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Research Article | Clinical Science and Epidemiology

Mycobacterium ulcerans Population Genomics To Inform on the Spread of Buruli Ulcer across Central Africa

Koen Vandelannoote, Delphin Mavinga Phanzu, Kapay Kibadi, Miriam Eddyani, Conor J. Meehan, Kurt Jordaens, Herwig Leirs, Françoise Portaels, Timothy P. Stinear, Simon R. Harris, Bouke C. de Jong
Brandi M. Limbago, Editor
Koen Vandelannoote
Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, BelgiumEvolutionary Ecology Group, University of Antwerp, Antwerp, Belgium
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Delphin Mavinga Phanzu
Institut Médical Evangélique, Kimpese, Democratic Republic of Congo
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Kapay Kibadi
Institut National de Recherche Biomédicale, Kinshasa, Democratic Republic of Congo
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Miriam Eddyani
Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium
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Conor J. Meehan
Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium
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  • ORCID record for Conor J. Meehan
Kurt Jordaens
Invertebrates Section, Royal Museum for Central Africa, Tervuren, Belgium
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Herwig Leirs
Evolutionary Ecology Group, University of Antwerp, Antwerp, Belgium
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Françoise Portaels
Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium
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Timothy P. Stinear
Department of Microbiology and Immunology, University of Melbourne, Melbourne, Victoria, Australia
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Simon R. Harris
Wellcome Trust Sanger Institute, Cambridge, United Kingdom
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Bouke C. de Jong
Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium
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Brandi M. Limbago
U.S. Centers for Disease Control and Prevention
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DOI: 10.1128/mSphere.00472-18
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ABSTRACT

Buruli ulcer is a neglected tropical disease of skin and subcutaneous tissue caused by infection with the pathogen Mycobacterium ulcerans. Many critical issues for disease control, such as understanding the mode of transmission and identifying source reservoirs of M. ulcerans, are still largely unknown. Here, we used genomics to reconstruct in detail the evolutionary trajectory and dynamics of M. ulcerans populations at a central African scale and at smaller geographical village scales. Whole-genome sequencing (WGS) data were analyzed from 179 M. ulcerans strains isolated from all Buruli ulcer foci in the Democratic Republic of the Congo, The Republic of Congo, and Angola that have ever yielded positive M. ulcerans cultures. We used both temporal associations and the study of the mycobacterial demographic history to estimate the contribution of humans as a reservoir in Buruli ulcer transmission. Our phylogeographic analysis revealed one almost exclusively predominant sublineage of M. ulcerans that arose in Central Africa and proliferated in its different regions of endemicity during the Age of Discovery. We observed how the best sampled endemic hot spot, the Songololo territory, became an area of endemicity while the region was being colonized by Belgium (1880s). We furthermore identified temporal parallels between the observed past population fluxes of M. ulcerans from the Songololo territory and the timing of health policy changes toward control of the Buruli ulcer epidemic in that region. These findings suggest that an intervention based on detecting and treating human cases in an area of endemicity might be sufficient to break disease transmission chains, irrespective of other reservoirs of the bacterium.

IMPORTANCE Buruli ulcer is a destructive skin and soft tissue infection caused by Mycobacterium ulcerans. The disease is characterized by progressive skin ulceration, which can lead to permanent disfigurement and long-term disability. Currently, the major hurdles facing disease control are incomplete understandings of both the mode of transmission and environmental reservoirs of M. ulcerans. As decades of spasmodic environmental sampling surveys have not brought us much closer to overcoming these hurdles, the Buruli ulcer research community has recently switched to using comparative genomics. The significance of our research is in how we used both temporal associations and the study of the mycobacterial demographic history to estimate the contribution of humans as a reservoir in Buruli ulcer transmission. Our approach shows that it might be possible to use bacterial population genomics to assess the impact of health interventions, providing valuable feedback for managers of disease control programs in areas where health surveillance infrastructure is poor.

  • Copyright © 2019 Vandelannoote et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Mycobacterium ulcerans Population Genomics To Inform on the Spread of Buruli Ulcer across Central Africa
Koen Vandelannoote, Delphin Mavinga Phanzu, Kapay Kibadi, Miriam Eddyani, Conor J. Meehan, Kurt Jordaens, Herwig Leirs, Françoise Portaels, Timothy P. Stinear, Simon R. Harris, Bouke C. de Jong
mSphere Feb 2019, 4 (1) e00472-18; DOI: 10.1128/mSphere.00472-18

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Mycobacterium ulcerans Population Genomics To Inform on the Spread of Buruli Ulcer across Central Africa
Koen Vandelannoote, Delphin Mavinga Phanzu, Kapay Kibadi, Miriam Eddyani, Conor J. Meehan, Kurt Jordaens, Herwig Leirs, Françoise Portaels, Timothy P. Stinear, Simon R. Harris, Bouke C. de Jong
mSphere Feb 2019, 4 (1) e00472-18; DOI: 10.1128/mSphere.00472-18
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KEYWORDS

bacterial pathogen transmission
Buruli ulcer
Democratic Republic of the Congo
microbial comparative population genomics
molecular evolution
phylogeography

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