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A major role for mammals in the ecology of Mycobacterium ulcerans.

ABSTRACT: Mycobacterium ulcerans is the causative agent of Buruli ulcer (BU), a destructive skin disease found predominantly in sub-Saharan Africa and south-eastern Australia. The precise mode(s) of transmission and environmental reservoir(s) remain unknown, but several studies have explored the role of aquatic invertebrate species. The purpose of this study was to investigate the environmental distribution of M. ulcerans in south-eastern Australia.A range of environmental samples was collected from Point Lonsdale (a small coastal town southwest of Melbourne, Australia, endemic for BU) and from areas with fewer or no reported incident cases of BU. Mycobacterium ulcerans DNA was detected at low levels by real-time PCR in soil, sediment, water residue, aquatic plant biofilm and terrestrial vegetation collected in Point Lonsdale. Higher levels of M. ulcerans DNA were detected in the faeces of common ringtail (Pseudocheirus peregrinus) and common brushtail (Trichosurus vulpecula) possums. Systematic testing of possum faeces revealed that M. ulcerans DNA could be detected in 41% of faecal samples collected in Point Lonsdale compared with less than 1% of faecal samples collected from non-endemic areas (p<0.0001). Capture and clinical examination of live possums in Point Lonsdale validated the accuracy of the predictive value of the faecal surveys by revealing that 38% of ringtail possums and 24% of brushtail possums had laboratory-confirmed M. ulcerans skin lesions and/or M. ulcerans PCR positive faeces. Whole genome sequencing revealed an extremely close genetic relationship between human and possum M. ulcerans isolates.The prevailing wisdom is that M. ulcerans is an aquatic pathogen and that BU is acquired by contact with certain aquatic environments (swamps, slow-flowing water). Now, after 70 years of research, we propose a transmission model for BU in which terrestrial mammals are implicated as reservoirs for M. ulcerans.

SUBMITTER: Fyfe JA

PROVIDER: S-EPMC2919402 | biostudies-literature | 2010 Aug

REPOSITORIES: biostudies-literature

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A major role for mammals in the ecology of Mycobacterium ulcerans.

Fyfe Janet A M JA Lavender Caroline J CJ Handasyde Kathrine A KA Legione Alistair R AR O'Brien Carolyn R CR Stinear Timothy P TP Pidot Sacha J SJ Seemann Torsten T Benbow M Eric ME Wallace John R JR McCowan Christina C Johnson Paul D R PD

PLoS neglected tropical diseases 20100810 8

<h4>Background</h4>Mycobacterium ulcerans is the causative agent of Buruli ulcer (BU), a destructive skin disease found predominantly in sub-Saharan Africa and south-eastern Australia. The precise mode(s) of transmission and environmental reservoir(s) remain unknown, but several studies have explored the role of aquatic invertebrate species. The purpose of this study was to investigate the environmental distribution of M. ulcerans in south-eastern Australia.<h4>Methodology/principal findings</h4 ...[more]

PMID: 20706592

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Project description:Disease ecology is a rapidly growing subdiscipline, and mammals and their parasites feature prominently in both historical and more recent research efforts. Nevertheless, the diversity of topics explored, and those not well explored, has not been systematically assessed. We conducted a systematic review of the published scientific literature in disease ecology of mammals and subjected the collection of original and review articles identified to a topic modeling approach, which is based on the words used in the published texts and their contexts (i.e., the frequency and strength of their semantic relationships with one another). In addition to concept maps identifying the most prominent research themes, we identified eight (not mutually exclusive) subcategories of studies, including experimental, theoretical, comparative, behavioral, immunological-microbiological, biogeographic-macroecological, vector-focused (e.g., mosquitoes), and disturbance-focused. The most prominent themes arising in review papers included the ecology of zoonotic diseases transmitted from non-human mammals, comparisons of pathogen prevalence between mammalian species, and pathogen discovery-disease surveillance studies, particularly of marine mammals and bats. For the original articles, the most prominent themes included ecology of rodent-transmitted viral and bacterial diseases and the population biology of zoonotic hosts. Most studies used comparative or descriptive approaches to investigate mammal-pathogen-disease relationships at a local scale, focusing on vector-borne diseases. Experimental, modeling, immunological, and behavioral approaches were strikingly underrepresented. Topics of strong conceptual importance, but that are underrepresented in the current literature, include: 1) the effects of the population density of mammalian hosts, and manipulations of density, on pathogen transmission; 2) macroecological studies that quantify effects of mammalian host species on parasite abundance and prevalence; and 3) effects of climate change on physiological and behavioral processes relevant to mammal-parasite interactions.

Project description:BackgroundThe reservoir and mode of transmission of Mycobacterium ulcerans, the causative agent of Buruli ulcer, still remain a mystery. It has been suggested that M. ulcerans persists with difficulty as a free-living organism due to its natural fragility and inability to withstand exposure to direct sunlight, and thus probably persists within a protective host environment.Methodology/principal findingsWe investigated the role of free-living amoebae as a reservoir of M. ulcerans by screening the bacterium in free-living amoebae (FLA) cultures isolated from environmental specimens using real-time PCR. We also followed the survival of M. ulcerans expressing green fluorescence protein (GFP) in Acanthameoba castellanii by flow cytometry and observed the infected cells using confocal and transmission electron microscopy for four weeks in vitro. IS2404 was detected by quantitative PCR in 4.64% of FLA cultures isolated from water, biofilms, detritus and aerosols. While we could not isolate M. ulcerans, 23 other species of mycobacteria were cultivated from inside FLA and/or other phagocytic microorganisms. Laboratory experiments with GFP-expressing M. ulcerans in A. castellani trophozoites for 28 days indicated the bacteria did not replicate inside amoebae, but they could remain viable at low levels in cysts. Transmission electron microscopy of infected A. castellani confirmed the presence of bacteria within both trophozoite vacuoles and cysts. There was no correlation of BU notification rate with detection of the IS2404 in FLA (r = 0.07, n = 539, p = 0.127).Conclusion/significanceThis study shows that FLA in the environment are positive for the M. ulcerans insertion sequence IS2404. However, the detection frequency and signal strength of IS2404 positive amoabae was low and no link with the occurrence of BU was observed. We conclude that FLA may host M. ulcerans at low levels in the environment without being directly involved in the transmission to humans.

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A major role for mammals in the ecology of Mycobacterium ulcerans.

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A major role for mammals in the ecology of Mycobacterium ulcerans.

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