Evaluation of surrogate animal models of melioidosis

Frontiers in Microbiology

Volumn 1, Issue DEC, 2010, Pages

  Warawa, Jonathan Mark ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

Hamster; Infant diabetic rat; Inflammatory response; Mouse; Non human primate; Pneumonia; Septicemia

Indexed keywords

EID: 84867615595     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2010.00141     Document Type: Review

References (105)

1. Abbink, F. C., Orendi, J. M., and de Beaufort, A. J. (2001). Mother-tochild transmission of Burkholderia pseudomallei. N. Engl. J. Med. 344, 1171-1172.
2. Atkins, T., Prior, R. G., Mack, K., Russell, P., Nelson, M., Oyston, P. C., Dougan, G., and Titball, R. W. (2002). A mutant of Burkholderia pseudomallei, auxotrophic in the branched chain amino acid biosynthetic pathway, is attenuated and protective in a murine model of melioidosis. Infect. Immun. 70, 5290-5294.
3. Barnes, J. L., and Ketheesan, N. (2005). Route of infection in melioidosis. Emerging Infect. Dis. 11, 638-639.
4. Blanc, G., and Baltazard, M. (1949). Recherches sur la melioidose infection a bacille de Whitmore - etude experimentale. Arch. Inst. Pasteur Maroc 3, 520-584.
5. Breitbach, K., Sun, G. W., Kohler, J., Eske, K., Wongprompitak, P., Tan, G., Liu, Y., Gan, Y. H., and Steinmetz, I. (2009). Caspase-1 mediates resistance in murine melioidosis. Infect. Immun. 77, 1589-1595.
6. Brett, P. J., Deshazer, D., and Woods, D. E. (1997). Characterization of Burkholderia pseudomallei and Burkholderia pseudomallei-like strains. Epidemiol. Infect. 118, 137-148.
7. Brieland, J., Freeman, P., Kunkel, R., Chrisp, C., Hurley, M., Fantone, J., and Engleberg, C. (1994). Replicative Legionella pneumophila lung infection in intratracheally inoculated A/J mice. A murine model of human Legionnaires' disease. Am. J. Pathol. 145, 1537-1546.
8. Brown, A. E., Dance, D. A., Suputtamongkol, Y., Chaowagul, W., Kongchareon, S., Webster, H. K., and White, N. J. (1991). Immune cell activation in melioidosis: increased serum levels of interferon-gamma and soluble interleukin-2 receptors without change in soluble CD8 protein. J. Infect. Dis. 163, 1145-1148.
9. Chadwick, D. R., Ang, B., Sitoh, Y. Y., and Lee, C. C. (2002). Cerebral melioidosis in Singapore: a review of five cases. Trans. R. Soc. Trop. Med. Hyg. 96, 72-76.
10. Chaowagul, W., White, N. J., Dance, D. A., Wattanagoon, Y., Naigowit, P., Davis, T. M., Looareesuwan, S., and Pitakwatchara, N. (1989). Melioidosis: a major cause of community-acquired septicemia in northeastern Thailand. J. Infect. Dis. 159, 890-899.
11. Cheng, A. C., and Currie, B. J. (2005). Melioidosis: epidemiology, pathophysiology, and management. Clin. Microbiol. Rev. 18, 383-416.
12. Chetchotisakd, P., Anunnatsiri, S., Kiatchoosakun, S., and Kularbkaew, C. (2010). Melioidosis pericarditis mimicking tuberculous pericarditis. Clin. Infect. Dis. 51, e46-e49.
13. Chiu, C. H., Ostry, A., and Speert, D. P. (2001). Invasion of murine respiratory epithelial cells in vivo by Burkholderia cepacia. J. Med. Microbiol. 50, 594-601.
14. Chodimella, U., Hoppes, W. L., Whalen, S., Ognibene, A. J., and Rutecki, G. W. (1997). Septicemia and suppuration in a Vietnam veteran. Hosp. Pract. (Off. Ed.) 32, 219-221.
15. Choy, J. L., Mayo, M., Janmaat, A., and Currie, B. J. (2000). Animal melioidosis in Australia. Acta Trop. 74, 153-158.
16. Chua, K. L., Chan, Y. Y., and Gan, Y. H. (2003). Flagella are virulence determinantsof Burkholderia pseudomallei. Infect. Immun. 71, 1622-1629.
