Advertisement

Burkholderia pseudomallei

  • Kathryn J. Pflughoeft
  • Derrick Hau
  • Peter Thorkildson
  • David P. AuCoinEmail author
Chapter

Abstract

Melioidosis is an infectious disease caused by the bacterium Burkholderia pseudomallei, a motile, Gram-negative saprophyte commonly found in soil and water in tropical and subtropical areas. Melioidosis is considered one of the most neglected tropical diseases. The bacterium is endemic to South-eastern Asia and northern Australia; however, a more representative assessment may expand the endemic regions to include Southern Asia, Africa, and parts of America. Underreporting is likely due to the initial undifferentiated symptoms and clinical signs associated with the disease and the vast array of patient outcomes, which can range from localized skin abscesses to pneumonia and bacteremia. Differences in clinical outcomes may be attributed to the intrinsic antibiotic resistance of the organism, availability of critical care services, and the underlying health of the patient. Increased disease burden correlates with diabetes, excessive alcohol use, chronic renal failure, and lung disease. Due to the high case fatality rate associated with melioidosis, which can reach 70% in untreated cases, the ease of aerosolization, and prevalence in the soil of endemic regions, the organism has been classified as a Tier 1 Select Agent by the United States Department of Agriculture (USDA) and Health and Human Services (DHHS). Diagnosis is dependent on a culture-positive patient sample, a difficult standard for a pathogen with a low bioburden. Recent advances in vaccine development and rapid, cost-effective diagnostics, have the potential to improve the burden associated with melioidosis.

Keywords

Burkholderia pseudomallei Antibiotic resistance Opportunistic Modes of transmission Mechanism of disease Patient outcomes 

References

  1. 1.
    Dance DA. Melioidosis as an emerging global problem. Acta Trop. 2000;74(2–3):115–9.CrossRefPubMedGoogle Scholar
  2. 2.
    Chong VF, Fan YF. The radiology of melioidosis. Australas Radiol. 1996;40(3):244–9.CrossRefPubMedGoogle Scholar
  3. 3.
    White NJ. Melioidosis. Lancet. 2003;361(9370):1715–22.CrossRefPubMedGoogle Scholar
  4. 4.
    Khosravi Y, Vellasamy KM, Mariappan V, Ng SL, Vadivelu J. Antimicrobial susceptibility and genetic characterisation of Burkholderia pseudomallei isolated from Malaysian patients. ScientificWorldJournal. 2014;2014:132971.  https://doi.org/10.1155/2014/132971.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Peacock SJ, Schweizer HP, Dance DA, Smith TL, Gee JE, Wuthiekanun V, DeShazer D, Steinmetz I, Tan P, Currie BJ. Management of accidental laboratory exposure to Burkholderia pseudomallei and B. mallei. Emerg Infect Dis. 2008;14(7):e2.  https://doi.org/10.3201/eid1407.071501.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Limmathurotsakul D, Golding N, Dance DA, Messina JP, Pigott DM, Moyes CL, Rolim DB, Bertherat E, Day NP, Peacock SJ, Hay SI. Predicted global distribution of Burkholderia pseudomallei and burden of melioidosis. Nat Microbiol. 2016;1(1):15008.  https://doi.org/10.1038/nmicrobiol.2015.8.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    White NJ, Dance DA, Chaowagul W, Wattanagoon Y, Wuthiekanun V, Pitakwatchara N. Halving of mortality of severe melioidosis by ceftazidime. Lancet. 1989;2(8665):697–701.CrossRefPubMedGoogle Scholar
  8. 8.
    Lo TJ, Ang LW, James L, Goh KT. Melioidosis in a tropical city state, Singapore. Emerg Infect Dis. 2009;15(10):1645–7.  https://doi.org/10.3201/eid1510.090246.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Cheng AC, Hanna JN, Norton R, Hills SL, Davis J, Krause VL, Dowse G, Inglis TJ, Currie BJ. Melioidosis in northern Australia, 2001-02. Commun Dis Intell Q Rep. 2003;27(2):272–7.PubMedGoogle Scholar
  10. 10.
    Wuthiekanun V, Peacock SJ. Management of melioidosis. Expert Rev Anti-Infect Ther. 2006;4(3):445–55.  https://doi.org/10.1586/14787210.4.3.445.CrossRefPubMedGoogle Scholar
  11. 11.
    Stanton A, Fletcher W. Melioidosis, a new disease of the tropics, 1921.Google Scholar
  12. 12.
    Whitmore A. An account of a Glanders-like disease occurring in Rangoon. J Hyg (Lond). 1913;13(1):1–34.31.CrossRefGoogle Scholar
  13. 13.
    Frothingham L. The diagnosis of Glanders by the Strauss method. J Med Res. 1901;6(2):331–40.PubMedPubMedCentralGoogle Scholar
  14. 14.
    Stanton A. Melioidosis, a disease of rodents communicable to man. Lancet. 1925;205(5288):10–3.  https://doi.org/10.1016/S0140-6736(01)04724-9.CrossRefGoogle Scholar
  15. 15.
    Bergey DH, Breed RS. Bergey’s manual of determinative bacteriology. American Society for Microbiology. 7th ed. Baltimore: Williams & Wilkins; 1957.Google Scholar
  16. 16.
    Sokatch J. The biology of pseudomonas. Elsevier; 2012.Google Scholar
  17. 17.
    Levine HB, Dowling JH, Evenson M, Lien OG. Growth of Malleomyces pseudomallei in simple chemically defined media. J Bacteriol. 1954;67(3):350–2.PubMedPubMedCentralGoogle Scholar
  18. 18.
