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Published in: BMC Infectious Diseases 1/2017

Open Access 01-12-2017 | Research article

Genetic diversity of Mycobacterium tuberculosis isolates from Tochigi prefecture, a local region of Japan

Authors: Fuminori Mizukoshi, Tohru Miyoshi-Akiyama, Hiroki Iwai, Takako Suzuki, Reiko Kiritani, Teruo Kirikae, Keiji Funatogawa

Published in: BMC Infectious Diseases | Issue 1/2017

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Abstract

Background

Foreign-born patients with tuberculosis (TB) may introduce globally disseminated isolates of Mycobacterium tuberculosis into large cities in Japan. The risk of dissemination of these isolates into local regions, however, has not been determined. This study analyzed the molecular epidemiology of M. tuberculosis isolates obtained from TB patients living in a local region of Japan.

Methods

Whole genome sequences of 169 M. tuberculosis isolates, obtained from 148 Japanese-born and 21 foreign-born patients living in Tochigi, Japan, were analyzed using the Comprehensive analysis server for the Mycobacterium t u b erculosis complex (CASTB).

Results

The 169 isolates were clustered into four clades; Lineage 2 (111 isolates 65.7%), Lineage 4 (43 isolates, 25.4%), Lineage 1 (13 isolates, 7.7%), and Lineage 3 (2 isolates, 1.2%). Of the 111 isolates belonging to Lineage 2, 79 (71.2%) were of the atypical Beijing sub-genotype. Of the 13 Lineage 1 isolates, nine (69.2%) were from foreign-born patients. The isolates belonging to Lineage 4 were further clustered into three clades, two containing isolates shared by both Japanese- and foreign-born patients. The two isolates belonging to Lineage 3 were obtained from foreign-born patients.