17. Currie, B. J., Fisher, D. A., Howard, D. M., and Burrow, J. N. (2000a). Neurological melioidosis. Acta Trop. 74, 145-151.
18. Currie, B. J., Fisher, D. A., Howard, D. M., Burrow, J. N., Lo, D., Selva-Nayagam, S., Anstey, N. M., Huffam, S. E., Snelling, P. L., Marks, P. J., Stephens, D. P., Lum, G. D., Jacups, S. P., and Krause, V. L. (2000b). Endemic melioidosis in tropical northern Australia: a 10-year prospective study and review of the literature. Clin. Infect. Dis. 31, 981-986.
19. Currie, B. J., Fisher, D. A., Howard, D. M., Burrow, J. N., Selvanayagam, S., Snelling, P. L., Anstey, N. M., and Mayo, M. J. (2000c). The epidemiology of melioidosis in Australia and Papua New Guinea. Acta Trop. 74, 121-127.
20. Dannenberg, A. M. Jr., and Scott, E. M. (1958). Melioidosis: pathogenesis and immunity in mice and hamsters. Studies, I. with virulent strains of Malleomyces pseudomallei. J. Exp. Med. 107, 153-166.
21. Derbyshire, J. B. (2002). The eradication of glanders in Canada. Can. Vet. J. 43, 722-726.
22. DeShazer, D., Brett, P. J., Carlyon, R., and Woods, D. E. (1997). Mutagenesis of Burkholderia pseudomallei with Tn5-OT182: isolation of motility mutants and molecular characterization of the flagellin structural gene. J. Bacteriol. 179, 2116-2125.
23. DeShazer, D., Brett, P. J., and Woods, D. E. (1998). The type II O-antigenic polysaccharide moiety of Burkholderia pseudomallei lipopolysaccharide is required for serum resistance and virulence. Mol. Microbiol. 30, 1081-1100.
24. Fan, M. H., Klein, R. D., Steinstraesser, L., Merry, A. C., Nemzek, J. A., Remick, D. G., Wang, S. C., and Su, G. L. (2002). An essential role for lipopolysaccharide-binding protein in pulmonary innate immune responses. Shock 18, 248-254.
25. Fisher, M. W., Hillegas, A. B., and Nazeeri, P. L. (1971). Susceptibility in vitro and in vivo of Pseudomonas pseudomallei to rifampin and tetracyclines. Appl. Microbiol. 22, 13-16.
26. Friedland, J. S., Suputtamongkol, Y., Remick, D. G., Chaowagul, W., Strieter, R. M., Kunkel, S. L., White, N. J., and Griffin, G. E. (1992). Prolonged elevation of interleukin-8 and interleukin-6 concentrations in plasma and of leukocyte interleukin-8 mRNA levels during septicemic and localized Pseudomonas pseudomallei infection. Infect. Immun. 60, 2402-2408.
27. Goodyear, A., Kellihan, L., Bielefeldt-Ohmann, H., Troyer, R., Propst, K., and Dow, S. (2009). Protection from pneumonic infection with Burkholderia species by inhalational immunotherapy. Infect. Immun. 77, 1579-1588.
28. Haque, A., Easton, A., Smith, D., O'Garra Van, A.,Rooijen, N., Lertmemongkolchai, G., Titball, R. W., and Bancroft, G. J. (2006). Role of T cells in innate and adaptive immunity against murine Burkholderia pseudomallei infection. J. Infect. Dis. 193, 370-379.
29. Harland, D. N., Chu, K., Haque, A., Nelson, M., Walker, N. J., Sarkar-Tyson, M., Atkins, T. P., Moore, B., Brown, K. A., Bancroft, G., Titball, R. W., and Atkins, H. S. (2007). Identification of a LolC homologue in Burkholderia pseudomallei, a novel protective antigen for melioidosis. Infect. Immun. 75, 4173-4180.
30. Heitmann, S., Tschernig, T., Larbig, M., Steinmetz, I., Hedrich, H. J., and Pabst, R. (1999). Immunohistological characterization of leukocytes in the lungs of healthy mice and after bacterial intratracheal infection. Lab. Anim. 33, 288-294.
31. Hicks, C. L., Kinoshita, R., and Ladds, P. W. (2000). Pathology of melioidosis in captive marine mammals. Aust. Vet. J. 78, 193-195.