    Bokman AH, Levine HB, Lusby M. Glucose catabolism in Malleomyces pseudomallei. J Bacteriol. 1957;73(5):649–54.PubMedPubMedCentralGoogle Scholar
  19. 19.
    Palleroni N, Kunisawa R, Contopoulou R, Doudoroff M. Nucleic acid homologies in the genus Pseudomonas. Int J Syst Evol Microbiol. 1973;23(4):333–9.Google Scholar
  20. 20.
    Yabuuchi E, Kosako Y, Oyaizu H, Yano I, Hotta H, Hashimoto Y, Ezaki T, Arakawa M. Proposal of Burkholderia gen. nov. and transfer of seven species of the genus Pseudomonas homology group II to the new genus, with the type species Burkholderia cepacia (Palleroni and Holmes 1981) comb. nov. Microbiol Immunol. 1992;36(12):1251–75.CrossRefPubMedGoogle Scholar
  21. 21.
    Suputtamongkol Y, Hall AJ, Dance DA, Chaowagul W, Rajchanuvong A, Smith MD, White NJ. The epidemiology of melioidosis in Ubon Ratchatani, northeast Thailand. Int J Epidemiol. 1994;23(5):1082–90.CrossRefPubMedGoogle Scholar
  22. 22.
    Currie BJ, Jacups SP, Cheng AC, Fisher DA, Anstey NM, Huffam SE, Krause VL. Melioidosis epidemiology and risk factors from a prospective whole-population study in northern Australia. Tropical Med Int Health. 2004;9(11):1167–74.  https://doi.org/10.1111/j.1365-3156.2004.01328.x.CrossRefGoogle Scholar
  23. 23.
    Leelarasamee A. Melioidosis in Southeast Asia. Acta Trop. 2000;74(2–3):129–32.CrossRefPubMedGoogle Scholar
  24. 24.
    Bhengsri S, Lertiendumrong J, Baggett HC, Thamthitiwat S, Chierakul W, Tisayaticom K, Tanwisaid K, Chantra S, Kaewkungwal J. Economic burden of bacteremic melioidosis in Eastern and Northeastern, Thailand. Am J Trop Med Hyg. 2013;89(2):369–73.  https://doi.org/10.4269/ajtmh.13-0148.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Perumal Samy R, Stiles BG, Sethi G, Lim LHK. Melioidosis: clinical impact and public health threat in the tropics. PLoS Negl Trop Dis. 2017;11(5):e0004738.  https://doi.org/10.1371/journal.pntd.0004738.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Dance DA. Melioidosis: the tip of the iceberg? Clin Microbiol Rev. 1991;4(1):52–60.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Pearson T, Giffard P, Beckstrom-Sternberg S, Auerbach R, Hornstra H, Tuanyok A, Price EP, Glass MB, Leadem B, Beckstrom-Sternberg JS, Allan GJ, Foster JT, Wagner DM, Okinaka RT, Sim SH, Pearson O, Wu Z, Chang J, Kaul R, Hoffmaster AR, Brettin TS, Robison RA, Mayo M, Gee JE, Tan P, Currie BJ, Keim P. Phylogeographic reconstruction of a bacterial species with high levels of lateral gene transfer. BMC Biol. 2009;7:78.  https://doi.org/10.1186/1741-7007-7-78.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Price EP, Sarovich DS, Smith EJ, MacHunter B, Harrington G, Theobald V, Hall CM, Hornstra HM, McRobb E, Podin Y, Mayo M, Sahl JW, Wagner DM, Keim P, Kaestli M, Currie BJ. Unprecedented melioidosis cases in Northern Australia caused by an Asian Burkholderia pseudomallei strain identified by using large-scale comparative genomics. Appl Environ Microbiol. 2016;82(3):954–63.  https://doi.org/10.1128/AEM.03013-15.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Vesaratchavest M, Tumapa S, Day NP, Wuthiekanun V, Chierakul W, Holden MT, White NJ, Currie BJ, Spratt BG, Feil EJ, Peacock SJ. Nonrandom distribution of Burkholderia pseudomallei clones in relation to geographical location and virulence. J Clin Microbiol. 2006;44(7):2553–7.  https://doi.org/10.1128/jcm.00629-06.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Benoit TJ, Blaney DD, Gee JE, Elrod MG, Hoffmaster AR, Doker TJ, Bower WA, Walke HT, (CDC) CfDCaP. Melioidosis cases and selected reports of occupational exposures to Burkholderia pseudomallei – United States, 2008-2013. MMWR Surveill Summ. 2015;64(5):1–9.PubMedGoogle Scholar
  31. 31.
    Lim C, Peacock SJ, Limmathurotsakul D. Association between activities related to routes of infection and clinical manifestations of melioidosis. Clin Microbiol Infect. 2016;22(1):79.e1–3.  https://doi.org/10.1016/j.cmi.2015.09.016.CrossRefGoogle Scholar
  32. 32.
