Dataset Information

Topography and land cover of watersheds predicts the distribution of the environmental pathogen Mycobacterium ulcerans in aquatic insects.

ABSTRACT:

Background

An understanding of the factors driving the distribution of pathogens is useful in preventing disease. Often we achieve this understanding at a local microhabitat scale; however the larger scale processes are often neglected. This can result in misleading inferences about the distribution of the pathogen, inhibiting our ability to manage the disease. One such disease is Buruli ulcer, an emerging neglected tropical disease afflicting many thousands in Africa, caused by the environmental pathogen Mycobacterium ulcerans. Herein, we aim to describe the larger scale landscape process describing the distribution of M. ulcerans.

Methodology

Following extensive sampling of the community of aquatic macroinvertebrates in Cameroon, we select the 5 dominant insect Orders, and conduct an ecological niche model to describe how the distribution of M. ulcerans positive insects changes according to land cover and topography. We then explore the generalizability of the results by testing them against an independent dataset collected in a second endemic region, French Guiana.

Principal findings

We find that the distribution of the bacterium in Cameroon is accurately described by the land cover and topography of the watershed, that there are notable seasonal differences in distribution, and that the Cameroon model does not predict the distribution of M. ulcerans in French Guiana.

Conclusions/significance

Future studies of M. ulcerans would benefit from consideration of local structure of the local stream network in future sampling, and further work is needed on the reasons for notable differences in the distribution of this species from one region to another. This work represents a first step in the identification of large-scale environmental drivers of this species, for the purposes of disease risk mapping.

SUBMITTER: Carolan K

PROVIDER: S-EPMC4222759 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Topography and land cover of watersheds predicts the distribution of the environmental pathogen Mycobacterium ulcerans in aquatic insects.

Carolan Kevin K Garchitorena Andres A García-Peña Gabriel E GE Morris Aaron A Landier Jordi J Fontanet Arnaud A Le Gall Philippe P Texier Gaëtan G Marsollier Laurent L Gozlan Rodolphe E RE Eyangoh Sara S Lo Seen Danny D Guégan Jean-Francois JF

PLoS neglected tropical diseases 20141106 11

<h4>Background</h4>An understanding of the factors driving the distribution of pathogens is useful in preventing disease. Often we achieve this understanding at a local microhabitat scale; however the larger scale processes are often neglected. This can result in misleading inferences about the distribution of the pathogen, inhibiting our ability to manage the disease. One such disease is Buruli ulcer, an emerging neglected tropical disease afflicting many thousands in Africa, caused by the envi ...[more]

PMID: 25375173

Similar Datasets

Project description:BackgroundBiting aquatic insects belonging to the order Hemiptera have been suggested as potential vectors of Mycobacterium ulcerans in endemic areas for Buruli ulcer (BU). If this is the case, these insects would be expected to co-exist with M. ulcerans in the same geographical areas. Here, we studied the geographical distribution of six aquatic Hemiptera families that are thought to be vectors of M. ulcerans and explored their potential geographical overlapping with communities reporting BU cases in endemic countries.MethodsWe have developed ensemble ecological models of predicted distribution for six families of the Hemiptera (Naucoridae, Belostomatidae, Notonectidae, Nepidae, Corixidae and Gerridae) applying a robust modelling framework over a collection of recorded presences and a suite of environmental and topographical factors. Ecological niche factor analysis (ENFA) was first used to identify factors that best described the ecological niches for each hemipteran family. Finally, we explored the potential geographical co-occurrence of these insects and BU in two endemic countries, Cameroon and Ghana.ResultsSpecies of the families Naucoridae and Belostomatidae, according to our models, are widely distributed across Africa, although absent from drier and hotter areas. The other two families of biting Hemiptera, the Notonectidae and Nepidae, would have a more restricted distribution, being more predominant in western and southern Africa. All these four families of biting water bugs are widely distributed across coastal areas of West Africa. They would thrive in areas where annual mean temperature varies between 15-22 °C, with moderate annual precipitation (i.e. 350-1000 mm/annual) and near to water courses. Species of all hemipteran families show preference for human-made environments such as agricultural landscapes and urbanized areas. Finally, our analysis suggests that M. ulcerans and species of these aquatic insects might coexist in the same ecological niches, although there would be variation in species diversity between BU endemic areas.ConclusionsOur findings predict the geographical co-existence of some species of aquatic hemipteran families and BU. Considering the existing biological evidence that points to some of these aquatic insects as potential phoretic vectors of M. ulcerans, its presence in BU endemic areas should be considered a risk factor. The ecological models here presented may be helpful to inform future environmental based models intended to delineate the potential geographical distribution of BU in the African region.

Project description:BackgroundBuruli ulcer is a severe human skin disease caused by Mycobacterium ulcerans. This disease is primarily diagnosed in West Africa with increasing incidence. Antimycobacterial drug therapy is relatively effective during the preulcerative stage of the disease, but surgical excision of lesions with skin grafting is often the ultimate treatment. The mode of transmission of this Mycobacterium species remains a matter of debate, and relevant interventions to prevent this disease lack (i) the proper understanding of the M. ulcerans life history traits in its natural aquatic ecosystem and (ii) immune signatures that could be correlates of protection. We previously set up a laboratory ecosystem with predatory aquatic insects of the family Naucoridae and laboratory mice and showed that (i) M. ulcerans-carrying aquatic insects can transmit the mycobacterium through bites and (ii) that their salivary glands are the only tissues hosting replicative M. ulcerans. Further investigation in natural settings revealed that 5%-10% of these aquatic insects captured in endemic areas have M. ulcerans-loaded salivary glands. In search of novel epidemiological features we noticed that individuals working close to aquatic environments inhabited by insect predators were less prone to developing Buruli ulcers than their relatives. Thus we set out to investigate whether those individuals might display any immune signatures of exposure to M. ulcerans-free insect predator bites, and whether those could correlate with protection.Methods and findingsWe took a two-pronged approach in this study, first investigating whether the insect bites are protective in a mouse model, and subsequently looking for possibly protective immune signatures in humans. We found that, in contrast to control BALB/c mice, BALB/c mice exposed to Naucoris aquatic insect bites or sensitized to Naucoris salivary gland homogenates (SGHs) displayed no lesion at the site of inoculation of M. ulcerans coated with Naucoris SGH components. Then using human serum samples collected in a Buruli ulcer-endemic area (in the Republic of Benin, West Africa), we assayed sera collected from either ulcer-free individuals or patients with Buruli ulcers for the titre of IgGs that bind to insect predator SGH, focusing on those molecules otherwise shown to be retained by M. ulcerans colonies. IgG titres were lower in the Buruli ulcer patient group than in the ulcer-free group.ConclusionsThese data will help structure future investigations in Buruli ulcer-endemic areas, providing a rationale for research into human immune signatures of exposure to predatory aquatic insects, with special attention to those insect saliva molecules that bind to M. ulcerans.

Dataset Information

Topography and land cover of watersheds predicts the distribution of the environmental pathogen Mycobacterium ulcerans in aquatic insects.

Background

Methodology

Principal findings

Conclusions/significance

Publications

Topography and land cover of watersheds predicts the distribution of the environmental pathogen Mycobacterium ulcerans in aquatic insects.

Similar Datasets

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