32. Hoppe, I., Brenneke, B., Rohde, M., Kreft, A., Haussler, S., Reganzerowski, A., and Steinmetz, I. (1999). Characterization of a murine model of melioidosis: comparison of different strains of mice. Infect. Immun. 67, 2891-2900.
33. Hoyt, R. F. J., Hawkins, J. V., St. Clair, M. B., and Kennet, M. B. (2007). "Mouse physiology," in The Mouse in Biomedical Research, eds J. G. Fox, S. W. Barthold, M. T. Davisson, C. E. Newcomer, F. W. Quimby, and A. L. Smith (Burlington, MA: Academic Press), 23-90.
34. Inglis, T. J., Garrow, S. C., Henderson, M., Clair, A., Sampson, J., O'Reilly, L., and Cameron, B. (2000a). Burkholderia pseudomallei traced to water treatment plant in Australia. Emerging Infect. Dis. 6, 56-59.
35. Inglis, T. J., Rigby, P., Robertson, T. A., Dutton, N. S., Henderson, M., and Chang, B. J. (2000b). Interaction between Burkholderia pseudomallei and Acanthamoeba species results in coiling phagocytosis, endamebic bacterial survival, and escape. Infect. Immun. 68, 1681-1686.
36. Inglis, T. J., Robertson, T., Woods, D. E., Dutton, N., and Chang, B. J. (2003). Flagellum-mediated adhesion by Burkholderia pseudomallei precedes invasion of Acanthamoeba astronyxis. Infect. Immun. 71, 2280-2282.
37. Jeddeloh, J. A., Fritz, D. L., Waag, D. M., Hartings, J. M., and Andrews, G. P. (2003). Biodefense-driven murine model of pneumonic melioidosis. Infect. Immun. 71, 584-587.
38. Jones, A. L., DeShazer, D., and Woods, D. E. (1997). Identification and characterization of a two-component regulatory system involved in invasion of eukaryotic cells and heavy-metal resistance in Burkholderia pseudomallei. Infect. Immun. 65, 4972-4977.
39. Kaestli, M., Mayo, M., Harrington, G., Ward, L., Watt, F., Hill, J. V., Cheng, A. C., and Currie, B. J. (2009). Landscape changes influence the occurrence of the melioidosis bacterium Burkholderia pseudomallei in soil in Northern Australia. PLoS Negl. Trop. Dis. 3, e364. doi: 10.1371/journal. pntd.0000364.
40. Kharbov, D., Velianov, D., and Raucheva, T. (1981). Ecological aspects of Pseudomonas pseudomallei interactionswith Ixodid ticks. Acta Microbiol. Bulg. 8, 17-24.
41. Kim, C. S., and Hu, S. C. (1998). Regional deposition of inhaled particles in human lungs: comparison between men and women. J. Appl. Physiol. 84, 1834-1844.
42. Koh, G. C., and Limmathurotsakul, D. (2010). Gamma interferon supplementation for melioidosis. Antimicrob. Agents Chemother. 54, 4520; author reply 4520-4521.
43. Lacher, S. E., Johnson, C., Jessop, F., Holian, A., and Migliaccio, C. T. (2010). Murine pulmonary inflammation model: a comparative study of anesthesia and instillation methods. Inhal. Toxicol. 22, 77-83.
44. Laopaiboon, V., Chamadol, N., Buttham, H., and Sukeepaisarnjareon, W. (2009). CT findings of liver and splenic abscesses in melioidosis: comparison with those in non-melioidosis. J. Med. Assoc. Thai. 92, 1476-1484.
45. Lauw, F. N., Simpson, A. J., Prins, J. M., Smith, M. D., Kurimoto, M., van Deventer, S. J., Speelman, P., Chaowagul, W., White, N. J., and van der Poll, T. (1999). Elevated plasma concentrations of interferon (IFN)-gamma and the IFN-gamma-inducing cytokines interleukin (IL)-18, IL-12, and IL-15 in severe melioidosis. J. Infect. Dis. 180, 1878-1885.
46. Lauw, F. N., Simpson, A. J., Prins, J. M., van Deventer, S. J., Chaowagul, W., White, N. J., and van der Poll, T. (2000). The CXC chemokines gamma interferon (IFN-gamma)-inducible protein 10 and monokine induced by IFN-gamma are released during severe melioidosis. Infect. Immun. 68, 3888-3893.