    Kamjumphol W, Chareonsudjai P, Taweechaisupapong S, Chareonsudjai S. Morphological alteration and survival of Burkholderia pseudomallei in soil microcosms. Am J Trop Med Hyg. 2015;93(5):1058–65.  https://doi.org/10.4269/ajtmh.15-0177.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Limmathurotsakul D, Kanoksil M, Wuthiekanun V, Kitphati R, deStavola B, Day NP, Peacock SJ. Activities of daily living associated with acquisition of melioidosis in northeast Thailand: a matched case-control study. PLoS Negl Trop Dis. 2013;7(2):e2072.  https://doi.org/10.1371/journal.pntd.0002072.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Currie BJ, Jacups SP. Intensity of rainfall and severity of melioidosis, Australia. Emerg Infect Dis. 2003;9(12):1538–42.  https://doi.org/10.3201/eid0912.020750.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Liu X, Pang L, Sim SH, Goh KT, Ravikumar S, Win MS, Tan G, Cook AR, Fisher D, Chai LY. Association of melioidosis incidence with rainfall and humidity, Singapore, 2003-2012. Emerg Infect Dis. 2015;21(1):159–62.  https://doi.org/10.3201/eid2101.140042.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Chen PS, Chen YS, Lin HH, Liu PJ, Ni WF, Hsueh PT, Liang SH, Chen C, Chen YL. Airborne transmission of melioidosis to humans from environmental aerosols contaminated with B. pseudomallei. PLoS Negl Trop Dis. 2015;9(6):e0003834.  https://doi.org/10.1371/journal.pntd.0003834.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Mayo M, Kaesti M, Harrington G, Cheng AC, Ward L, Karp D, Jolly P, Godoy D, Spratt BG, Currie BJ. Burkholderia pseudomallei in unchlorinated domestic bore water, Tropical Northern Australia. Emerg Infect Dis. 2011;17(7):1283–5.  https://doi.org/10.3201/eid1707.100614.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Currie BJ, Ward L, Cheng AC. The epidemiology and clinical spectrum of melioidosis: 540 cases from the 20 year Darwin prospective study. PLoS Negl Trop Dis. 2010;4(11):e900.  https://doi.org/10.1371/journal.pntd.0000900.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Chin J. Control of communicable diseases manual, 2000.Google Scholar
  40. 40.
    Cheng AC, Currie BJ, Dance DA, Funnell SG, Limmathurotsakul D, Simpson AJ, Peacock SJ. Clinical definitions of melioidosis. Am J Trop Med Hyg. 2013;88(3):411–3.  https://doi.org/10.4269/ajtmh.12-0555.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Domthong P, Chaisuksant S, Sawanyawisuth K. What clinical factors are associated with mortality in septicemic melioidosis? A report from an endemic area. J Infect Dev Ctries. 2016;10(4):404–9.CrossRefPubMedGoogle Scholar
  42. 42.
    McLeod C, Morris PS, Bauert PA, Kilburn CJ, Ward LM, Baird RW, Currie BJ. Clinical presentation and medical management of melioidosis in children: a 24-year prospective study in the Northern Territory of Australia and review of the literature. Clin Infect Dis. 2015;60(1):21–6.  https://doi.org/10.1093/cid/ciu733.CrossRefPubMedGoogle Scholar
  43. 43.
    Teparrukkul P, Kongkasame W, Chitsaeng S, Wongsuwan G, Wuthiekanun V, Peacock SJ, Limmathurotsakul D. Gastrointestinal tract involvement in melioidosis. Trans R Soc Trop Med Hyg. 2017;111(4):185–7.  https://doi.org/10.1093/trstmh/trx031.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Kelser EA. Melioidosis: a greater threat than previously suspected? Microbes Infect. 2016;18(11):661–8.  https://doi.org/10.1016/j.micinf.2016.07.001.CrossRefPubMedGoogle Scholar
  45. 45.
    Thatrimontrichai A, Maneenil G. Neonatal melioidosis: systematic review of the literature. Pediatr Infect Dis J. 2012;31(11):1195–7.  https://doi.org/10.1097/INF.0b013e318265ac62.CrossRefPubMedGoogle Scholar
  46. 46.
    Jenney AW, Lum G, Fisher DA, Currie BJ. Antibiotic susceptibility of Burkholderia pseudomallei from tropical northern Australia and implications for therapy of melioidosis. Int J Antimicrob Agents. 2001;17(2):109–13.CrossRefPubMedGoogle Scholar
  47. 47.
    Inglis TJ. The treatment of melioidosis. Pharmaceuticals (Basel). 2010;3(5):1296–303.  https://doi.org/10.3390/ph3051296.CrossRefGoogle Scholar
  48. 48.
    Thibault FM, Hernandez E, Vidal DR, Girardet M, Cavallo JD. Antibiotic susceptibility of 65 isolates of Burkholderia pseudomallei and Burkholderia mallei to 35 antimicrobial agents. J Antimicrob Chemother. 2004;54(6):1134–8.  https://doi.org/10.1093/jac/dkh471.CrossRefPubMedGoogle Scholar
  49. 49.
    Wuthiekanun V, Amornchai P, Saiprom N, Chantratita N, Chierakul W, Koh GC, Chaowagul W, Day NP, Limmathurotsakul D, Peacock SJ. Survey of antimicrobial resistance in clinical Burkholderia pseudomallei isolates over two decades in Northeast Thailand. Antimicrob Agents Chemother. 2011;55(11):5388–91.  https://doi.org/10.1128/AAC.05517-11.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Dharakul T, Vejbaesya S, Chaowagul W, Luangtrakool P, Stephens HA, Songsivilai S. HLA-DR and -DQ associations with melioidosis. Hum Immunol. 1998;59(9):580–6.CrossRefPubMedGoogle Scholar
  51. 51.
    Chierakul W, Wuthiekanun V, Chaowagul W, Amornchai P, Cheng AC, White NJ, Day NP, Peacock SJ. Short report: disease severity and outcome of melioidosis in HIV coinfected individuals. Am J Trop Med Hyg. 2005;73(6):1165–6.CrossRefPubMedGoogle Scholar
  52. 52.