Conclusions

The genotypic diversity of M. tuberculosis in a local region of Japan is increased primarily by the presence of isolates obtained from foreign-born patients.
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Literature
1.
go back to reference World Health Organization. Global tuberculosis report 2015. Geneva: World Health Organization; 2015. World Health Organization. Global tuberculosis report 2015. Geneva: World Health Organization; 2015.
3.
go back to reference Kato-Miyazawa M, Miyoshi-Akiyama T, Kanno Y, Takasaki J, Kirikae T, Kobayashi N. Genetic diversity of Mycobacterium tuberculosis isolates from foreign-born and Japan-born residents in Tokyo. Clin Microbiol Infect. 2015;21(3):248.e1–8.CrossRef Kato-Miyazawa M, Miyoshi-Akiyama T, Kanno Y, Takasaki J, Kirikae T, Kobayashi N. Genetic diversity of Mycobacterium tuberculosis isolates from foreign-born and Japan-born residents in Tokyo. Clin Microbiol Infect. 2015;21(3):248.e1–8.CrossRef
4.
go back to reference Comas I, Coscolla M, Luo T, Borrell S, Holt KE, Kato-Maeda M, et al. Out-of-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nat Genet. 2013;45:1176–82.CrossRefPubMedPubMedCentral Comas I, Coscolla M, Luo T, Borrell S, Holt KE, Kato-Maeda M, et al. Out-of-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nat Genet. 2013;45:1176–82.CrossRefPubMedPubMedCentral
5.
go back to reference Gagneux S, Small PM. Global phylogeography of Mycobacterium tuberculosis and implications for tuberculosis product development. Lancet Infect Dis. 2007;7:328–37.CrossRefPubMed Gagneux S, Small PM. Global phylogeography of Mycobacterium tuberculosis and implications for tuberculosis product development. Lancet Infect Dis. 2007;7:328–37.CrossRefPubMed
6.
go back to reference Gagneux S, DeRiemer K, Van T, Kato-Maeda M, de Jong BC, Narayanan S, et al. Variable host-pathogen compatibility in Mycobacterium tuberculosis. Proc Natl Acad Sci U S A. 2006;103:2869–73.CrossRefPubMedPubMedCentral Gagneux S, DeRiemer K, Van T, Kato-Maeda M, de Jong BC, Narayanan S, et al. Variable host-pathogen compatibility in Mycobacterium tuberculosis. Proc Natl Acad Sci U S A. 2006;103:2869–73.CrossRefPubMedPubMedCentral
7.
8.
go back to reference Mazars E, Lesjean S, Banuls AL, Gilbert M, Vincent V, Gicquel B, et al. High-resolution minisatellite-based typing as a portable approach to global analysis of Mycobacterium tuberculosis molecular epidemiology. Proc Natl Acad Sci U S A. 2001;98:1901–6.CrossRefPubMedPubMedCentral Mazars E, Lesjean S, Banuls AL, Gilbert M, Vincent V, Gicquel B, et al. High-resolution minisatellite-based typing as a portable approach to global analysis of Mycobacterium tuberculosis molecular epidemiology. Proc Natl Acad Sci U S A. 2001;98:1901–6.CrossRefPubMedPubMedCentral
9.
go back to reference Thierry D, Brisson-Noel A, Vincent-Levy-Frebault V, Nguyen S, Guesdon JL, Gicquel B. Characterization of a Mycobacterium tuberculosis insertion sequence, IS6110, and its application in diagnosis. J Clin Microbiol. 1990;28:2668–73.PubMedPubMedCentral Thierry D, Brisson-Noel A, Vincent-Levy-Frebault V, Nguyen S, Guesdon JL, Gicquel B. Characterization of a Mycobacterium tuberculosis insertion sequence, IS6110, and its application in diagnosis. J Clin Microbiol. 1990;28:2668–73.PubMedPubMedCentral
10.
go back to reference Hirsh AE, Tsolaki AG, DeRiemer K, Feldman MW, Small PM. Stable association between strains of Mycobacterium tuberculosis and their human host populations. Proc Natl Acad Sci U S A. 2004;101:4871–6.CrossRefPubMedPubMedCentral Hirsh AE, Tsolaki AG, DeRiemer K, Feldman MW, Small PM. Stable association between strains of Mycobacterium tuberculosis and their human host populations. Proc Natl Acad Sci U S A. 2004;101:4871–6.CrossRefPubMedPubMedCentral
11.
go back to reference Okumura K, Kato M, Kirikae T, Kayano M, Miyoshi-Akiyama T. Construction of a virtual Mycobacterium tuberculosis consensus genome and its application to data from a next generation sequencer. BMC Genomics. 2015;16:218. 015-1368-9.CrossRefPubMedPubMedCentral Okumura K, Kato M, Kirikae T, Kayano M, Miyoshi-Akiyama T. Construction of a virtual Mycobacterium tuberculosis consensus genome and its application to data from a next generation sequencer. BMC Genomics. 2015;16:218. 015-1368-9.CrossRefPubMedPubMedCentral
12.
go back to reference Sekizuka T, Yamashita A, Murase Y, Iwamoto T, Mitarai S, Kato S, et al. TGS-TB: total genotyping solution for Mycobacterium tuberculosis using short-read whole-genome sequencing. PLoS One. 2015;10, e0142951.CrossRefPubMedPubMedCentral Sekizuka T, Yamashita A, Murase Y, Iwamoto T, Mitarai S, Kato S, et al. TGS-TB: total genotyping solution for Mycobacterium tuberculosis using short-read whole-genome sequencing. PLoS One. 2015;10, e0142951.CrossRefPubMedPubMedCentral
13.
go back to reference Walker TM, Kohl TA, Omar SV, Hedge J, Del Ojo EC, Bradley P, et al. Whole-genome sequencing for prediction of Mycobacterium tuberculosis drug susceptibility and resistance: a retrospective cohort study. Lancet Infect Dis. 2015;15:1193–202.CrossRefPubMedPubMedCentral Walker TM, Kohl TA, Omar SV, Hedge J, Del Ojo EC, Bradley P, et al. Whole-genome sequencing for prediction of Mycobacterium tuberculosis drug susceptibility and resistance: a retrospective cohort study. Lancet Infect Dis. 2015;15:1193–202.CrossRefPubMedPubMedCentral
