B. PSEUDOMALLEI AND ENVIRONMENT

Burkholderia pseudomalleihas been isolated from soil, water and food contaminated with animal excreta (Currie et al. 2001). The main characteristics that support its survival in hostile environments are:

resistance to detergents/antiseptic compounds through its biodegradation capability, growth under nutrient deficiency, low pH, wide range of temperatures and dehydration, but susceptibility to UV irradiation (Dejsirilertet al., 1991; Chenet al., 2003; Inglis & Sagripanti, 2006). South-east Asia is one of the world endemic areas for B. pseudomallei and this fact is apparently linked to the rainy season (monsoons) and flooded rice fields that help transmit this pathogen as a result of direct contact with water or inhalation of aerosols supported by these climatic conditions (Wuthikanum et al., 1995).

Another described endemic area is northern Australia where clustered cases were associated with extreme weather events or environmental contamination (Chenget al.2006) (Figure 2.14.1). Water table movement, such as in cases of monsoonal rainy seasons, was speculated to have moved dormant or non-culturable state forms of this bacterium to the soil’s surface, which in turn was converted into a more replicative and infectious form (Currie, 2008).

B. pseudomallei’sinteraction with the protozoaAcanthamoebasp. (in a similar fashion described for another human pathogen, Legionella pneumophila, by internalization through phagocytosis and chronic infection) and pathogenicity to plants and larval insects is believed to facilitate its environmental survival (Inglis et al., 2000; Lee and Seleena, 1990). There are many factors that impact B. pseudomallei’s

b) chemical (soil chemistry, pH, vegetation, fertilizers, genetical diversity, etc.) (Thomas et al., 1979;

Wuthiekanun et al., 2009; Palasatien et al., 2009). A recent study demonstrated experimentally that B.

pseudomallei can survive salt stress through the alteration of secreted proteins (secretome) a process which may explain its environmental epidemiology (Pumiratet al., 2009). Kaestliet al.(2009) surveyed the Darwin area in tropical Australia for soil presence of B. pseudomallei in two habitats: undisturbed and environmentally manipulated areas. Significant association at undisturbed sites was found to be linked to areas rich in grasses, and at environmentally disturbed sites the presence of livestock animals, lower soil pH and different combinations of soil texture and color were the significant factors. The close association to grass and livestock animals in both habitats is probably linked to B. pseudomallei’s saprophytic characteristics and their excretion from infected animals (Figure 2.14.2).

B. pseudomallei’sability to survive and biodegrade extreme concentrations of phenol (1.5 g/l) in seven days was shown experimentally by Afzalet al.(2007) and in the context of other chemicals Galet al.(2004) found a hand cleanse detergent as the source of human contamination with this pathogen which confirms its biodegradation capability.

As already highlighted, B. pseudomallei was also identified as a plant pathogen (Lee et al.

2009); nevertheless, this species, owing to a facultative intracellular lifestyle articulated by its presence in various eukaryotes, was demonstrated to be present in arbuscular mycorrhizal fungus (AMF) sporesin vitro (Levy et al., 2009). AMF is a worldwide phenomenon of the highly evolved mutualistic relationship (symbiosis) between fungi and vascular plant, and therefore B. pseudomallei’s presence Figure 2.14.1. Global distribution of melioidosis (Burkholderia pseudomallei). (with permission from Currie, B.

J., Dance, D.A.B. & Cheng, A.C. (2008),Trans. R. Soc. Trop. Med. Hyg.102/S1, S1-S4.).*-documented temperate outbreaks of melioidosis: France; southeast Queensland, Australia; and southwest Western Australia

Melioidosis 93

is very important in understanding the ecology and environmental aspects of plant-soil and animals interactions.

