Landscape and environmental influences on Mycobacterium ulcerans distribution among aquatic sites in Ghana

Abstract

Buruli ulcer, caused by Mycobacterium ulcerans, is highly endemic in West Africa. While the mode of transmission is unknown, many studies associate Buruli ulcer with different types of water exposure. We present results from the largest study to date to test for M. ulcerans in aquatic sites and identify environmental attributes associated with its presence. Environmental samples from 98 aquatic sites in the Greater Accra, Ashanti, and Volta regions of Ghana were tested for the presence of M. ulcerans DNA by polymerase chain reaction. The proportion of aquatic sites positive for M. ulcerans varied by region: Ashanti 66% (N = 39), Greater Accra 34% (N = 29), and Volta 0% (N = 30). We explored the spatial distribution of M. ulcerans positive and negative water bodies and found no significant clusters. We also determined both highly localized water attributes and broad scale remotely sensed land cover and terrain environmental characteristics associated with M. ulcerans presence through logistic regression. Our results concur with published results regarding conditions suitable for M. ulcerans growth and associations with Buruli ulcer disease burden with regards to water characteristics and disturbed environments, but differ from others with regards to spatial associations and topographic effects such as elevation and wetness. While our results suggest M. ulcerans is an environmental organism existing in a specific ecological niche, they also reveal variation in the elements defining this niche across the sites considered. In addition, despite the causal association between Buruli ulcer and M. ulcerans, we observed no significant statistical association between case reports of Buruli ulcer and presence of M. ulcerans in nearby waterbodies.

Fig 1. Locations of sampled aquatic sites in the Ashanti, Greater Accra, and Volta regions of Ghana.

Administrative districts that reported cases from 2004–07 are shaded in gray. Red symbols indicate M. ulcerans positive sites, whereas blue symbols indicate M. ulcerans negative sites. Triangles represent sites that reported cases 2004–07, and circles represent sites with no reported cases 2004–07.

Fig 2. Land use/land cover in study area.

Land use/land cover (LULC) from Landsat ETM+ imagery with 30 m resolution.

Fig 3. Land use/land cover distribution within buffers.

Boxplots show the distribution of percent of pixels characterized by a land use / land cover type within a specified buffer distance from 29 sites in Greater Accra, 39 sites in Ashanti, and 30 sites in Volta. Plots showing only isolated dots have more than 75% of values as zero; plots showing only a horizontal bar have all values as zero.

Fig 4. Ripley’s case-control K-function.

Clustering patterns for Greater Accra were assessed up to 15 km, and for Ashanti 45 km. Shown in the solid horizontal line, the expected value of this function is 0 under the assumption of complete spatial randomness. The bold line shows the observed difference between the transformed K functions of the positive and negative sites, and the dashed lines show the theoretical confidence bounds calculated by Monte Carlo simulation.

Fig 5. Depiction of results from best fitting model for land use / land cover variables.

Land cover representing most disturbed areas are associated with a higher probability of M. ulcerans presence compared to land cover representing less disturbed areas.

Fig 6. Empirical semivariogram of residuals.

Circles display the observed semivariance at distance d and dashed lines indicate Monte Carlo simulation envelopes.

Fig 7. Map of the predicted probability of M. ulcerans positive based on the best fitting model.

Blue circles represent sites that were actually M. ulcerans negative and red circles M. ulcerans positive. The size of the circle indicates the predicted probability of M. ulcerans positive, and shaded circles indicate poor fit (MU+ sites with low predicted probability or MU- sites with high predicted probability).