    Cahn A, Koslowsky B, Nir-Paz R, Temper V, Hiller N, Karlinsky A, Gur I, Hidalgo-Grass C, Heyman SN, Moses AE, Block C. Imported melioidosis, Israel, 2008. Emerg Infect Dis. 2009;15(11):1809–11.  https://doi.org/10.3201/eid1511.090038.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Mustafa M, Menon J, Robinson F, Rahman M. Clinical manifestations, diagnosis, and treatment of Melioidosis. IOSR Journal Of Pharmacy. 2015;5(2):13–19.Google Scholar
  54. 54.
    Vidyalakshmi K, Chakrapani M, Shrikala B, Damodar S, Lipika S, Vishal S. Tuberculosis mimicked by melioidosis. Int J Tuberc Lung Dis. 2008;12(10):1209–15.PubMedGoogle Scholar
  55. 55.
    Stewart JD, Smith S, Binotto E, McBride WJ, Currie BJ, Hanson J. The epidemiology and clinical features of melioidosis in Far North Queensland: implications for patient management. PLoS Negl Trop Dis. 2017;11(3):e0005411.  https://doi.org/10.1371/journal.pntd.0005411.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Chaowagul W, White NJ, Dance DA, Wattanagoon Y, Naigowit P, Davis TM, Looareesuwan S, Pitakwatchara N. Melioidosis: a major cause of community-acquired septicemia in northeastern Thailand. J Infect Dis. 1989;159(5):890–9.CrossRefPubMedGoogle Scholar
  57. 57.
    Gong L, Cullinane M, Treerat P, Ramm G, Prescott M, Adler B, Boyce JD, Devenish RJ. The Burkholderia pseudomallei type III secretion system and BopA are required for evasion of LC3-associated phagocytosis. PLoS One. 2011;6(3):e17852.  https://doi.org/10.1371/journal.pone.0017852.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Stevens MP, Friebel A, Taylor LA, Wood MW, Brown PJ, Hardt WD, Galyov EE. A Burkholderia pseudomallei type III secreted protein, BopE, facilitates bacterial invasion of epithelial cells and exhibits guanine nucleotide exchange factor activity. J Bacteriol. 2003;185(16):4992–6.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Bocan TM, Panchal RG, Bavari S. Applications of in vivo imaging in the evaluation of the pathophysiology of viral and bacterial infections and in development of countermeasures to BSL3/4 pathogens. Mol Imaging Biol. 2015;17(1):4–17.  https://doi.org/10.1007/s11307-014-0759-7.CrossRefPubMedGoogle Scholar
  60. 60.
    Kespichayawattana W, Rattanachetkul S, Wanun T, Utaisincharoen P, Sirisinha S. Burkholderia pseudomallei induces cell fusion and actin-associated membrane protrusion: a possible mechanism for cell-to-cell spreading. Infect Immun. 2000;68(9):5377–84.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Natesan M, Corea E, Krishnananthasivam S, Sathkumara HD, Dankmeyer JL, Dyas BK, Amemiya K, De Silva AD, Ulrich RG. Calprotectin as a biomarker for melioidosis disease progression and management. J Clin Microbiol. 2017;55(4):1205–10.  https://doi.org/10.1128/JCM.02284-16.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Lau SK, Lee KC, Lo GC, Ding VS, Chow WN, Ke TY, Curreem SO, To KK, Ho DT, Sridhar S, Wong SC, Chan JF, Hung IF, Sze KH, Lam CW, Yuen KY, Woo PC. Metabolomic profiling of plasma from melioidosis patients using UHPLC-QTOF MS reveals novel biomarkers for diagnosis. Int J Mol Sci. 2016;17(3):307.  https://doi.org/10.3390/ijms17030307.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Wiersinga WJ, Wieland CW, Dessing MC, Chantratita N, Cheng AC, Limmathurotsakul D, Chierakul W, Leendertse M, Florquin S, de Vos AF, White N, Dondorp AM, Day NP, Peacock SJ, van der Poll T. Toll-like receptor 2 impairs host defense in gram-negative sepsis caused by Burkholderia pseudomallei (Melioidosis). PLoS Med. 2007;4(7):e248.  https://doi.org/10.1371/journal.pmed.0040248.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Utaisincharoen P, Tangthawornchaikul N, Kespichayawattana W, Chaisuriya P, Sirisinha S. Burkholderia pseudomallei interferes with inducible nitric oxide synthase (iNOS) production: a possible mechanism of evading macrophage killing. Microbiol Immunol. 2001;45(4):307–13.CrossRefPubMedGoogle Scholar
  65. 65.
