Whole genome sequencing, analyses of drug resistance-conferring mutations, and correlation with transmission of Mycobacterium tuberculosis carrying katG-S315T in Hanoi, Vietnam
Identifieur interne : 000137 ( Pmc/Checkpoint ); précédent : 000136; suivant : 000138Whole genome sequencing, analyses of drug resistance-conferring mutations, and correlation with transmission of Mycobacterium tuberculosis carrying katG-S315T in Hanoi, Vietnam
Auteurs : Nguyen Thi Le Hang [Viêt Nam] ; Minako Hijikata [Japon] ; Shinji Maeda [Japon] ; Pham Huu Thuong [Viêt Nam] ; Jun Ohashi [Japon] ; Hoang Van Huan [Viêt Nam] ; Nguyen Phuong Hoang [Viêt Nam] ; Akiko Miyabayashi [Japon] ; Vu Cao Cuong [Viêt Nam] ; Shintaro Seto [Japon] ; Nguyen Van Hung [Viêt Nam] ; Naoto Keicho [Japon]Source :
- Scientific Reports [ 2045-2322 ] ; 2019.
Abstract
Drug-resistant tuberculosis (TB) is a serious global problem, and pathogen factors involved in the transmission of isoniazid (INH)-resistant TB have not been fully investigated. We performed whole genome sequencing of 332 clinical
Url:
DOI: 10.1038/s41598-019-51812-7
PubMed: 31653940
PubMed Central: 6814805
Affiliations:
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wicri:step="Curation">000462</idno><idno type="wicri:Area/Pmc/Checkpoint">000137</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000137</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Whole genome sequencing, analyses of drug resistance-conferring mutations, and correlation with transmission of <italic>Mycobacterium tuberculosis</italic> carrying <italic>katG</italic>-S315T in Hanoi, Vietnam</title><author><name sortKey="Hang, Nguyen Thi Le" sort="Hang, Nguyen Thi Le" uniqKey="Hang N" first="Nguyen Thi Le" last="Hang">Nguyen Thi Le Hang</name><affiliation wicri:level="1"><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 4691 4377</institution-id><institution-id institution-id-type="GRID">grid.414163.5</institution-id><institution>NCGM-BMH Medical Collaboration Center,</institution></institution-wrap>Hanoi, Vietnam</nlm:aff><country xml:lang="fr">Viêt Nam</country><wicri:regionArea>Hanoi</wicri:regionArea></affiliation></author><author><name sortKey="Hijikata, Minako" sort="Hijikata, Minako" uniqKey="Hijikata M" first="Minako" last="Hijikata">Minako Hijikata</name><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 1545 6914</institution-id><institution-id institution-id-type="GRID">grid.419151.9</institution-id><institution>Department of Pathophysiology and Host Defense,</institution><institution>The Research Institute of Tuberculosis, JATA,</institution></institution-wrap>Tokyo, Japan</nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Tokyo</wicri:regionArea></affiliation></author><author><name sortKey="Maeda, Shinji" sort="Maeda, Shinji" uniqKey="Maeda S" first="Shinji" last="Maeda">Shinji Maeda</name><affiliation wicri:level="1"><nlm:aff id="Aff3"><institution-wrap><institution-id institution-id-type="GRID">grid.444700.3</institution-id><institution>Faculty of Pharmaceutical Sciences,</institution><institution>Hokkaido University of Science,</institution></institution-wrap>Hokkaido, Japan</nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Hokkaido</wicri:regionArea></affiliation></author><author><name sortKey="Thuong, Pham Huu" sort="Thuong, Pham Huu" uniqKey="Thuong P" first="Pham Huu" last="Thuong">Pham Huu Thuong</name><affiliation wicri:level="1"><nlm:aff id="Aff4"><institution-wrap><institution-id institution-id-type="GRID">grid.470059.f</institution-id><institution>Hanoi Lung Hospital,</institution></institution-wrap>Hanoi, Vietnam</nlm:aff><country xml:lang="fr">Viêt Nam</country><wicri:regionArea>Hanoi</wicri:regionArea></affiliation></author><author><name sortKey="Ohashi, Jun" sort="Ohashi, Jun" uniqKey="Ohashi J" first="Jun" last="Ohashi">Jun Ohashi</name><affiliation wicri:level="1"><nlm:aff id="Aff5"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2151 536X</institution-id><institution-id institution-id-type="GRID">grid.26999.3d</institution-id><institution>Department of Biological Sciences,</institution><institution>Graduate