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      Systematic Review and Consensus Guidelines for Environmental Sampling of Burkholderia pseudomallei

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          Abstract

          Background

          Burkholderia pseudomallei, a Tier 1 Select Agent and the cause of melioidosis, is a Gram-negative bacillus present in the environment in many tropical countries. Defining the global pattern of B. pseudomallei distribution underpins efforts to prevent infection, and is dependent upon robust environmental sampling methodology. Our objective was to review the literature on the detection of environmental B. pseudomallei, update the risk map for melioidosis, and propose international consensus guidelines for soil sampling.

          Methods/Principal Findings

          An international working party (Detection of Environmental Burkholderia pseudomallei Working Party (DEBWorP)) was formed during the VIth World Melioidosis Congress in 2010. PubMed (January 1912 to December 2011) was searched using the following MeSH terms: pseudomallei or melioidosis. Bibliographies were hand-searched for secondary references. The reported geographical distribution of B. pseudomallei in the environment was mapped and categorized as definite, probable, or possible. The methodology used for detecting environmental B. pseudomallei was extracted and collated. We found that global coverage was patchy, with a lack of studies in many areas where melioidosis is suspected to occur. The sampling strategies and bacterial identification methods used were highly variable, and not all were robust. We developed consensus guidelines with the goals of reducing the probability of false-negative results, and the provision of affordable and ‘low-tech’ methodology that is applicable in both developed and developing countries.

          Conclusions/Significance

          The proposed consensus guidelines provide the basis for the development of an accurate and comprehensive global map of environmental B. pseudomallei.

          Author Summary

          Melioidosis is a serious infectious disease caused by the Tier 1 selected agent and Gram-negative environmental saprophyte, Burkholderia pseudomallei. The organism is commonly found in soil and water in melioidosis endemic areas. Infection in humans occurs following bacterial inoculation, inhalation or ingestion. There is a striking lack of accurate information on the global risk of melioidosis, something that could be determined from the global distribution of environmental B. pseudomallei. Soil sampling to detect the presence of B. pseudomallei has been ad hoc, poorly standardized, and the available information poorly collated. Negative studies are almost never reported, and there is no published review on this topic. We responded to this problem during the VI th World Melioidosis Congress held in Townsville, Australia in December 2010 by forming the ‘Detection of Environmental Burkholderia pseudomallei Working Party (DEBWorP)’. We have since worked together to undertake a systematic review, map the available information, and reach a consensus on low cost methods for the detection of environmental B. pseudomallei. Our goal is to promote the use of these consensus methods and encourage people worldwide to participate in an effort to produce a comprehensive global map of environmental B. pseudomallei.

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          Most cited references89

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          Increasing Incidence of Human Melioidosis in Northeast Thailand

          Melioidosis is a serious community-acquired infectious disease caused by the Gram-negative environmental bacterium Burkholderia pseudomallei. A prospective cohort study identified 2,243 patients admitted to Sappasithiprasong Hospital in northeast Thailand with culture-confirmed melioidosis between 1997 and 2006. These data were used to calculate an average incidence rate for the province of 12.7 cases of melioidosis per 100,000 people per year. Incidence increased incrementally from 8.0 (95% confidence interval [CI] = 7.2–10.0) in 2000 to 21.3 (95% CI = 19.2–23.6) in 2006 (P < 0.001; χ2 test for trend). Male sex, age ≥ 45 years, and either known or undiagnosed diabetes were independent risk factors for melioidosis. The average mortality rate from melioidosis over the study period was 42.6%. The minimum estimated population mortality rate from melioidosis in 2006 was 8.63 per 100,000 people (95% CI = 7.33–10.11), the third most common cause of death from infectious diseases in northeast Thailand after human immunodeficiency virus (HIV)/acquired immunodeficiency syndrome (AIDS) and tuberculosis.
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            Multilocus sequence typing and evolutionary relationships among the causative agents of melioidosis and glanders, Burkholderia pseudomallei and Burkholderia mallei.