47. Leakey, A. K., Ulett, G. C., and Hirst, R. G. (1998). BALB/c and C57Bl/6 mice infected with virulent Burkholderia pseudomallei provide contrasting animal models for the acute and chronic forms of human melioidosis. Microb. Pathog. 24, 269-275.
48. Leelarasamee, A. (1998). Burkholderia pseudomallei: the unbeatable foe? Southeast Asian J. Trop. Med. Public Health 29, 410-415.
49. Lever, M. S., Nelson, M., Stagg, A. J., Beedham, R. J., and Simpson, A. J. (2009). Experimental acute respiratory Burkholderia pseudomallei infection in BALB/c mice. Int. J. Exp. Pathol. 90, 16-25.
50. Levy, A., Chang, B. J., Abbott, L. K., Kuo, J., Harnett, G., and Inglis, T. J. (2003). Invasion of spores of the arbuscular mycorrhizal fungus Gigaspora decipiens by Burkholderia spp. Appl. Environ. Microbiol. 69, 6250-6256.
51. Lim, K. S., and Chong, V. H. (2010). Radiological manifestations of melioidosis. Clin. Radiol. 65, 66-72.
52. Limmathurotsakul, D., Chaowagul, W., Chierakul, W., Stepniewska, K., Maharjan, B., Wuthiekanun, V., White, N. J., Day, N. P., and Peacock, S. J. (2006). Risk factors for recurrent melioidosis in northeast Thailand. Clin. Infect. Dis. 43, 979-986.
53. Limmathurotsakul, D., Wongratanacheewin, S., Teerawattanasook, N., Wongsuvan, G., Chaisuksant, S., Chetchotisakd, P., Chaowagul, W., Day, N. P., and Peacock, S. J. (2010a). Increasing incidence of human melioidosis in Northeast Thailand. Am. J. Trop. Med. Hyg. 82, 1113-1117.
54. Limmathurotsakul, D., Wuthiekanun, V., Chantratita, N., Wongsuvan, G., Amornchai, P., Day, N. P., and Peacock, S. J. (2010b). Burkholderia pseudomallei is spatially distributed in soil in northeast Thailand. PLoS Negl. Trop. Dis. 4, e694. doi: 10.1371/journal. pntd.0000694.
55. Liu, B., Koo, G. C., Yap, E. H., Chua, K. L., and Gan, Y. H. (2002). Model of differential susceptibility to mucosal Burkholderia pseudomallei infection. Infect. Immun. 70, 504-511.
56. Manzeniuk, I. N., Galina, E. A., Dorokhin, V. V., Kalachev, I., Borzenkov, V. N., and Svetoch, E. A. (1999). Burkholderia mallei and Burkholderia pseudomallei. Study of immunoand pathogenesis of glanders and melioidosis. Heterologous vaccines. Antibiot. Khimioter 44, 21-26.
57. McCormick, J. B., Sexton, D. J., McMurray, J. G., Carey, E., Hayes, P., and Feldman, R. A. (1975). Human-to-human transmission of Pseudomonas pseudomallei. Ann. Intern. Med. 83, 512-513.
58. Miller, W. R., Pannell, L., Cravitz, L., Tanner, W. A., and Rosebury, T. (1948). Studies on certain biological characteristics of Malleomyces mallei and Malleomyces pseudomallei. IVirulence, I. and infectivity for animals. J. Bacteriol. 55, 127-135.
59. Moore, R. A., DeShazer, D., Reckseidler, S., Weissman, A., and Woods, D. E. (1999). Efflux-mediated aminoglycoside and macrolide resistance in Burkholderia pseudomallei. Antimicrob. Agents Chemother. 43, 465-470.
60. Moore, R. A., Reckseidler-Zenteno, S., Kim, H., Nierman, W., Yu, Y., Tuanyok, A., Warawa, J., DeShazer, D., and Woods, D. E. (2004). Contribution of gene loss to the pathogenic evolution of Burkholderia pseudomallei and Burkholderia mallei. Infect. Immun. 72, 4172-4187.
61. Morse, L. P., Moller, C. C., Harvey, E., Ward, L., Cheng, A. C., Carson, P. J., and Currie, B. J. (2009). Prostatic abscess due to Burkholderia pseudomallei: 81 cases from a 19-yearprospective melioidosis study. J. Urol. 182, 542-547; discussion 547.
62. Moser, C., Johansen, H. K., Song, Z., Hougen, H. P., Rygaard, J., and Hoiby, N. (1997). Chronic Pseudomonas aeruginosa lung infection is more severe in Th2 responding BALB/c mice compared to Th1 responding C3H/HeN mice. APMIS 105, 838-842.
