of sensors for quantitative biowarfare agent and glucose detection. J. Raman Spectrosc. 36:471-484.
38. Hodges, L. R., L. J. Rose, A. Peterson, J. Noble-Wang, and M. J. Arduino. 2006. Evaluation of a macrofoam swab protocol for the recovery of Bacillus anthracis spores from a steel surface. Appl. Environ. Microbiol. 72:4429-4430.
39. Hoffmaster, A. R., R. F. Meyer, M. P. Bowen, C. K. Marston, R. S. Weyant, K. Thurman, S. L. Messenger, E. E. Minor, J. M. Winchell, M. V. Rassmussen, B. R. Newton, J. T. Parker, W. E. Morrill, N. McKinney, G. A. Barnett, J. J. Sejvar, J. A. Jernigan, B. A. Perkins, and T. Popovic. 2002. Evaluation and validation of a real-time polymerase chain reaction assay for rapid identification of Bacillus anthracis. Emerg. Infect. Dis. 8:1178-1182. (Pubitemid 35257012)
40. Hoile, R., M. Yuen, G. James, and G. L. Gilbert. 2007. Evaluation of the rapid analyte measurement platform (RAMP) for the detection of Bacillus anthracis at a crime scene. Forensic Sci. Int. 171:1-4.
41. Hurtle, W., E. Bode, D. A. Kulesh, R. S. Kaplan, J. Garrison, D. Bridge, M. House, M. S. Frye, B. Loveless, and D. Norwood. 2004. Detection of the Bacillus anthracis gyrA gene by using a minor groove binder probe. J. Clin. Microbiol. 42:179-185.
42. Kim, K., J. Seo, K. Wheeler, C. Park, D. Kim, S. Park, W. Kim, S. I. Chung, and T. Leighton. 2005. Rapid genotypic detection of Bacillus anthracis and the Bacillus cereus group by multiplex real-time PCR melting curve analysis. FEMS Immunol. Med. Microbiol. 43:301-310.
43. Krebs, M. D., A. M. Zapata, E. G. Nazarov, R. A. Miller, I. S. Costa, A. L. Sonenshein, and C. E. Davis. 2005. Detection of biological and chemical agents using differential mobility spectrometry (DMS) technology. IEEE Sens. J. 5:696-703.
44. Kuske, C. R., K. L. Banton, D. L. Adorada, P. C. Stark, K. K. Hill, and P. J. Jackson. 1998. Small-scale DNA sample preparation method for field PCR detection of microbial cells and spores in soil. Appl. Environ. Microbiol. 64:2463-2472.
45. Lee, M. A., G. Brightwell, D. Leslie, H. Bird, and A. Hamilton. 1999. Fluorescent detection techniques for real-time multiplex strand specific detection of Bacillus anthracis using rapid PCR. J. Appl. Microbiol. 87:218-223.
46. Lee, S. H., D. D. Stubbs, J. Cairney, and W. D. Hunt. 2005. Rapid detection of bacterial spores using a quartz crystal microbalance (QCM) immunoassay. IEEE Sens. J. 5:737-743.
47. Lester, E. D., G. Bearman, and A. Ponce. 2004. A second-generation anthrax "smoke detector." IEEE Eng. Med. Biol. Mag. 23:130-135.
48. Merrill, L., J. Richardson, C. R. Kuske, and J. Dunbar. 2003. Fluorescent heteroduplex assay for monitoring Bacillus anthracis and close relatives in environmental samples. Appl. Environ. Microbiol. 69:3317-3326.
49. Moser, M. J., D. R. Christensen, D. Norwood, and J. R. Prudent. 2006. Multiplexed detection of anthrax-related toxin genes. J. Mol. Diagn. 8:89-96.
50. Nubel, U., P. M. Schmidt, E. Reiss, F. Bier, W. Beyer, and D. Naumann. 2004. Oligonucleotide microarray for identification of Bacillus anthracis based on intergenic transcribed spacers in ribosomal DNA. FEMS Microbiol. Lett. 240:215-223.
51. Pai, S., A. D. Ellington, and M. Levy. 2005. Proximity ligation assays with peptide conjugate 'burrs' for the sensitive detection of spores. Nucleic Acids Res. 33:e162.
52. Pal, S., E. C. Alocilja, and F. P. Downes. 2007. Nanowire labeled directcharge transfer biosensor for detecting Bacillus species. Biosens. Bioelectron. 22:2329-2336.
53. Patra, G., L. E. Williams, Y. Qi, S. Rose, R. Redkar, and V. G. DelVecchio. 2002. Rapid genotyping of Bacillus anthracis strains by real-time polymerase chain reaction. Ann. N. Y. Acad. Sci. 969:106-111.
54. Perez, A., C. Hohn, and J. Higgins. 2005. Filtration methods for recovery of Bacillus anthracis spores spiked into source and finished water. Water Res. 39:5199-5211.
55. Premasiri, W. R., D. T. Moir, M. S. Klempner, N. Krieger, G. Jones, and L. D. Ziegler. 2005. Characterization of the surface enhanced Raman scattering (SERS) of bacteria. J. Phys. Chem. B 109:312-320.
56. Qi, Y. A., G. Patra, X. D. Liang, L. E. Williams, S. Rose, R. J. Redkar, and V. G. DelVecchio. 2001. Utilization of the rpoB gene as a specific chromosomal marker for real-time PCR detection of Bacillus anthracis. Appl. Environ. Microbiol. 67:3720-3727.
57. Reif, T. C., M. Johns, S. D. Pillai, and M. Carl. 1994. Identification of capsule-forming Bacillus anthracis spores with the PCR and a novel dual-probe hybridization format. Appl. Environ. Microbiol. 60:1622-1625.