Another study showed an interesting biochemical divergence (utilization of L-arabinose as substrate, Ara⁺gene controlled) between some soil and clinical isolates ofB. pseudomallei(clinical and some soil isolates were found to be Ara⁻). Arabinose is known to be one of the major components of hemicellulose and pectin found in plants that may explainB. pseudomallei’spathogenicity toward plants (by carrying theAra⁺gene) beside animals (Sirisinhaet al., 1998).

Wildlife animals were also shown to harborB. pseudomalleias identified in a batch of feral cynomolgus monkeys (Macaca fascicularis) imported to Britain from the Philippines (Danceet al., 1992).

Human migration as well imported work forces can also contribute to the spread of this disease as reported by Cahn et al. (2009) in relation to an agricultural worker from Thailand who was diagnosed with diabetes mellitus and melioidiosis in Israel. Finally, in the Northeast part of Thailand, Limmathurotsakulet al. (2010) performed a prospective cohort study on 2,243 patients identified with culture-confirmed melioidosis, admitted to a hospital in northeast Thailand between 1997 and 2006.

These authors found that diabetes mellitus was the strongest and most statistically relevant risk factor responsible for the rise over time in the melioidosis prevalence in Thailand as an endemic area. The Figure 2.14.2. Melioidosis transmission cycle and environmental factors involved inBurkholderia

pseudomalleisurvival

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2.14.2 REFERENCES

Afzal, M., Iqbal, S., Rauf, S. & Khalid, Z.M. (2007) Characteristics of phenol biodegradation in saline solutions by monocultures ofPseudomonas aeruginosaandPseudomonas pseudomallei. J. Hazard. Mater.149, 60–66.

Cahn, A., Koslowsky, B., Nir-Paz, R.,Temper, V., Hiller, N.et al.(2009) Imported Melioidosis, Israel, 2008.Emerging Infect. Dis.15, 1809–1811.

Chen, Y.S., Chen, S.C., Kao, C.M. & Chen, Y.L. (2003) Effects of Soil pH, Temperature and Water Content on the Growth ofBurkholderia pseudomallei. Folia Microbiol.48, 253–256.

Cheng, A.C. & Currie, B.J. (2005) Melioidosis: epidemiology, pathophysiology, and management.Clin. Microbiol.

Rev.18, 383–416.

Cheng, A.C., Jacups, S.P., Gal, D., Mayo, M. & Currie, B.J. (2006) Extreme weather events and environmental contamination are associated with case-clusters of melioidosis in the northern territory of Australia. Int J Epidemiol35,323–329.

Currie, B.J. (2008) Advances and remaining uncertainties in the epidemiology ofBurkholderia pseudomallei and melioidosis.Trans. R. Soc. Trop. Med. Hyg.102, 225–227.

Currie, B.J., Dance, D.A.B. & Cheng, A.C. (2008) The global distribution of Burkholderia pseudomallei and melioidosis: an update.Trans. R. Soc. Trop. Med. Hyg.102/S1, S1-S4.

Currie, B.J., Mayo, M., Anstey, N.M., Donohoe, P., Haase, A. & Kemp, D.J. (2001) A cluster of melioidosis cases from an endemic region is clonal and is linked to the water supply using molecular typing ofBurkholderia pseudomallei isolates.Am. J. Trop. Med. Hyg.,65, 177–179.

Dance, D.A., King, C., Aucken, H., Knott, C.D., West, P.G. & Pitt, T.L. (1992) An outbreak of melioidosis in imported primates in Britain.Vet. Rec.130, 525–529.

Dejsirilert, S., Kondo, E., Chiewslip, D. & Kanai, K. (1991) Growth and survival ofPseudomonas pseudomalleiin acidic environments.Jpn. J. Med. Sci. Biol.44, 63–74.

Gal, D., Mayo, M., Smith-Vaughan, H., Dasari, P., McKinnon, M., Jacups, S.P., Urquhart, A.I., Hassell, M. & Currie, B.

J. (2004) Contamination of hand wash detergent linked to occupationally acquired melioidosis.Am. J. Trop. Med.

Hyg.71, 360–362.