    Kessler B, Rinchai D, Kewcharoenwong C, Nithichanon A, Biggart R, Hawrylowicz CM, Bancroft GJ, Lertmemongkolchai G. Interleukin 10 inhibits pro-inflammatory cytokine responses and killing of Burkholderia pseudomallei. Sci Rep. 2017;7:42791.  https://doi.org/10.1038/srep42791.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Sahl JW, Vazquez AJ, Hall CM, Busch JD, Tuanyok A, Mayo M, Schupp JM, Lummis M, Pearson T, Shippy K, Colman RE, Allender CJ, Theobald V, Sarovich DS, Price EP, Hutcheson A, Korlach J, LiPuma JJ, Ladner J, Lovett S, Koroleva G, Palacios G, Limmathurotsakul D, Wuthiekanun V, Wongsuwan G, Currie BJ, Keim P, Wagner DM. The effects of signal erosion and core genome reduction on the identification of diagnostic markers. MBio. 2016;7(5):e00846-16.  https://doi.org/10.1128/mBio.00846-16.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Hacker J, Carniel E. Ecological fitness, genomic islands and bacterial pathogenicity. A Darwinian view of the evolution of microbes. EMBO Rep. 2001;2(5):376–81.  https://doi.org/10.1093/embo-reports/kve097.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Bartpho T, Wongsurawat T, Wongratanacheewin S, Talaat AM, Karoonuthaisiri N, Sermswan RW. Genomic islands as a marker to differentiate between clinical and environmental Burkholderia pseudomallei. PLoS One. 2012;7(6):e37762.  https://doi.org/10.1371/journal.pone.0037762.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Ronning CM, Losada L, Brinkac L, Inman J, Ulrich RL, Schell M, Nierman WC, Deshazer D. Genetic and phenotypic diversity in Burkholderia: contributions by prophage and phage-like elements. BMC Microbiol. 2010;10:202.  https://doi.org/10.1186/1471-2180-10-202.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Gierok P, Kohler C, Steinmetz I, Lalk M. Burkholderia pseudomallei colony morphotypes show a synchronized metabolic pattern after acute infection. PLoS Negl Trop Dis. 2016;10(3):e0004483.  https://doi.org/10.1371/journal.pntd.0004483.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Al-Maleki AR, Mariappan V, Vellasamy KM, Tay ST, Vadivelu J. Altered proteome of Burkholderia pseudomallei colony variants induced by exposure to human lung epithelial cells. PLoS One. 2015;10(5):e0127398.  https://doi.org/10.1371/journal.pone.0127398.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Wikraiphat C, Saiprom N, Tandhavanant S, Heiss C, Azadi P, Wongsuvan G, Tuanyok A, Holden MT, Burtnick MN, Brett PJ, Peacock SJ, Chantratita N. Colony morphology variation of Burkholderia pseudomallei is associated with antigenic variation and O-polysaccharide modification. Infect Immun. 2015;83(5):2127–38.  https://doi.org/10.1128/IAI.02785-14.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Shea AA, Bernhards RC, Cote CK, Chase CJ, Koehler JW, Klimko CP, Ladner JT, Rozak DA, Wolcott MJ, Fetterer DP, Kern SJ, Koroleva GI, Lovett SP, Palacios GF, Toothman RG, Bozue JA, Worsham PL, Welkos SL. Two stable variants of Burkholderia pseudomallei strain MSHR5848 express broadly divergent in vitro phenotypes associated with their virulence differences. PLoS One. 2017;12(2):e0171363.  https://doi.org/10.1371/journal.pone.0171363.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Podnecky NL, Rhodes KA, Schweizer HP. Efflux pump-mediated drug resistance in. Burkholderia Front Microbiol. 2015;6:305.  https://doi.org/10.3389/fmicb.2015.00305.CrossRefPubMedGoogle Scholar
  75. 75.
    Schweizer HP. Mechanisms of antibiotic resistance in Burkholderia pseudomallei: implications for treatment of melioidosis. Future Microbiol. 2012;7(12):1389–99.  https://doi.org/10.2217/fmb.12.116.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Sarovich DS, Price EP, Von Schulze AT, Cook JM, Mayo M, Watson LM, Richardson L, Seymour ML, Tuanyok A, Engelthaler DM, Pearson T, Peacock SJ, Currie BJ, Keim P, Wagner DM. Characterization of ceftazidime resistance mechanisms in clinical isolates of Burkholderia pseudomallei from Australia. PLoS One. 2012;7(2):e30789.  https://doi.org/10.1371/journal.pone.0030789.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Webb JR, Price EP, Currie BJ, Sarovich DS. Loss of methyltransferase function and increased efflux activity leads to doxycycline resistance in Burkholderia pseudomallei. Antimicrob Agents Chemother. 2017;61(6):e00268-17.  https://doi.org/10.1128/AAC.00268-17.CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Barnes KB, Hamblin KA, Richards MI, Laws TR, Vente A, Atkins HS, Harding SV. Demonstrating the protective efficacy of the novel fluoroquinolone finafloxacin against an inhalational exposure to Burkholderia pseudomallei. Antimicrob Agents Chemother. 2017;61(7):e00082-17.  https://doi.org/10.1128/AAC.00082-17.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Reckseidler-Zenteno SL, DeVinney R, Woods DE. The capsular polysaccharide of Burkholderia pseudomallei contributes to survival in serum by reducing complement factor C3b deposition. Infect Immun. 2005;73(2):1106–15.  https://doi.org/10.1128/IAI.73.2.1106-1115.2005.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Holden MT, Titball RW, Peacock SJ, Cerdeño-Tárraga AM, Atkins T, Crossman LC, Pitt T, Churcher C, Mungall K, Bentley SD, Sebaihia M, Thomson NR, Bason N, Beacham IR, Brooks K, Brown KA, Brown NF, Challis GL, Cherevach I, Chillingworth T, Cronin A, Crossett B, Davis P, DeShazer D, Feltwell T, Fraser A, Hance Z, Hauser H, Holroyd S, Jagels K, Keith KE, Maddison M, Moule S, Price C, Quail MA, Rabbinowitsch E, Rutherford K, Sanders M, Simmonds M, Songsivilai S, Stevens K, Tumapa S, Vesaratchavest M, Whitehead S, Yeats C, Barrell BG, Oyston PC, Parkhill J. Genomic plasticity of the causative agent of melioidosis, Burkholderia pseudomallei. Proc Natl Acad Sci USA. 2004;101(39):14240–5.  https://doi.org/10.1073/pnas.0403302101.CrossRefPubMedGoogle Scholar
  81. 81.