14.
go back to reference Sekiguchi J, Nakamura T, Miyoshi-Akiyama T, Kirikae F, Kobayashi I, Augustynowicz-Kopec E, et al. Development and evaluation of a line probe assay for rapid identification of pncA mutations in pyrazinamide-resistant Mycobacterium tuberculosis strains. J Clin Microbiol. 2007;45:2802–7.CrossRefPubMedPubMedCentral Sekiguchi J, Nakamura T, Miyoshi-Akiyama T, Kirikae F, Kobayashi I, Augustynowicz-Kopec E, et al. Development and evaluation of a line probe assay for rapid identification of pncA mutations in pyrazinamide-resistant Mycobacterium tuberculosis strains. J Clin Microbiol. 2007;45:2802–7.CrossRefPubMedPubMedCentral
15.
go back to reference Iwai H, Kato-Miyazawa M, Kirikae T, Miyoshi-Akiyama T. CASTB (the comprehensive analysis server for the Mycobacterium tuberculosis complex): A publicly accessible web server for epidemiological analyses, drug-resistance prediction and phylogenetic comparison of clinical isolates. Tuberculosis (Edinb). 2015;95:843–4.CrossRef Iwai H, Kato-Miyazawa M, Kirikae T, Miyoshi-Akiyama T. CASTB (the comprehensive analysis server for the Mycobacterium tuberculosis complex): A publicly accessible web server for epidemiological analyses, drug-resistance prediction and phylogenetic comparison of clinical isolates. Tuberculosis (Edinb). 2015;95:843–4.CrossRef
17.
go back to reference Miyoshi-Akiyama T, Takeshita N, Ohmagari N, Kirikae T. Complete genome sequence of Helicobacter cinaedi type strain ATCC BAA-847. J Bacteriol. 2012;194:5692.CrossRefPubMedPubMedCentral Miyoshi-Akiyama T, Takeshita N, Ohmagari N, Kirikae T. Complete genome sequence of Helicobacter cinaedi type strain ATCC BAA-847. J Bacteriol. 2012;194:5692.CrossRefPubMedPubMedCentral
18.
go back to reference Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30:3059–66.CrossRefPubMedPubMedCentral Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30:3059–66.CrossRefPubMedPubMedCentral
19.
go back to reference Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–21.CrossRefPubMed Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–21.CrossRefPubMed
20.
go back to reference Inigo J, Garcia de Viedma D, Arce A, Palenque E, Alonso Rodriguez N, Rodriguez E, et al. Analysis of changes in recent tuberculosis transmission patterns after a sharp increase in immigration. J Clin Microbiol. 2007;45:63–9.CrossRefPubMed Inigo J, Garcia de Viedma D, Arce A, Palenque E, Alonso Rodriguez N, Rodriguez E, et al. Analysis of changes in recent tuberculosis transmission patterns after a sharp increase in immigration. J Clin Microbiol. 2007;45:63–9.CrossRefPubMed
21.
go back to reference Kunimoto D, Sutherland K, Wooldrage K, Fanning A, Chui L, Manfreda J, et al. Transmission characteristics of tuberculosis in the foreign-born and the Canadian-born populations of Alberta, Canada. Int J Tuberc Lung Dis. 2004;8:1213–20.PubMed Kunimoto D, Sutherland K, Wooldrage K, Fanning A, Chui L, Manfreda J, et al. Transmission characteristics of tuberculosis in the foreign-born and the Canadian-born populations of Alberta, Canada. Int J Tuberc Lung Dis. 2004;8:1213–20.PubMed
22.
go back to reference Fenner L, Gagneux S, Helbling P, Battegay M, Rieder HL, Pfyffer GE, et al. Mycobacterium tuberculosis transmission in a country with low tuberculosis incidence: role of immigration and HIV infection. J Clin Microbiol. 2012;50:388–95.CrossRefPubMedPubMedCentral Fenner L, Gagneux S, Helbling P, Battegay M, Rieder HL, Pfyffer GE, et al. Mycobacterium tuberculosis transmission in a country with low tuberculosis incidence: role of immigration and HIV infection. J Clin Microbiol. 2012;50:388–95.CrossRefPubMedPubMedCentral
23.
go back to reference Barniol J, Niemann S, Louis VR, Brodhun B, Dreweck C, Richter E, et al. Transmission dynamics of pulmonary tuberculosis between autochthonous and immigrant sub-populations. BMC Infect Dis. 2009;9:197. 2334-9-197.CrossRefPubMedPubMedCentral Barniol J, Niemann S, Louis VR, Brodhun B, Dreweck C, Richter E, et al. Transmission dynamics of pulmonary tuberculosis between autochthonous and immigrant sub-populations. BMC Infect Dis. 2009;9:197. 2334-9-197.CrossRefPubMedPubMedCentral
24.
go back to reference Reed MB, Pichler VK, McIntosh F, Mattia A, Fallow A, Masala S, et al. Major Mycobacterium tuberculosis lineages associate with patient country of origin. J Clin Microbiol. 2009;47:1119–28.CrossRefPubMedPubMedCentral Reed MB, Pichler VK, McIntosh F, Mattia A, Fallow A, Masala S, et al. Major Mycobacterium tuberculosis lineages associate with patient country of origin. J Clin Microbiol. 2009;47:1119–28.CrossRefPubMedPubMedCentral
Metadata
Title
Genetic diversity of Mycobacterium tuberculosis isolates from Tochigi prefecture, a local region of Japan
Authors
Fuminori Mizukoshi
Tohru Miyoshi-Akiyama
Hiroki Iwai
Takako Suzuki
Reiko Kiritani
Teruo Kirikae
Keiji Funatogawa
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2017
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-017-2457-y

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