School of Science, The University of Tokyo,</institution></institution-wrap>Tokyo, Japan</nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Tokyo</wicri:regionArea></affiliation></author><author><name sortKey="Van Huan, Hoang" sort="Van Huan, Hoang" uniqKey="Van Huan H" first="Hoang" last="Van Huan">Hoang Van Huan</name><affiliation wicri:level="1"><nlm:aff id="Aff4"><institution-wrap><institution-id institution-id-type="GRID">grid.470059.f</institution-id><institution>Hanoi Lung Hospital,</institution></institution-wrap>Hanoi, Vietnam</nlm:aff><country xml:lang="fr">Viêt Nam</country><wicri:regionArea>Hanoi</wicri:regionArea></affiliation></author><author><name sortKey="Hoang, Nguyen Phuong" sort="Hoang, Nguyen Phuong" uniqKey="Hoang N" first="Nguyen Phuong" last="Hoang">Nguyen Phuong Hoang</name><affiliation wicri:level="1"><nlm:aff id="Aff6"><institution-wrap><institution-id institution-id-type="GRID">grid.470059.f</institution-id><institution>Department of Microbiology,</institution><institution>Hanoi Lung Hospital,</institution></institution-wrap>Hanoi, Vietnam</nlm:aff><country xml:lang="fr">Viêt Nam</country><wicri:regionArea>Hanoi</wicri:regionArea></affiliation></author><author><name sortKey="Miyabayashi, Akiko" sort="Miyabayashi, Akiko" uniqKey="Miyabayashi A" first="Akiko" last="Miyabayashi">Akiko Miyabayashi</name><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 1545 6914</institution-id><institution-id institution-id-type="GRID">grid.419151.9</institution-id><institution>Department of Pathophysiology and Host Defense,</institution><institution>The Research Institute of Tuberculosis, JATA,</institution></institution-wrap>Tokyo, Japan</nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Tokyo</wicri:regionArea></affiliation></author><author><name sortKey="Cuong, Vu Cao" sort="Cuong, Vu Cao" uniqKey="Cuong V" first="Vu Cao" last="Cuong">Vu Cao Cuong</name><affiliation wicri:level="1"><nlm:aff id="Aff7">Hanoi Department of Health, Hanoi, Vietnam</nlm:aff><country xml:lang="fr">Viêt Nam</country><wicri:regionArea>Hanoi Department of Health, Hanoi</wicri:regionArea><wicri:noRegion>Hanoi</wicri:noRegion></affiliation></author><author><name sortKey="Seto, Shintaro" sort="Seto, Shintaro" uniqKey="Seto S" first="Shintaro" last="Seto">Shintaro Seto</name><affiliation wicri:level="1"><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 1545 6914</institution-id><institution-id institution-id-type="GRID">grid.419151.9</institution-id><institution>Department of Pathophysiology and Host Defense,</institution><institution>The Research Institute of Tuberculosis, JATA,</institution></institution-wrap>Tokyo, Japan</nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Tokyo</wicri:regionArea></affiliation></author><author><name sortKey="Van Hung, Nguyen" sort="Van Hung, Nguyen" uniqKey="Van Hung N" first="Nguyen" last="Van Hung">Nguyen Van Hung</name><affiliation wicri:level="1"><nlm:aff id="Aff8">Department of Microbiology, National Lung Hospital, Hanoi, Vietnam</nlm:aff><country xml:lang="fr">Viêt Nam</country><wicri:regionArea>Department of Microbiology, National Lung Hospital, Hanoi</wicri:regionArea><wicri:noRegion>Hanoi</wicri:noRegion></affiliation></author><author><name sortKey="Keicho, Naoto" sort="Keicho, Naoto" uniqKey="Keicho N" first="Naoto" last="Keicho">Naoto Keicho</name><affiliation wicri:level="1"><nlm:aff id="Aff9"><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 1545 6914</institution-id><institution-id institution-id-type="GRID">grid.419151.9</institution-id><institution>The Research Institute of Tuberculosis JATA,</institution></institution-wrap>Tokyo, Japan</nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Tokyo</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="Aff10"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0489 0290</institution-id><institution-id institution-id-type="GRID">grid.45203.30</institution-id><institution>National Center for Global Health and Medicine,</institution></institution-wrap>Tokyo, Japan</nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea>Tokyo</wicri:regionArea></affiliation></author></analytic><series><title