    Reckseidler-Zenteno SL, Viteri DF, Moore R, Wong E, Tuanyok A, Woods DE. Characterization of the type III capsular polysaccharide produced by Burkholderia pseudomallei. J Med Microbiol. 2010;59. (Pt 12:1403–14.  https://doi.org/10.1099/jmm.0.022202-0.CrossRefPubMedGoogle Scholar
  82. 82.
    Woodman ME, Worth RG, Wooten RM. Capsule influences the deposition of critical complement C3 levels required for the killing of Burkholderia pseudomallei via NADPH-oxidase induction by human neutrophils. PLoS One. 2012;7(12):e52276.  https://doi.org/10.1371/journal.pone.0052276.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Borlee GI, Plumley BA, Martin KH, Somprasong N, Mangalea MR, Islam MN, Burtnick MN, Brett PJ, Steinmetz I, AuCoin DP, Belisle JT, Crick DC, Schweizer HP, Borlee BR. Genome-scale analysis of the genes that contribute to Burkholderia pseudomallei biofilm formation identifies a crucial exopolysaccharide biosynthesis gene cluster. PLoS Negl Trop Dis. 2017;11(6):e0005689.  https://doi.org/10.1371/journal.pntd.0005689.CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Gutierrez MG, Yoder-Himes DR, Warawa JM. Comprehensive identification of virulence factors required for respiratory melioidosis using Tn-seq mutagenesis. Front Cell Infect Microbiol. 2015;5:78.  https://doi.org/10.3389/fcimb.2015.00078.CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Dando SJ, Ipe DS, Batzloff M, Sullivan MJ, Crossman DK, Crowley M, Strong E, Kyan S, Leclercq SY, Ekberg JA, St John J, Beacham IR, Ulett GC. Burkholderia pseudomallei capsule exacerbates respiratory melioidosis but does not afford protection against antimicrobial signaling or bacterial killing in human olfactory ensheathing cells. Infect Immun. 2016;84(7):1941–56.  https://doi.org/10.1128/IAI.01546-15.CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Mulye M, Bechill MP, Grose W, Ferreira VP, Lafontaine ER, Wooten RM. Delineating the importance of serum opsonins and the bacterial capsule in affecting the uptake and killing of Burkholderia pseudomallei by murine neutrophils and macrophages. PLoS Negl Trop Dis. 2014;8(8):e2988.  https://doi.org/10.1371/journal.pntd.0002988.CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    AuCoin DP, Reed DE, Marlenee NL, Bowen RA, Thorkildson P, Judy BM, Torres AG, Kozel TR. Polysaccharide specific monoclonal antibodies provide passive protection against intranasal challenge with Burkholderia pseudomallei. PLoS One. 2012;7(4):e35386.  https://doi.org/10.1371/journal.pone.0035386.CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Mariappan V, Vellasamy KM, Vadivelu J. Host-adaptation of Burkholderia pseudomallei alters metabolism and virulence: a global proteome analysis. Sci Rep. 2017;7(1):9015.  https://doi.org/10.1038/s41598-017-09373-0.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Balder R, Lipski S, Lazarus JJ, Grose W, Wooten RM, Hogan RJ, Woods DE, Lafontaine ER. Identification of Burkholderia mallei and Burkholderia pseudomallei adhesins for human respiratory epithelial cells. BMC Microbiol. 2010;10:250.  https://doi.org/10.1186/1471-2180-10-250.CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Essex-Lopresti AE, Boddey JA, Thomas R, Smith MP, Hartley MG, Atkins T, Brown NF, Tsang CH, Peak IR, Hill J, Beacham IR, Titball RW. A type IV pilin, PilA, contributes to adherence of Burkholderia pseudomallei and virulence in vivo. Infect Immun. 2005;73(2):1260–4.  https://doi.org/10.1128/IAI.73.2.1260-1264.2005.CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Gori AH, Ahmed K, Martinez G, Masaki H, Watanabe K, Nagatake T. Mediation of attachment of Burkholderia pseudomallei to human pharyngeal epithelial cells by the asialoganglioside GM1-GM2 receptor complex. Am J Trop Med Hyg. 1999;61(3):473–5.CrossRefPubMedGoogle Scholar
  92. 92.
    Kanai K, Suzuki Y, Kondo E, Maejima Y, Miyamoto D, Suzuki T, Kurata T. Specific binding of Burkholderia pseudomallei cells and their cell-surface acid phosphatase to gangliotetraosylceramide (asialo GM1) and gangliotriaosylceramide (asialo GM2). Southeast Asian J Trop Med Public Health. 1997;28(4):781–90.PubMedGoogle Scholar
  93. 93.
    Comolli JC, Waite LL, Mostov KE, Engel JN. Pili binding to asialo-GM1 on epithelial cells can mediate cytotoxicity or bacterial internalization by Pseudomonas aeruginosa. Infect Immun. 1999;67(7):3207–14.PubMedPubMedCentralGoogle Scholar
  94. 94.
    Kang WT, Vellasamy KM, Chua EG, Vadivelu J. Functional characterizations of effector protein BipC, a type III secretion system protein, in Burkholderia pseudomallei pathogenesis. J Infect Dis. 2015;211(5):827–34.  https://doi.org/10.1093/infdis/jiu492.CrossRefPubMedGoogle Scholar
  95. 95.
    French CT, Toesca IJ, Wu TH, Teslaa T, Beaty SM, Wong W, Liu M, Schröder I, Chiou PY, Teitell MA, Miller JF. Dissection of the Burkholderia intracellular life cycle using a photothermal nanoblade. Proc Natl Acad Sci USA. 2011;108(29):12095–100.  https://doi.org/10.1073/pnas.1107183108.CrossRefPubMedGoogle Scholar
  96. 96.
