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      The Concentrations of Ambient Burkholderia Pseudomallei during Typhoon Season in Endemic Area of Melioidosis in Taiwan

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          Abstract

          Background

          Melioidosis is a severe bacterial infection caused by Burkholderia pseudomallei with a high case-fatality rate. Epidemiological and animal studies show the possibility of inhalation transmission. However, no B. pseudomallei concentrations in ambient air have been researched. Here, we developed a method to quantify ambient B. pseudomallei and then measured concentrations of ambient B. pseudomallei during the typhoon season and the non-typhoon season to determine the factors influencing ambient B. pseudomallei levels.

          Methods

          We quantified ambient B. pseudomallei by using a filter/real-time qPCR method in the Zoynan Region in Kaohsiung, southern Taiwan. Twenty-four hour samples were collected at a sampling rate of 20 L/min every day from June 11 to December 21, 2012 including during the typhoon season (June to September) and reference season (October to December).

          Results

          We successfully developed a filtration/real-time qPCR method to quantify ambient B. pseudomallei. To our knowledge, this is the first report describing concentrations of ambient B. pseudomallei. Ambient B. pseudomallei were only detected during the typhoon season when compared to the reference season. For the typhoons affecting the Zoynan Region, the positive rates of ambient B. pseudomallei were very high at 80% to 100%. During June to December, rainfall was positively correlated with ambient B. pseudomallei with a statistical significance. Sediment at a nearby pond significantly influenced the concentration of ambient B. pseudomallei. During the typhoon month, the typhoon was positively correlated with ambient B. pseudomallei whereas wind speed was reversely correlated with ambient B. pseudomallei.

          Conclusions

          Our data suggest the possibility of transmission of B. pseudomallei via inhalation during the typhoon season.

          Author Summary

          Melioidosis is a severe bacterial infection caused by Burkholderia pseudomallei with a high case-fatality rate. Epidemiological and animal studies show the possibility of inhalation transmission. However, no B. pseudomallei concentrations in ambient air have been researched. Here, we successfully developed a method to quantify ambient B. pseudomallei by using a filter/real-time qPCR method. Twenty-four hour samples were collected every day from June 11 to December 21, 2012 including during the typhoon season (June to September) and reference season (October to December) in the Zoynan Region in Kaohsiung, southern Taiwan. To our knowledge, this is the first report describing concentrations of B. pseudomallei in ambient air. For the typhoons affecting the Zoynan Region, the positive rates of ambient B. pseudomallei were very high. Our data imply the possibility of air transmission of Melioidosis during the typhoon season. In addition, ambient B. pseudomallei aerosolized from sediment of a nearby lake should be a concern as an important source of transmission. Our results could provide deeper insight into Melioidosis transmissibility and infection control.

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          Most cited references30

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          Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei.

          W. Joost Wiersinga, Tom van der Poll, Nicholas J. White … (2006)
          Burkholderia pseudomallei is a potential bioterror agent and the causative agent of melioidosis, a severe disease that is endemic in areas of Southeast Asia and Northern Australia. Infection is often associated with bacterial dissemination to distant sites, and there are many possible disease manifestations, with melioidosis septic shock being the most severe. Eradication of the organism following infection is difficult, with a slow fever-clearance time, the need for prolonged antibiotic therapy and a high rate of relapse if therapy is not completed. Mortality from melioidosis septic shock remains high despite appropriate antimicrobial therapy. Prevention of disease and a reduction in mortality and the rate of relapse are priority areas for future research efforts. Studying how the disease is acquired and the host-pathogen interactions involved will underpin these efforts; this review presents an overview of current knowledge in these areas, highlighting key topics for evaluation.
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            Increasing Incidence of Human Melioidosis in Northeast Thailand

            Direk Limmathurotsakul, Surasakdi Wongratanacheewin, Nittaya Teerawattanasook … (2010)
            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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              Melioidosis.

              N. White (2003)
              Melioidosis, which is infection with the gram-negative bacterium Burkholderia pseudomallei, is an important cause of sepsis in east Asia and northern Australia. In northeastern Thailand, melioidosis accounts for 20% of all community-acquired septicaemias, and causes death in 40% of treated patients. B pseudomallei is an environmental saprophyte found in wet soils. It mostly infects adults with an underlying predisposing condition, mainly diabetes mellitus. Melioidosis is characterised by formation of abscesses, especially in the lungs, liver, spleen, skeletal muscle, and prostate. In a third of paediatric cases in southeast Asia, the disease presents as parotid abscess. In northern Australia, 4% of patients present with brain stem encephalitis. Ceftazidime is the treatment of choice for severe melioidosis, but response to high dose parenteral treatment is slow (median time to abatement of fever 9 days). Maintenance antibiotic treatment is with a four-drug regimen of chloramphenicol, doxycycline, and trimethoprim-sulfamethoxazole, or with amoxicillin-clavulanate in children and pregnant women. However, even with 20 weeks' antibiotic treatment, 10% of patients relapse. With improvements in health care and diagnostic microbiology in endemic areas of Asia, and increased travel, melioidosis will probably be recognised increasingly during the next decade.
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                Author and article information

                Contributors
                Ruifu Yang: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS Negl Trop Dis
                Journal ID (iso-abbrev): PLoS Negl Trop Dis
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosntds
                Title: PLoS Neglected Tropical Diseases
                Publisher: Public Library of Science (San Francisco, USA )
                ISSN (Print): 1935-2727
                ISSN (Electronic): 1935-2735
                Publication date Collection: May 2014
                Publication date (Electronic): 29 May 2014
                Volume: 8
                Issue: 5
                Electronic Location Identifier: e2877
                Affiliations
                [1 ]Department of Biotechnology, National Kaohsiung Normal University, Kaohsiung, Taiwan
                [2 ]Department of Public Health, College of Health Science, Kaohsiung Medical University, Kaohsiung, Taiwan
                [3 ]Department of Pediatrics, Kaohsiung Medical University Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan
                [4 ]Epidemiology, Human Genetics, and Environmental Sciences, School of Public Health, University of Texas Health Science Center at Houston, Houston, Texas, United States of America
                [5 ]Disaster Prevention & Water Environment Research Center, National Chiao Tung University, Hsin Chu, Taiwan
                [6 ]Institute of Environmental Engineering, College of Engineering, National Sun Yat-Sen University, Kaohsiung, Taiwan
                Beijing Institute of Microbiology and Epidemiology, China
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: YLC YCY PSC. Performed the experiments: YLC YCY PSC CYY MSL. Analyzed the data: YLC YCY PSC CYY. Contributed reagents/materials/analysis tools: MSL CKH KDM PYW. Wrote the paper: YLC YCY PSC.

                Article
                Publisher ID: PNTD-D-14-00035
                DOI: 10.1371/journal.pntd.0002877
                PMC ID: 4038478
                PubMed ID: 24874950
                SO-VID: 01b1820e-18e5-4074-afef-4db64ed54809
                Copyright statement: Copyright @ 2014
                License:

                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
                Date received : 9 January 2014
                Date accepted : 4 April 2014
                Page count
                Pages: 11
                Funding
                This work was supported by two grants DOH 101-DC-1032 and DOH 102-DC-1202 from the Centers for Disease Control, Republic of China (Taiwan). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Subject: Research Article
                Subject: Medicine and Health Sciences
                Subject: Tropical Diseases
                Subject: Neglected Tropical Diseases
                Subject: Infectious Diseases

                ScienceOpen disciplines: Infectious disease & Microbiology
                Data availability:
                ScienceOpen disciplines: Infectious disease & Microbiology

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