level="j">Scientific Reports</title><idno type="eISSN">2045-2322</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p id="Par1">Drug-resistant tuberculosis (TB) is a serious global problem, and pathogen factors involved in the transmission of isoniazid (INH)-resistant TB have not been fully investigated. We performed whole genome sequencing of 332 clinical <italic>Mycobacterium tuberculosis</italic> (Mtb) isolates collected from patients newly diagnosed with smear-positive pulmonary TB in Hanoi, Vietnam. Using a bacterial genome-wide approach based on linear mixed models, we investigated the associations between 31-bp k-mers and clustered strains harboring <italic>katG</italic>-S315T, a major INH-resistance mutation in the present cohort and in the second panel previously published in South Africa. Five statistically significant genes, namely, <italic>PPE18/19</italic>, <italic>gid</italic>, <italic>emrB</italic>, <italic>Rv1588c</italic>, and <italic>pncA</italic>, were shared by the two panels. We further identified variants of the genes responsible for these k-mers, which are relevant to the spread of INH-resistant strains. Phylogenetic convergence test showed that variants relevant to <italic>PPE46/47</italic>-like chimeric genes were significantly associated with the same phenotype in Hanoi. The associations were further confirmed after adjustment for the confounders. These findings suggest that genomic variations of the pathogen facilitate the expansion of INH-resistance TB, at least in part, and our study provides a new insight into the mechanisms by which drug-resistant Mtb maintains fitness and spreads in Asia and Africa.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Bastos, Ml" uniqKey="Bastos M">ML Bastos</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Pooran, A" uniqKey="Pooran A">A Pooran</name></author><author><name sortKey="Pieterson, E" uniqKey="Pieterson E">E Pieterson</name></author><author><name sortKey="Davids, M" uniqKey="Davids M">M Davids</name></author><author><name sortKey="Theron, G" uniqKey="Theron G">G Theron</name></author><author><name sortKey="Dheda, K" uniqKey="Dheda K">K Dheda</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Muller, B" uniqKey="Muller B">B 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Sci Rep</journal-id><journal-id journal-id-type="iso-abbrev">Sci Rep</journal-id><journal-title-group><journal-title>Scientific Reports</journal-title></journal-title-group><issn pub-type="epub">2045-2322</issn><publisher><publisher-name>Nature Publishing Group UK</publisher-name><publisher-loc>London</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31653940</article-id><article-id pub-id-type="pmc">6814805</article-id><article-id pub-id-type="publisher-id">51812</article-id><article-id pub-id-type="doi">10.1038/s41598-019-51812-7</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Whole genome sequencing, analyses of drug resistance-conferring mutations, and correlation with transmission of <italic>Mycobacterium tuberculosis</italic> carrying <italic>katG</italic>-S315T in Hanoi, Vietnam</article-title></title-group><contrib-group><contrib contrib-type="author" equal-contrib="yes"><name><surname>Hang</surname><given-names>Nguyen Thi Le</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author" equal-contrib="yes"><name><surname>Hijikata</surname><given-names>Minako</given-names></name><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Maeda</surname><given-names>Shinji</given-names></name><xref ref-type="aff" rid="Aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Thuong</surname><given-names>Pham Huu</given-names></name><xref ref-type="aff" rid="Aff4">4</xref></contrib><contrib contrib-type="author"><name><surname>Ohashi</surname><given-names>Jun</given-names></name><xref ref-type="aff" rid="Aff5">5</xref></contrib><contrib contrib-type="author"><name><surname>Van Huan</surname><given-names>Hoang</given-names></name><xref ref-type="aff" rid="Aff4">4</xref></contrib><contrib contrib-type="author"><name><surname>Hoang</surname><given-names>Nguyen