    Kang WT, Vellasamy KM, Rajamani L, Beuerman RW, Vadivelu J. Burkholderia pseudomallei type III secreted protein BipC: role in actin modulation and translocation activities required for the bacterial intracellular lifecycle. PeerJ. 2016;4:e2532.  https://doi.org/10.7717/peerj.2532.CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Vander Broek CW, Zainal Abidin N, Stevens JM. BipC, a predicted Burkholderia pseudomallei type 3 secretion system translocator protein with actin binding activity. Front Cell Infect Microbiol. 2017;7:333.  https://doi.org/10.3389/fcimb.2017.00333.CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Schell MA, Ulrich RL, Ribot WJ, Brueggemann EE, Hines HB, Chen D, Lipscomb L, Kim HS, Mrázek J, Nierman WC, Deshazer D. Type VI secretion is a major virulence determinant in Burkholderia mallei. Mol Microbiol. 2007;64(6):1466–85.  https://doi.org/10.1111/j.1365-2958.2007.05734.x.CrossRefPubMedGoogle Scholar
  99. 99.
    Toesca IJ, French CT, Miller JF. The Type VI secretion system spike protein VgrG5 mediates membrane fusion during intercellular spread by pseudomallei group Burkholderia species. Infect Immun. 2014;82(4):1436–44.  https://doi.org/10.1128/IAI.01367-13.CrossRefPubMedPubMedCentralGoogle Scholar
  100. 100.
    Burtnick MN, Brett PJ, Harding SV, Ngugi SA, Ribot WJ, Chantratita N, Scorpio A, Milne TS, Dean RE, Fritz DL, Peacock SJ, Prior JL, Atkins TP, Deshazer D. The cluster 1 type VI secretion system is a major virulence determinant in Burkholderia pseudomallei. Infect Immun. 2011;79(4):1512–25.  https://doi.org/10.1128/IAI.01218-10.CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Chieng S, Mohamed R, Nathan S. Transcriptome analysis of Burkholderia pseudomallei T6SS identifies Hcp1 as a potential serodiagnostic marker. Microb Pathog. 2015;79:47–56.  https://doi.org/10.1016/j.micpath.2015.01.006.CrossRefPubMedGoogle Scholar
  102. 102.
    Kaestli M, Schmid M, Mayo M, Rothballer M, Harrington G, Richardson L, Hill A, Hill J, Tuanyok A, Keim P, Hartmann A, Currie BJ. Out of the ground: aerial and exotic habitats of the melioidosis bacterium Burkholderia pseudomallei in grasses in Australia. Environ Microbiol. 2012;14(8):2058–70.  https://doi.org/10.1111/j.1462-2920.2011.02671.x.CrossRefPubMedGoogle Scholar
  103. 103.
    Vietri N, DeShazer D. Melioidosis. Medical Aspects of Biological Warfare, 2007;147–166.Google Scholar
  104. 104.
    Rubin HL, Alexander AD, Yager RH. Melioidosis – a military medical problem? Mil Med. 1963;128:538–42.CrossRefPubMedGoogle Scholar
  105. 105.
    Sanford JP, Moore WL. Recrudescent melioidosis: a southeast asian legacy. Am Rev Respir Dis. 1971;104(3):452–3.  https://doi.org/10.1164/arrd.1971.104.3.452.CrossRefPubMedGoogle Scholar
  106. 106.
    Cox CD, Arbogast JL. Melioidosis. Am J Clin Pathol. 1945;15:567–70.CrossRefPubMedGoogle Scholar
  107. 107.
    Ngauy V, Lemeshev Y, Sadkowski L, Crawford G. Cutaneous melioidosis in a man who was taken as a prisoner of war by the Japanese during World War II. J Clin Microbiol. 2005;43(2):970–2.  https://doi.org/10.1128/jcm.43.2.970-972.2005.CrossRefPubMedPubMedCentralGoogle Scholar
  108. 108.
    Lim MK, Tan EH, Soh CS, Chang TL. Burkholderia pseudomallei infection in the Singapore Armed Forces from 1987 to 1994 – an epidemiological review. Ann Acad Med Singap. 1997;26(1):13–7.PubMedGoogle Scholar
  109. 109.
    Limmathurotsakul D, Jamsen K, Arayawichanont A, Simpson JA, White LJ, Lee SJ, Wuthiekanun V, Chantratita N, Cheng A, Day NP, Verzilli C, Peacock SJ. Defining the true sensitivity of culture for the diagnosis of melioidosis using Bayesian latent class models. PLoS One. 2010;5(8):e12485.  https://doi.org/10.1371/journal.pone.0012485.CrossRefPubMedPubMedCentralGoogle Scholar
  110. 110.
    Wuthiekanun V, Limmathurotsakul D, Wongsuvan G, Chierakul W, Teerawattanasook N, Teparrukkul P, Day NP, Peacock SJ. Quantitation of B. pseudomallei in clinical samples. Am J Trop Med Hyg. 2007;77(5):812–3.CrossRefPubMedGoogle Scholar
  111. 111.
    Short B. Melioidosis: an important emerging infectious disease – a military problem, 2002.Google Scholar
  112. 112.