63. Muttarak, M., Peh, W. C., Euathrongchit, J., Lin, S. E., Tan, A. G., Lerttumnongtum, P., and Sivasomboon, C. (2008). Spectrum of imaging findings in melioidosis. Br. J. Radiol. 82, 514-521.
64. Najdenski, H., Kussovski, V., and Vesselinova, A. (2004). Experimental Burkholderia pseudomallei infection of pigs. J. Vet. Med. B Infect. Dis. Vet. Public Health 51, 225-230.
65. Nelson, M., Prior, J. L., Lever, M. S., Jones, H. E., Atkins, T. P., and Titball, R. W. (2004). Evaluation of lipopolysaccharide and capsular polysaccharide as subunit vaccines against experimental melioidosis. J. Med. Microbiol. 53, 1177-1182.
66. Ngauy, V., Lemeshev, Y., Sadkowski, L., and Crawford, G. (2005). Cutaneous melioidosis in a man who was taken as a prisoner of war by the Japanese during World War II. J. Clin. Microbiol. 43, 970-972.
67. Nierman, W. C., DeShazer, D., Kim, H. S., Tettelin, H., Nelson, K. E., Feldblyum, T., Ulrich, R. L., Ronning, C. M., Brinkac, L. M., Daugherty, S. C., Davidsen, T. D., Deboy, R. T., Dimitrov, G., Dodson, R. J., Durkin, A. S., Gwinn, M. L., Haft, D. H., Khouri, H., Kolonay, J. F., Madupu, R., Mohammoud, Y., Nelson, W. C., Radune, D., Romero, C. M., Sarria, S., Selengut, J., Shamblin, C., Sullivan, S. A., White, O., Yu, Y., Zafar, N., Zhou, L., and Fraser, C. M. (2004). Structural flexibility in the Burkholderia mallei genome. Proc. Natl. Acad. Sci. U.S.A. 101, 14246-14251.
68. Nigg, C., Ruch, J., Scott, E., and Noble, K. (1956). Enhancement of virulence of Malleomyces pseudomallei. J. Bacteriol. 71, 530-541.
69. O'Quinn, A. L., Wiegand, E. M., and Jeddeloh, J. A. (2001). Burkholderia pseudomallei kills the nematode Caenorhabditis elegans using an endotoxin-mediated paralysis. Cell. Microbiol. 3, 381-393.
70. Owen, S. J., Batzloff, M., Chehrehasa, F., Meedeniya, A., Casart, Y., Logue, C. A., Hirst, R. G., Peak, I. R., Mackay-Sim, A., and Beacham, I. R. (2009). Nasal-associated lymphoid tissue and olfactory epithelium as portals of entry for Burkholderia pseudomallei in murine Melioidosis. J. Infect. Dis. 199, 1761-1770.
71. Pilatz, S., Breitbach, K., Hein, N., Fehlhaber, B., Schulze, J., Brenneke, B., Eberl, L.,and Steinmetz, I. (2006). Identification of Burkholderia pseudomallei genes required for the intracellular life cycle and in vivo virulence. Infect. Immun. 74, 3576-3586.
72. Propst, K. L., Troyer, R. M., Kellihan, L. M., Schweizer, H. P., and Dow, S. W. (2010). Immunotherapy markedly increases the effectiveness of antimicrobial therapy for treatment of Burkholderia pseudomallei infection. Antimicrob. Agents Chemother. 54, 1785-1792.
73. Reckseidler, S. L., DeShazer, D., Sokol, P. A., and Woods, D. E. (2001). Detection of bacterial virulence genes by subtractive hybridization: identification of capsular polysaccharide of Burkholderia pseudomallei as a major virulence determinant. Infect. Immun. 69, 34-44.
74. Reznik, G. K. (1990). Comparative anatomy, physiology, and function of the upper respiratory tract. Environ. Health Perspect. 85, 171-176.
75. Santanirand, P., Harley, V. S., Dance, D. A., Drasar, B. S., and Bancroft, G. J. (1999). Obligatory role of gamma interferon for host survival in a murine model of infection with Burkholderia pseudomallei. Infect. Immun. 67, 3593-3600.