Phuong</given-names></name><xref ref-type="aff" rid="Aff6">6</xref></contrib><contrib contrib-type="author"><name><surname>Miyabayashi</surname><given-names>Akiko</given-names></name><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Cuong</surname><given-names>Vu Cao</given-names></name><xref ref-type="aff" rid="Aff7">7</xref></contrib><contrib contrib-type="author"><name><surname>Seto</surname><given-names>Shintaro</given-names></name><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Van Hung</surname><given-names>Nguyen</given-names></name><xref ref-type="aff" rid="Aff8">8</xref></contrib><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid">http://orcid.org/0000-0001-8232-9448</contrib-id><name><surname>Keicho</surname><given-names>Naoto</given-names></name><address><email>nkeicho-tky@umin.ac.jp</email></address><xref ref-type="aff" rid="Aff9">9</xref><xref ref-type="aff" rid="Aff10">10</xref></contrib><aff id="Aff1"><label>1</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 4691 4377</institution-id><institution-id institution-id-type="GRID">grid.414163.5</institution-id><institution>NCGM-BMH Medical Collaboration Center,</institution></institution-wrap>Hanoi, Vietnam</aff><aff id="Aff2"><label>2</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 1545 6914</institution-id><institution-id institution-id-type="GRID">grid.419151.9</institution-id><institution>Department of Pathophysiology and Host Defense,</institution><institution>The Research Institute of Tuberculosis, JATA,</institution></institution-wrap>Tokyo, Japan</aff><aff id="Aff3"><label>3</label><institution-wrap><institution-id institution-id-type="GRID">grid.444700.3</institution-id><institution>Faculty of Pharmaceutical Sciences,</institution><institution>Hokkaido University of Science,</institution></institution-wrap>Hokkaido, Japan</aff><aff id="Aff4"><label>4</label><institution-wrap><institution-id institution-id-type="GRID">grid.470059.f</institution-id><institution>Hanoi Lung Hospital,</institution></institution-wrap>Hanoi, Vietnam</aff><aff id="Aff5"><label>5</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 2151 536X</institution-id><institution-id institution-id-type="GRID">grid.26999.3d</institution-id><institution>Department of Biological Sciences,</institution><institution>Graduate School of Science, The University of Tokyo,</institution></institution-wrap>Tokyo, Japan</aff><aff id="Aff6"><label>6</label><institution-wrap><institution-id institution-id-type="GRID">grid.470059.f</institution-id><institution>Department of Microbiology,</institution><institution>Hanoi Lung Hospital,</institution></institution-wrap>Hanoi, Vietnam</aff><aff id="Aff7"><label>7</label>Hanoi Department of Health, Hanoi, Vietnam</aff><aff id="Aff8"><label>8</label>Department of Microbiology, National Lung Hospital, Hanoi, Vietnam</aff><aff id="Aff9"><label>9</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0001 1545 6914</institution-id><institution-id institution-id-type="GRID">grid.419151.9</institution-id><institution>The Research Institute of Tuberculosis JATA,</institution></institution-wrap>Tokyo, Japan</aff><aff id="Aff10"><label>10</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0489 0290</institution-id><institution-id institution-id-type="GRID">grid.45203.30</institution-id><institution>National Center for Global Health and Medicine,</institution></institution-wrap>Tokyo, Japan</aff></contrib-group><pub-date pub-type="epub"><day>25</day><month>10</month><year>2019</year></pub-date><pub-date pub-type="pmc-release"><day>25</day><month>10</month><year>2019</year></pub-date><pub-date pub-type="collection"><year>2019</year></pub-date><volume>9</volume><elocation-id>15354</elocation-id><history><date date-type="received"><day>26</day><month>7</month><year>2019</year></date><date date-type="accepted"><day>8</day><month>10</month><year>2019</year></date></history><permissions><copyright-statement>© The Author(s) 2019</copyright-statement><license license-type="OpenAccess"><license-p><bold>Open Access</bold> This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>.