    Houghton RL, Reed DE, Hubbard MA, Dillon MJ, Chen H, Currie BJ, Mayo M, Sarovich DS, Theobald V, Limmathurotsakul D, Wongsuvan G, Chantratita N, Peacock SJ, Hoffmaster AR, Duval B, Brett PJ, Burtnick MN, Aucoin DP. Development of a prototype lateral flow immunoassay (LFI) for the rapid diagnosis of melioidosis. PLoS Negl Trop Dis. 2014;8(3):e2727.  https://doi.org/10.1371/journal.pntd.0002727.CrossRefPubMedPubMedCentralGoogle Scholar
  113. 113.
    Nualnoi T, Norris MH, Tuanyok A, Brett PJ, Burtnick MN, Keim PS, Settles EW, Allender CJ, AuCoin DP. Development of immunoassays for Burkholderia pseudomallei typical and atypical lipopolysaccharide strain typing. Am J Trop Med Hyg. 2017;96(2):358–67.  https://doi.org/10.4269/ajtmh.16-0308.CrossRefPubMedPubMedCentralGoogle Scholar
  114. 114.
    Chantratita N, Meumann E, Thanwisai A, Limmathurotsakul D, Wuthiekanun V, Wannapasni S, Tumapa S, Day NP, Peacock SJ. Loop-mediated isothermal amplification method targeting the TTS1 gene cluster for detection of Burkholderia pseudomallei and diagnosis of melioidosis. J Clin Microbiol. 2008;46(2):568–73.  https://doi.org/10.1128/JCM.01817-07.CrossRefPubMedGoogle Scholar
  115. 115.
    Kaestli M, Richardson LJ, Colman RE, Tuanyok A, Price EP, Bowers JR, Mayo M, Kelley E, Seymour ML, Sarovich DS, Pearson T, Engelthaler DM, Wagner DM, Keim PS, Schupp JM, Currie BJ. Comparison of TaqMan PCR assays for detection of the melioidosis agent Burkholderia pseudomallei in clinical specimens. J Clin Microbiol. 2012;50(6):2059–62.  https://doi.org/10.1128/JCM.06737-11.CrossRefPubMedPubMedCentralGoogle Scholar
  116. 116.
    Michel PA, Lascols C, Gee JE, Weigel LM, Sue D. Rapid filter-based detection and culture of Burkholderia pseudomallei from small volumes of urine. J Clin Microbiol. 2017;55(9):2698–707.  https://doi.org/10.1128/JCM.00764-17.CrossRefPubMedPubMedCentralGoogle Scholar
  117. 117.
    Scott AE, Burtnick MN, Stokes MG, Whelan AO, Williamson ED, Atkins TP, Prior JL, Brett PJ. Burkholderia pseudomallei capsular polysaccharide conjugates provide protection against acute melioidosis. Infect Immun. 2014;82(8):3206–13.  https://doi.org/10.1128/IAI.01847-14.CrossRefPubMedPubMedCentralGoogle Scholar
  118. 118.
    Scott AE, Ngugi SA, Laws TR, Corser D, Lonsdale CL, D’Elia RV, Titball RW, Williamson ED, Atkins TP, Prior JL. Protection against experimental melioidosis following immunisation with a lipopolysaccharide-protein conjugate. J Immunol Res. 2014;2014:392170.  https://doi.org/10.1155/2014/392170.CrossRefPubMedPubMedCentralGoogle Scholar
  119. 119.
    Nieves W, Petersen H, Judy BM, Blumentritt CA, Russell-Lodrigue K, Roy CJ, Torres AG, Morici LA. A Burkholderia pseudomallei outer membrane vesicle vaccine provides protection against lethal sepsis. Clin Vaccine Immunol. 2014;21(5):747–54.  https://doi.org/10.1128/CVI.00119-14.CrossRefPubMedPubMedCentralGoogle Scholar
  120. 120.
    Tamigney Kenfack M, Mazur M, Nualnoi T, Shaffer TL, Ngassimou A, Blériot Y, Marrot J, Marchetti R, Sintiprungrat K, Chantratita N, Silipo A, Molinaro A, AuCoin DP, Burtnick MN, Brett PJ, Gauthier C. Deciphering minimal antigenic epitopes associated with Burkholderia pseudomallei and Burkholderia mallei lipopolysaccharide O-antigens. Nat Commun. 2017;8(1):115.  https://doi.org/10.1038/s41467-017-00173-8.CrossRefPubMedPubMedCentralGoogle Scholar
  121. 121.
    Zimmerman SM, Dyke JS, Jelesijevic TP, Michel F, Lafontaine ER, Hogan RJ. Antibodies against in vivo-expressed antigens are sufficient to protect against lethal aerosol infection with Burkholderia mallei and Burkholderia pseudomallei. Infect Immun. 2017;85(8):e00102-17.  https://doi.org/10.1128/IAI.00102-17.CrossRefPubMedPubMedCentralGoogle Scholar
  122. 122.
    Lin HH, Chen YS, Li YC, Tseng IL, Hsieh TH, Buu LM, Chen YL. Burkholderia multivorans acts as an antagonist against the growth of Burkholderia pseudomallei in soil. Microbiol Immunol. 2011;55(9):616–24.  https://doi.org/10.1111/j.1348-0421.2011.00365.x.CrossRefPubMedGoogle Scholar
  123. 123.
    Loutet SA, Valvano MA. A decade of Burkholderia cenocepacia virulence determinant research. Infect Immun. 2010;78(10):4088–100.  https://doi.org/10.1128/IAI.00212-10.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Kathryn J. Pflughoeft
    • 1
  • Derrick Hau
    • 1
  • Peter Thorkildson
    • 1
  • David P. AuCoin
    • 1
    Email author
  1. 1.Department of Microbiology and ImmunologyUniversity of Nevada, Reno School of MedicineRenoUSA

Personalised recommendations