Mycobacterium africanum Is Associated with Patient Ethnicity in Ghana

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Abstract

Mycobacterium africanum is a member of the Mycobacterium tuberculosis complex (MTBC) and an important cause of human tuberculosis in West Africa that is rarely observed elsewhere. Here we genotyped 613 MTBC clinical isolates from Ghana, and searched for associations between the different phylogenetic lineages of MTBC and patient variables. We found that 17.1% (105/613) of the MTBC isolates belonged to M. africanum, with the remaining belonging to M. tuberculosis sensu stricto. No M. bovis was identified in this sample. M. africanum was significantly more common in tuberculosis patients belonging to the Ewe ethnic group (adjusted odds ratio: 3.02; 95% confidence interval: 1.67–5.47, p<0.001). Stratifying our analysis by the two phylogenetic lineages of M. africanum (i.e. MTBC Lineages 5 and 6) revealed that this association was mainly driven by Lineage 5 (also known as M. africanum West Africa 1). Our findings suggest interactions between the genetic diversity of MTBC and human diversity, and offer a possible explanation for the geographical restriction of M. africanum to parts of West Africa.

Author Summary

Tuberculosis remains one of the main global public health problems. Human tuberculosis is caused by bacteria known as the Mycobacterium tuberculosis complex (MTBC). The MTBC includes a variant called Mycobacterium africanum, which causes up to half of all tuberculosis cases in West Africa. For reasons unknown, M. africanum does not occur in other parts of the world. To explore the possible reasons for this geographic restriction of M. africanum, we analysed a large collection of bacterial strains isolated from tuberculosis patients in Ghana. We genetically characterized these bacterial isolates and collected relevant socio-demographic and epidemiological data. We found tuberculosis patients infected with M. africanum were more likely to belong to the Ewe ethnic group, compared to patients carrying other MTBC bacteria. The Ewes are indigenous inhabitants of coastal regions in West Africa that have previously been shown to harbour a high prevalence of M. africanum. Our findings support the hypothesis that different variants of MTBC have adapted to different human populations, and offer a possible explanation for the geographical restriction of M. africanum to West Africa.

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Most cited references 25

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Global phylogeography of Mycobacterium tuberculosis and implications for tuberculosis product development.

Sebastien Gagneux, Peter Small (2007)

New tools for controlling tuberculosis are urgently needed. Despite our emerging understanding of the biogeography of Mycobacterium tuberculosis, the implications for development of new diagnostics, drugs, and vaccines is unknown. M tuberculosis has a clonal genetic population structure that is geographically constrained. Evidence suggests strain-specific differences in virulence and immunogenicity in light of this global phylogeography. We propose a strain selection framework, based on robust phylogenetic markers, which will allow for systematic and comprehensive evaluation of new tools for tuberculosis control.

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SITVITWEB--a publicly available international multimarker database for studying Mycobacterium tuberculosis genetic diversity and molecular epidemiology.

Christophe Demay, Benjamin Liens, Thomas Burguière … (2012)

Among various genotyping methods to study Mycobacterium tuberculosis complex (MTC) genotypic polymorphism, spoligotyping and mycobacterial interspersed repetitive units-variable number of DNA tandem repeats (MIRU-VNTRs) have recently gained international approval as robust, fast, and reproducible typing methods generating data in a portable format. Spoligotyping constituted the backbone of a publicly available database SpolDB4 released in 2006; nonetheless this method possesses a low discriminatory power when used alone and should be ideally used in conjunction with a second typing method such as MIRU-VNTRs for high-resolution epidemiological studies. We hereby describe a publicly available international database named SITVITWEB which incorporates such multimarker data allowing to have a global vision of MTC genetic diversity worldwide based on 62,582 clinical isolates corresponding to 153 countries of patient origin (105 countries of isolation). We report a total of 7105 spoligotype patterns (corresponding to 58,180 clinical isolates) - grouped into 2740 shared-types or spoligotype international types (SIT) containing 53,816 clinical isolates and 4364 orphan patterns. Interestingly, only 7% of the MTC isolates worldwide were orphans whereas more than half of SITed isolates (n=27,059) were restricted to only 24 most prevalent SITs. The database also contains a total of 2379 MIRU patterns (from 8161 clinical isolates) from 87 countries of patient origin (35 countries of isolation); these were grouped in 847 shared-types or MIRU international types (MIT) containing 6626 isolates and 1533 orphan patterns. Lastly, data on 5-locus exact tandem repeats (ETRs) were available on 4626 isolates from 59 countries of patient origin (22 countries of isolation); a total of 458 different VNTR patterns were observed - split into 245 shared-types or VNTR International Types (VIT) containing 4413 isolates) and 213 orphan patterns. Datamining of SITVITWEB further allowed to update rules defining MTC genotypic lineages as well to have a new insight into MTC population structure and worldwide distribution at country, sub-regional and continental levels. At evolutionary level, the data compiled may be useful to distinguish the occasional convergent evolution of genotypes versus specific evolution of sublineages essentially influenced by adaptation to the host. This database is publicly available at: http://www.pasteur-guadeloupe.fr:8081/SITVIT_ONLINE. Copyright © 2012 Elsevier B.V. All rights reserved.