</license-p></license></permissions><abstract id="Abs1"><p id="Par1">Drug-resistant tuberculosis (TB) is a serious global problem, and pathogen factors involved in the transmission of isoniazid (INH)-resistant TB have not been fully investigated. We performed whole genome sequencing of 332 clinical <italic>Mycobacterium tuberculosis</italic> (Mtb) isolates collected from patients newly diagnosed with smear-positive pulmonary TB in Hanoi, Vietnam. Using a bacterial genome-wide approach based on linear mixed models, we investigated the associations between 31-bp k-mers and clustered strains harboring <italic>katG</italic>-S315T, a major INH-resistance mutation in the present cohort and in the second panel previously published in South Africa. Five statistically significant genes, namely, <italic>PPE18/19</italic>, <italic>gid</italic>, <italic>emrB</italic>, <italic>Rv1588c</italic>, and <italic>pncA</italic>, were shared by the two panels. We further identified variants of the genes responsible for these k-mers, which are relevant to the spread of INH-resistant strains. Phylogenetic convergence test showed that variants relevant to <italic>PPE46/47</italic>-like chimeric genes were significantly associated with the same phenotype in Hanoi. The associations were further confirmed after adjustment for the confounders. These findings suggest that genomic variations of the pathogen facilitate the expansion of INH-resistance TB, at least in part, and our study provides a new insight into the mechanisms by which drug-resistant Mtb maintains fitness and spreads in Asia and Africa.</p></abstract><kwd-group kwd-group-type="npg-subject"><title>Subject terms</title><kwd>Bacterial genes</kwd><kwd>Tuberculosis</kwd></kwd-group><funding-group><award-group><funding-source><institution>This research was supported by AMED under Grant Number JP19fm0108001 (Japan Initiative for Global Research Network on Infectious Diseases; J-GRID).</institution></funding-source></award-group></funding-group><custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name><meta-value>© The Author(s) 2019</meta-value></custom-meta></custom-meta-group></article-meta></front></pmc><affiliations><list><country><li>Japon</li><li>Viêt Nam</li></country></list><tree><country name="Viêt Nam"><noRegion><name sortKey="Hang, Nguyen Thi Le" sort="Hang, Nguyen Thi Le" uniqKey="Hang N" first="Nguyen Thi Le" last="Hang">Nguyen Thi Le Hang</name></noRegion><name sortKey="Cuong, Vu Cao" sort="Cuong, Vu Cao" uniqKey="Cuong V" first="Vu Cao" last="Cuong">Vu Cao Cuong</name><name sortKey="Hoang, Nguyen Phuong" sort="Hoang, Nguyen Phuong" uniqKey="Hoang N" first="Nguyen Phuong" last="Hoang">Nguyen Phuong Hoang</name><name sortKey="Thuong, Pham Huu" sort="Thuong, Pham Huu" uniqKey="Thuong P" first="Pham Huu" last="Thuong">Pham Huu Thuong</name><name sortKey="Van Huan, Hoang" sort="Van Huan, Hoang" uniqKey="Van Huan H" first="Hoang" last="Van Huan">Hoang Van Huan</name><name sortKey="Van Hung, Nguyen" sort="Van Hung, Nguyen" uniqKey="Van Hung N" first="Nguyen" last="Van Hung">Nguyen Van Hung</name></country><country name="Japon"><noRegion><name sortKey="Hijikata, Minako" sort="Hijikata, Minako" uniqKey="Hijikata M" first="Minako" last="Hijikata">Minako Hijikata</name></noRegion><name sortKey="Keicho, Naoto" sort="Keicho, Naoto" uniqKey="Keicho N" first="Naoto" last="Keicho">Naoto Keicho</name><name sortKey="Keicho, Naoto" sort="Keicho, Naoto" uniqKey="Keicho N" first="Naoto" last="Keicho">Naoto Keicho</name><name sortKey="Maeda, Shinji" sort="Maeda, Shinji" uniqKey="Maeda S" first="Shinji" last="Maeda">Shinji Maeda</name><name sortKey="Miyabayashi, Akiko" sort="Miyabayashi, Akiko" uniqKey="Miyabayashi A" first="Akiko" last="Miyabayashi">Akiko Miyabayashi</name><name sortKey="Ohashi, Jun" sort="Ohashi, Jun" uniqKey="Ohashi J" first="Jun" last="Ohashi">Jun Ohashi</name><name sortKey="Seto, Shintaro" sort="Seto, Shintaro" uniqKey="Seto S" first="Shintaro" last="Seto">Shintaro Seto</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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