58. Reiman, R. W., D. H. Atchley, and K. J. Voorhees. 2007. Indirect detection of Bacillus anthracis using real-time PCR to detect amplified gamma phage DNA. J. Microbiol. Methods 68:651-653.
59. Rose, L., B. Jensen, A. Peterson, S. N. Banerjee, and M. J. Arduino. 2004. Swab materials and Bacilius anthracis spore recovery from nonporous surfaces. Emerg. Infect. Dis. 10:1023-1029.
60. Ryu, C., K. Lee, C. Yoo, W. K. Seong, and H. B. Oh. 2003. Sensitive and rapid quantitative detection of anthrax spores isolated from soil samples by realtime PCR. Microbiol. Immunol. 47:693-699.
61. Sanderson, W. T., M. J. Hein, L. Taylor, B. D. Curwin, G. M. Kinnes, T. A. Seitz, T. Popovic, H. T. Holmes, M. E. Kellum, S. K. McAllister, D. N. Whaley, E. A. Tupin, T. Walker, J. A. Freed, D. S. Small, B. Klusaritz, and J. H. Bridges. 2002. Surface sampling methods for Bacillus anthracis spore contamination. Emerg. Infect. Dis. 8:1145-1151.
62. 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.
63. Sjostedt, A., U. Eriksson, V. Ramisse, and H. Garrigue. 1997. Detection of Bacillus anthracis spores in soil by PCR. FEMS Microbiol. Ecol. 23:159-168.
64. Song, L. N., S. Ahn, and D. R. Walt. 2005. Detecting biological warfare agents. Emerg. Infect. Dis. 11:1629-1632.
65. Stopa, P. J. 2000. The flow cytometry of Bacillus anthracis spores revisited. Cytometry 41:237-244.
66. Stratis-Cullum, D. N., G. D. Griffin, J. Mobley, A. A. Vass, and T. Vo-Dinh. 2003. A miniature biochip system for detection of aerosolized Bacillus globigii spores. Anal. Chem. 75:275-280.
67. Subcommittee on Homeland Security, Committee on Appropriations, House of Representatives. 2007. Anthrax detection: DHS cannot ensure that sampling activities will be validated. Statement of Keith Rhodes, Chief Technologist, Center for Technology and Engineering Applied Research and Methods, United States Government Accountability Office (GAO-O-070687T). U.S. Government Accountability Office, Washington, DC.
68. Taitt, C. R., G. P. Anderson, B. M. Lingerfelt, M. J. Feldstein, and F. S. Ligler. 2002. Nine-analyte detection using an array-based biosensor. Anal. Chem. 74:6114-6120.
69. Tims, T. B., and D. V. Lim. 2004. Rapid detection of Bacillus anthracis spores directly from powders with an evanescent wave fiber-optic biosensor. J. Microbiol. Methods 59:127-130.
70. Ulrich, M. P., D. R. Christensen, S. R. Coyne, P. D. Craw, E. A. Henchal, S. H. Sakai, D. Swenson, J. Tholath, J. Tsai, A. F. Weir, and D. A. Norwood. 2006. Evaluation of the Cepheid GeneXpert system for detecting Bacillus anthracis. J. Appl. Microbiol. 100:1011-1016.
71. U.S. Environmental Protection Agency (EPA). 1997. Exposure factor handbook. National Center for Environmental Assessment, Washington, DC.
72. Van Ert, M. N., W. R. Easterday, T. S. Simonson, J. M. U'Ren, T. Pearson, L. J. Kenefic, J. D. Busch, L. Y. Huynh, M. Dukerich, C. B. Trim, J. Beaudry, A. Welty-Bernard, T. Read, C. M. Fraser, J. Ravel, and P. Keim. 2007. Strain-specific single-nucleotide polymorphism assays for the Bacillus anthracis Ames strain. J. Clin. Microbiol. 45:47-53.
73. Wan, J. H., B. Fiebor, B. A. Chin, I. H. Chen, J. Brigati, and V. A. Petrenko. 2005. Landscape phage-based magnetostrictive biosensor for detecting Bacillus anthracis spores, p. 1308-1311. In Sensors, IEEE 2005. IEEE, Los Alamitos, CA.
74. Wan, J. H., H. H. Shu, S. C. Huang, B. Fiebor, I. H. Chen, V. A. Petrenko, and B. A. Chin. 2007. Phage-based magnetoelastic wireless biosensors for detecting Bacillus anthracis spores. IEEE Sens. J. 7:470-477.
75. Wang, S. H., J. K. Wen, Y. F. Zhou, Z. P. Zhang, R. F. Yang, J. B. Zhang, J. Chen, and X. E. Zhang. 2004. Identification and characterization of Bacillus anthracis by multiplex PCR on DNA chip. Biosens. Bioelectron 20:807-813.
76. Wilson, W. J., A. M. Erler, S. L. Nasarabadi, E. W. Skowronski, and P. M. Imbro. 2005. A multiplexed PCR-coupled liquid bead array for the simultaneous detection of four biothreat agents. Mol. Cell. Probes 19:137-144.
77. Yu, H., J. W. Raymonda, T. M. McMahon, and A. A. Campagnari. 2000. Detection of biological threat agents by immunomagnetic microspherebased solid phase fluorogenicand electro-chemiluminescence. Biosens. Bioelectron. 14:829-840.
78. Zhang, X. Y., M. A. Young, O. Lyandres, and R. P. Van Duyne. 2005. Rapid detection of an anthrax biomarker by surface-enhanced Raman spectroscopy. J. Am. Chem. Soc. 127:4484-4489.