            A collection of 147 isolates of Burkholderia pseudomallei, B. mallei, and B. thailandensis was characterized by multilocus sequence typing (MLST). The 128 isolates of B. pseudomallei, the causative agent of melioidosis, were obtained from diverse geographic locations, from humans and animals with disease, and from the environment and were resolved into 71 sequence types. The utility of the MLST scheme for epidemiological investigations was established by analyzing isolates from captive marine mammals and birds and from humans in Hong Kong with melioidosis. MLST gave a level of resolution similar to that given by pulsed-field gel electrophoresis and identified the same three clones causing disease in animals, each of which was also associated with disease in humans. The average divergence between the alleles of B. thailandensis and B. pseudomallei was 3.2%, and there was no sharing of alleles between these species. Trees constructed from differences in the allelic profiles of the isolates and from the concatenated sequences of the seven loci showed that the B. pseudomallei isolates formed a cluster of closely related lineages that were fully resolved from the cluster of B. thailandensis isolates, confirming their separate species status. However, isolates of B. mallei, the causative agent of glanders, recovered from three continents over a 30-year period had identical allelic profiles, and the B. mallei isolates clustered within the B. pseudomallei group of isolates. Alleles at six of the seven loci in B. mallei were also present within B. pseudomallei isolates, and B. mallei is a clone of B. pseudomallei that, on population genetics grounds, should not be given separate species status.
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              The global distribution of Burkholderia pseudomallei and melioidosis: an update.

              While Southeast Asia and northern Australia are well recognized as the major endemic regions for melioidosis, recent reports have expanded the endemic zone. Severe weather events and environmental disasters such as the 2004 Asian tsunami have unmasked locations of sporadic cases and have reconfirmed endemicity in Indonesia. The endemic region now includes the majority of the Indian subcontinent, southern China, Hong Kong and Taiwan. Sporadic cases have occurred in Brazil and elsewhere in the Americas and in island communities such as New Caledonia, in the Pacific Ocean, and Mauritius in the Indian Ocean. Some of the factors that are critical to further elucidating the global distribution of Burkholderia pseudomallei and melioidosis include improved access to diagnostic laboratory facilities and formal confirmation of the identity of bacterial isolates from suspected cases.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                March 2013
                21 March 2013
                : 7
                : 3
                : e2105
                Affiliations
                [1 ]Department of Tropical Hygiene, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
                [2 ]Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
                [3 ]Wellcome Trust-Mahosot Hospital-Oxford Tropical Medicine Research Collaboration, Microbiology Laboratory, Mahosot Hospital, Vientiane, Lao People's Democratic Republic
                [4 ]Centre for Clinical Vaccinology and Tropical Medicine, Nuffield Department of Clinical Medicine, University of Oxford, Oxford, United Kingdom
                [5 ]Menzies School of Health Research and Northern Territory Clinical School, Royal Darwin Hospital, Darwin, Northern Territory, Australia
                [6 ]Microbiology and Immunology, James Cook University, Townsville, Australia
                [7 ]Center for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, Arizona, United States of America
                [8 ]Department of Biological Sciences, Northern Arizona University, Flagstaff, Arizona, United States of America
                [9 ]Oxford University Clinical Research Unit, Hanoi, Vietnam
                [10 ]DSO National Laboratories, Singapore, Singapore
                [11 ]Department of Microbiology, Kasturba Medical College, Manipal University, Manipal, Karnataka, India
                [12 ]Research and Evaluation Department, Duke-NUS Graduate Medical School Singapore, Singapore
                [13 ]Friedrich Loeffler Institute of Medical Microbiology, Ernst Moritz Arndt University of Greifswald, Greifswald, Germany
                [14 ]Department of Medicine, Cambridge University, Addenbrooke's Hospital, Cambridge, United Kingdom
                [15 ]Department of Microbiology and Immunology, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand
                Oxford University Clinical Research Unit, Viet Nam
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: DL DABD BJC SJP. Performed the experiments: DL DABD. Analyzed the data: DL DABD BJC SJP. Contributed reagents/materials/analysis tools: DL DABD VW MK MM JW DMW AT HW TYC CM SP NPJD IS BJC SJP. Wrote the paper: DL DABD BJC SJP.

                Article
                PNTD-D-12-00823
                10.1371/journal.pntd.0002105
                3605150
                23556010
                908e5093-6b0f-4743-92bc-197dbe01a719
                Copyright @ 2013

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 26 June 2012
                : 28 January 2013
                Page count
                Pages: 11
                Funding
                This study was funded by the Wellcome Trust. DL is supported by the Wellcome Trust (090219/Z/09/Z). SJP is supported by the NIHR Cambridge Biomedical Research Centre. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine
                Infectious Diseases
                Bacterial Diseases
                Burkholderia Infection
                Melioidosis

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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