Inglis, T.J., Mee, B. & Chang, B. 2001. The environmental microbiology of melioidosis.Rev. Med. Microbiol.12,13– 20.

Inglis, T.J.J. & Sagripanti, J-L. (2006) Environmental factors that affect the survival and persistence ofBurkholderia pseudomallei. Appl. Environ. Microbiol.72, 6865–6875.

Inglis, T.J.J., Rigby, P., Robertson, T.A., Dutton, N.S., Henderson, M. & Chang, B.J. (2000) Interaction between Burkholderia pseudomallei and Acanthamoeba species results in coiling phagocytosis, endamebic bacterial survival, and escape.Infect. Immun.68, 1681–1686.

Kaestli, M., Mayo, M., Harrington, G., Ward, L., Watt, F.et al.(2009) Landscape changes influence the occurrence of the melioidosis bacteriumBurkholderia pseudomalleiin soil in northern Australia.PLoS Negl Trop Dis3(1): e364.

doi:10.1371/journal.pntd.0000364.

Ketterer, P.J., Donald, B. & Rogers, R.J. (1975) Bovine melioidosis in South-Eastern Queensland.Aust. Vet. J.51, 395– 398.

Lee, H.L. & Seleena, P. (1990) Isolation of indigenous larvicidal microbial control agents of mosquitos: the Malaysian experience.Southeast Asian J. Trop. Med. Public Health21, 281–287.

Lee, Y.H., Chen, Y., Ouyang, X. & Gan, Y.H. (2010). Identification of tomato plant as a novel host model for Burkholderia pseudomallei.BMC Microbiol.10:28.

Levy, A., Merritt, A.J., Mayo, M.J., Chang, B.J., Abbott, L.K. & Inglis, T.J.J. (2009) Association between Burkholderia species and arbuscular mycorrhizal fungus spores in soil.Soil Biol. Biochem.41, 1757–1759.

Limmathurotsakul, D., Wongratanacheewin, S., Teerawattanasook, N., Wongsuvan, G., Chaisuksant, S.et al.(2010) Increasing incidence of human melioidosis in northeast Thailand.Am. J. Trop. Med. Hyg.,82, 1113–1117.

Palasatien, S., Lertsirivorakul, R., Royros, P., Wongratanacheewin, S., & Sermswan, R.W. (2008) Soil physicochemical properties related to the presence ofBurkholderia pseudomallei. Trans. R. Soc. Trop. Med.

Hyg.102/S1, S5-S9.

Melioidosis 95

Pumirat, P., Saetun, P., Sinchaikul, S., Chen, S-T., Korbsrisate, S. & Thongboonkerd, V. (2009) Altered secretome of Burkholderia pseudomallei induced by salt stress.Biochim. Biophys. Acta1794, 898–904.

Sirisinha, S., Anuntagool, N., Intachote, P., Wuthiekanun, V., Puthucheary, S.D.et al.(1998) Antigenic differences between clinical and environmental isolates ofBurkholderia pseudomallei. Microbiol. Immunol.42, 731–737.

Thomas, A.D., Forbes-Faulkner, J. & Parker, M. (1979) Isolation of Pseudomonas pseudomallei from clay layers at defined depths.Am. J. Epidemiol.110, 515–521.

Wuthiekanun, V., Limmathurotsakul, D., Chantratita, N., Feil, E.J., Day, N.P.J., et al. (2009) Burkholderia pseudomalleiis genetically diverse in agricultural land in northeast Thailand.PLoS Negl Trop Dis3(8): e496.

doi:10.1371/journal.pntd.0000496.

Wuthiekanun, V., Smith, M.D., Dance, D.A. & White, N.J. (1995) Isolation ofPseudomonas pseudomalleifrom soil in north-eastern Thailand.Trans. R. Soc. Trop. Med. Hyg.89, 41–43.

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Chapter 2.15