76. Sarkar-Tyson, M., Smither, S. J., Harding, S. V., Atkins, T. P., and Titball, R. W. (2009). Protective efficacy of heat-inactivated B. thailandensis, B. mallei or B. pseudomallei against experimental melioidosis and glanders. Vaccine 27, 4447-4451.
77. Simpson, A. J., Smith, M. D., Weverling, G. J., Suputtamongkol, Y., Angus, B. J., Chaowagul, W., White, N. J., van Deventer, S. J., and Prins, J. M. (2000). Prognostic value of cytokine concentrations (tumor necrosis factor-alpha, interleukin-6, and interleukin-10) and clinical parameters in severe melioidosis. J. Infect. Dis. 181, 621-625.
78. Smith, M. D., Angus, B. J., Wuthiekanun, V., and White, N. J. (1997). Arabinose assimilation defines a nonvirulent biotype of Burkholderia pseudomallei. Infect. Immun. 65, 4319-4321.
79. Sprague, L. D., and Neubauer, H. (2004). Melioidosis in animals: a review on epizootiology, diagnosis and clinical presentation. J. Vet. Med. B Infect. Dis. Vet. Public Health 51, 305-320.
80. Srilunchang, T., Proungvitaya, T., Wongratanacheewin, S., Strugnell, R., and Homchampa, P. (2009). Construction and characterization of an unmarked aroC deletion mutant of Burkholderia pseudomallei strain A2. Southeast Asian J. Trop. Med. Public Health 40, 123-130.
81. Srisurat, N., Sermswan, R. W., Tatawasart, U., and Wongratanacheewin, S. (2010). Bacterial loads and antibody responses in BALB/c mice infected with low and high doses of Burkholderia pseudomallei. Am. J. Trop. Med. Hyg. 82, 1102-1105.
82. Steward, J., Piercy, T., Lever, M. S., Nelson, M., Simpson, A. J., and Brooks, T. J. (2005). Comparison of gatifloxacin, moxifloxacin and ciprofloxacin for treatment of experimental Burkholderia pseudomallei infection. J. Antimicrob. Chemother. 55, 523-527.
83. Su, X., Looney, M., Robriquet, L., Fang, X., and Matthay, M. A. (2004). Direct visual instillation as a method for efficient delivery of fluid into the distal airspaces of anesthetized mice. Exp. Lung Res. 30, 479-493.
84. Sulaiman, S., Othman, M. Z., and Aziz, A. H. (2000). Isolations of enteric pathogens from synanthropic flies trapped in downtown Kuala Lumpur. J. Vector Ecol. 25, 90-93.
85. Suputtamongkol, Y., Kwiatkowski, D., Dance, D. A., Chaowagul, W., and White, N. J. (1992). Tumor necrosis factor in septicemic melioidosis. J. Infect. Dis. 165, 561-564.
86. Tan, G. Y., Liu, Y., Sivalingam, S. P., Sim, S. H., Wang, D., Paucod, J. C., Gauthier, Y., and Ooi, E. E. (2008). Burkholderia pseudomallei aerosol infection results in differential inflammatory responses in BALB/c and C57Bl/6 mice. J. Med. Microbiol. 57, 508-515.
87. Taweechaisupapong, S., Kaewpa, C., Arunyanart, C., Kanla, P., Homchampa, P., Sirisinha, S., Proungvitaya, T., and Wongratanacheewin, S. (2005). Virulence of Burkholderia pseudomallei does not correlate with biofilm formation. Microb. Pathog. 39, 77-85.
88. Thomas, R. J., Webber, D., Collinge, A., Stagg, A. J., Bailey, S. C., Nunez, A., Gates, A., Jayasekera, P. N., Taylor, R. R., Eley, S., and Titball, R. W. (2009). Different pathologies but equal levels of responsiveness to the recombinant F1 and V antigen vaccine and ciprofloxacin in a murine model of plague caused by small- and largeparticle aerosols. Infect. Immun. 77, 1315-1323.
89. Titball, R. W., Russell, P., Cuccui, J., Easton, A., Haque, A., Atkins, T., Sarkar-Tyson, M., Harley, V., Wren, B., and Bancroft, G. J. (2008). Burkholderia pseudomallei: animal models of infection. Trans. R. Soc. Trop. Med. Hyg. 102(Suppl. 1), S111-S116.