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Progression to active tuberculosis, but not transmission, varies by Mycobacterium tuberculosis lineage in The Gambia.

Martien Borgdorff, Maureen P Small, Timothy Awine … (2008)

There is considerable variability in the outcome of Mycobacterium tuberculosis infection. We hypothesized that Mycobacterium africanum was less likely than M. tuberculosis to transmit and progress to tuberculosis disease. In a cohort study of patients with tuberculosis and their household contacts in The Gambia, we categorized 1808 HIV-negative tuberculosis contacts according to exposure to M. tuberculosis or M. africanum. Positive skin test results indicated transmission, and development of tuberculosis during 2 years of follow-up indicated progression to disease. Transmission rates were similar, but rates of progression to disease were significantly lower in contacts exposed to M. africanum than in those exposed to M. tuberculosis (1.0% vs. 2.9%; hazard ratio [HR], 3.1 [95% confidence interval {CI}, 1.1-8.7]). Within M. tuberculosis sensu stricto, contacts exposed to a Beijing family strain were most likely to progress to disease (5.6%; HR relative to M. africanum, 6.7 [95% CI, 2.0-22]). M. africanum and M. tuberculosis transmit equally well to household contacts, but contacts exposed to M. africanum are less likely to progress to tuberculosis disease than those exposed to M. tuberculosis. The variable rate of progression by lineage suggests that tuberculosis variability matters in clinical settings and should be accounted for in studies evaluating tuberculosis vaccines and treatment regimens for latent tuberculosis infection.

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Author and article information

Contributors

Pamela L. C. Small: 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: January 2015

Publication date (Electronic): 8 January 2015

Volume: 9

Issue: 1

Electronic Location Identifier: e3370

Affiliations

[1 ]Bacteriology Department, Noguchi Memorial Institute for Medical Research, University of Ghana, Legon, Ghana

[2 ]Department of Medical Parasitology and Infection Biology, Swiss Tropical and Public Health Institute, Basel, Switzerland

[3 ]University of Basel, Basel, Switzerland

[4 ]Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Basel, Switzerland

University of Tennessee, United States of America

Author notes

* E-mail: sebastien.gagneux@ 123456unibas.ch

The authors have declared that no competing interests exist.

Conceived and designed the experiments: AAP DYM SG. Performed the experiments: AAP IDO SYA JF ED. Analyzed the data: AAP DYM JH SG. Contributed reagents/materials/analysis tools: DYM SB DS SG. Wrote the paper: AAP DYM SG.

Article

Publisher ID: PNTD-D-14-01295

DOI: 10.1371/journal.pntd.0003370

PMC ID: 4287525

PubMed ID: 25569290

SO-VID: b5d57661-ae67-426d-8ec5-f6ff699ce109

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 : 29 July 2014

Date accepted : 24 October 2014

Page count

Pages: 10

Funding

This study was supported by the Leverhulme-Royal Society Africa Award (grant AA080019 to DYM and SG), the National Tuberculosis Program Ghana, and the Swiss National Science Foundation (PP00P3_150750). AAP was supported by the “Amt für Ausbildungsbeiträge”, Canton of Basel, Switzerland and the government of Ghana. Funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Data Availability The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files.

ScienceOpen disciplines: Infectious disease & Microbiology

Data availability:

ScienceOpen disciplines: Infectious disease & Microbiology