90. Ulett, G. C., Currie, B. J., Clair, T. W., Mayo, M., Ketheesan, N., Labrooy, J., Gal, D., Norton, R., Smith, C. A.,Barnes, J., Warner, J., and Hirst, R. G. (2001). Burkholderia pseudomallei virulence: definition, stability and association with clonality. Microbes Infect. 3, 621-631.
91. Ulett, G. C., Ketheesan, N., Clair, T. W., McElnea, C. L., Barnes, J. L., and Hirst, R. G. (2002). Analogous cytokine responses to Burkholderia pseudomallei strains contrasting in virulence correlate with partial cross-protection in immunized mice. Infect. Immun. 70, 3953-3958.
92. Ulett, G. C., Ketheesan, N., and Hirst, R. G. (2000). Proinflammatory cytokine mRNA responses in experimental Burkholderia pseudomallei infection in mice. Acta Trop. 74, 229-234.
93. Ulrich, R. L., Deshazer, D., Brueggemann, E. E., Hines, H. B., Oyston, P. C., and Jeddeloh, J. A. (2004). Role of quorum sensing in the pathogenicity of Burkholderia pseudomallei. J. Med. Microbiol. 53, 1053-1064.
94. Valade, E., Thibault, F. M., Gauthier, Y. P., Palencia, M., Popoff, M. Y., and Vidal, D. R. (2004). The PmlI-PmlR quorum-sensing system in Burkholderia pseudomallei plays a key role in virulence and modulates production of the MprA protease. J. Bacteriol. 186, 2288-2294.
95. van Schaik, E., Tom, M., Devinney, R., and Woods, D. E. (2008). Development of novel animal infection models for the study of acute and chronic Burkholderia pseudomallei pulmonary infections. Microbes Infect. 10, 1291-1299.
96. van Schaik, E. J., Tom, M., and Woods, D. E. (2009). Burkholderia pseudomallei isocitrate lyase is a persistence factor in pulmonary melioidosis: implications for the development of isocitrate lyase inhibitors as novel antimicrobials. Infect. Immun. 77, 4275-4283.
97. Warawa, J., and Woods, D. E. (2005). Type III secretion system cluster 3 is required for maximal virulence of Burkholderia pseudomallei in a hamster infection model. FEMS Microbiol. Lett. 242, 101-108.
98. Warawa, J. M., and Gherardini, F. C. (2010). "Modeling of acute respiratory melioidosis and glanders," in National Institute of Allergy and Infectious Diseases, NIH Volume 3, Intramural Research, ed. V. S. Georgiev (New York, NY: Humana Press), 117-121.
99. Warawa, J. M., Long, D., Rosenke, R., Gardner, D., and Gherardini, F. C. (2009). Role for the Burkholderia pseudomallei capsular polysaccharide encoded by the wcb operon in acutedisseminated melioidosis. Infect. Immun. 77, 5252-5261.
100. West, T. E., Myers, N. D., Limmathurotsakul, D., Liggitt, H. D., Chantratita, N., Peacock, S. J., and Skerrett, S. J. (2010). Pathogenicity of high-dose enteral inoculation of Burkholderia pseudomallei to mice. Am. J. Trop. Med. Hyg. 83, 1066-1069.
101. Wikraiphat, C., Charoensap, J., Utaisincharoen, P., Wongratanacheewin, S., Taweechaisupapong, S., Woods, D. E., Bolscher, J. G., and Sirisinha, S. (2009). Comparative in vivo and in vitro analyses of putative virulence factors of Burkholderia pseudomallei using lipopolysaccharide, capsule and flagellin mutants. FEMS Immunol. Med. Microbiol. 56, 253-259.
102. Wong, K. T., Puthucheary, S. D., and Vadivelu, J. (1995). The histopathology of human melioidosis. Histopathology 26, 51-55.
103. Wong, K. T., Vadivelu, J., Puthucheary, S. D., and Tan, K. L. (1996). An immunohistochemical method for the diagnosis of melioidosis. Pathology 28, 188-191.
104. Woods, D. E., Jones, A. L., and Hill, P. J. (1993). Interaction of insulin with Pseudomonas pseudomallei. Infect. Immun. 61, 4045-4050.
105. Yap, E. H., Thong, T. W., Tan, A. L., Yeo, M., Tan, H. C., Loh, H., Teo, T. P., Thong, K. T., Singh, M., and Chan, Y. C. (1995). Comparison of Pseudomonas pseudomallei from humans, animals, soil and water by restriction endonuclease analysis. Singapore Med. J. 36, 60-62.