MDR M. tuberculosis outbreak clone in Eswatini missed by Xpert has elevated bedaquiline resistance dated to the pre-treatment era.


Journal

Genome medicine
ISSN: 1756-994X
Titre abrégé: Genome Med
Pays: England
ID NLM: 101475844

Informations de publication

Date de publication:
25 11 2020
Historique:
received: 18 05 2020
accepted: 27 10 2020
entrez: 26 11 2020
pubmed: 27 11 2020
medline: 6 11 2021
Statut: epublish

Résumé

Multidrug-resistant (MDR) Mycobacterium tuberculosis complex strains not detected by commercial molecular drug susceptibility testing (mDST) assays due to the RpoB I491F resistance mutation are threatening the control of MDR tuberculosis (MDR-TB) in Eswatini. We investigate the evolution and spread of MDR strains in Eswatini with a focus on bedaquiline (BDQ) and clofazimine (CFZ) resistance using whole-genome sequencing in two collections ((1) national drug resistance survey, 2009-2010; (2) MDR strains from the Nhlangano region, 2014-2017). MDR strains in collection 1 had a high cluster rate (95%, 117/123 MDR strains) with 55% grouped into the two largest clusters (gCL3, n = 28; gCL10, n = 40). All gCL10 isolates, which likely emerged around 1993 (95% highest posterior density 1987-1998), carried the mutation RpoB I491F that is missed by commercial mDST assays. In addition, 21 (53%) gCL10 isolates shared a Rv0678 M146T mutation that correlated with elevated minimum inhibitory concentrations (MICs) to BDQ and CFZ compared to wild type isolates. gCL10 isolates with the Rv0678 M146T mutation were also detected in collection 2. The high clustering rate suggests that transmission has been driving the MDR-TB epidemic in Eswatini for three decades. The presence of MDR strains in Eswatini that are not detected by commercial mDST assays and have elevated MICs to BDQ and CFZ potentially jeopardizes the successful implementation of new MDR-TB treatment guidelines. Measures to limit the spread of these outbreak isolates need to be implemented urgently.

Sections du résumé

BACKGROUND
Multidrug-resistant (MDR) Mycobacterium tuberculosis complex strains not detected by commercial molecular drug susceptibility testing (mDST) assays due to the RpoB I491F resistance mutation are threatening the control of MDR tuberculosis (MDR-TB) in Eswatini.
METHODS
We investigate the evolution and spread of MDR strains in Eswatini with a focus on bedaquiline (BDQ) and clofazimine (CFZ) resistance using whole-genome sequencing in two collections ((1) national drug resistance survey, 2009-2010; (2) MDR strains from the Nhlangano region, 2014-2017).
RESULTS
MDR strains in collection 1 had a high cluster rate (95%, 117/123 MDR strains) with 55% grouped into the two largest clusters (gCL3, n = 28; gCL10, n = 40). All gCL10 isolates, which likely emerged around 1993 (95% highest posterior density 1987-1998), carried the mutation RpoB I491F that is missed by commercial mDST assays. In addition, 21 (53%) gCL10 isolates shared a Rv0678 M146T mutation that correlated with elevated minimum inhibitory concentrations (MICs) to BDQ and CFZ compared to wild type isolates. gCL10 isolates with the Rv0678 M146T mutation were also detected in collection 2.
CONCLUSION
The high clustering rate suggests that transmission has been driving the MDR-TB epidemic in Eswatini for three decades. The presence of MDR strains in Eswatini that are not detected by commercial mDST assays and have elevated MICs to BDQ and CFZ potentially jeopardizes the successful implementation of new MDR-TB treatment guidelines. Measures to limit the spread of these outbreak isolates need to be implemented urgently.

Identifiants

pubmed: 33239092
doi: 10.1186/s13073-020-00793-8
pii: 10.1186/s13073-020-00793-8
pmc: PMC7687760
doi:

Substances chimiques

Antitubercular Agents 0
Bacterial Proteins 0
Diarylquinolines 0
bedaquiline 78846I289Y

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

104

Références

EBioMedicine. 2018 Feb;28:136-142
pubmed: 29337135
Public Health Action. 2015 Jun 21;5(2):140-6
pubmed: 26400386
Antimicrob Agents Chemother. 2017 May 24;61(6):
pubmed: 28320727
Am J Respir Crit Care Med. 2020 Jun 15;201(12):1564-1568
pubmed: 32053752
Eur Respir J. 2020 Sep 17;:
pubmed: 32943401
J Clin Microbiol. 2015 Jun;53(6):1806-11
pubmed: 25762769
Lancet. 2014 Apr 5;383(9924):1193-4
pubmed: 24439236
PLoS Med. 2013;10(2):e1001387
pubmed: 23424287
PLoS Pathog. 2018 Oct 18;14(10):e1007297
pubmed: 30335850
N Engl J Med. 2015 Mar 19;372(12):1181-2
pubmed: 25785984
Eur Respir J. 2020 Jun 4;55(6):
pubmed: 32060065
Am J Respir Crit Care Med. 2019 Aug 15;200(4):514-515
pubmed: 31026398
Genome Med. 2020 Mar 6;12(1):27
pubmed: 32143680
Lancet Infect Dis. 2018 Jun;18(6):675-683
pubmed: 29574065
PLoS One. 2017 Dec 27;12(12):e0189838
pubmed: 29281674
Eur Respir J. 2020 Aug 6;:
pubmed: 32764113
Antimicrob Agents Chemother. 2012 Dec;56(12):6080-7
pubmed: 23006760
J Antimicrob Chemother. 2017 Mar 1;72(3):684-690
pubmed: 28031270
Emerg Infect Dis. 2012 Jan;18(1):29-37
pubmed: 22260950
Public Health Action. 2017 Sep 21;7(3):240-242
pubmed: 29201660
N Engl J Med. 2019 May 30;380(22):2178-2180
pubmed: 31141643
Infect Genet Evol. 2012 Jun;12(4):748-54
pubmed: 22342955
Clin Infect Dis. 2019 Sep 13;69(7):1229-1231
pubmed: 30933266
Elife. 2018 Oct 30;7:
pubmed: 30373719
Clin Infect Dis. 2018 May 2;66(10):1625-1630
pubmed: 29126225
J Antimicrob Chemother. 2015 Sep;70(9):2427-39
pubmed: 26089441
J Clin Microbiol. 2019 Aug 26;57(9):
pubmed: 31315957
Antimicrob Agents Chemother. 2020 May 21;64(6):
pubmed: 32229496
Lancet Infect Dis. 2018 Dec;18(12):1350-1359
pubmed: 30342828
Emerg Infect Dis. 2019 Mar;25(3):564-568
pubmed: 30789124
J Antimicrob Chemother. 2020 Aug 1;75(8):2031-2043
pubmed: 32361756
Nucleic Acids Res. 2011 Jan;39(Database issue):D28-31
pubmed: 20972220
Lancet Microbe. 2020 Aug;1(4):e165-e174
pubmed: 32803174
Int J Infect Dis. 2019 Mar;80S:S32-S35
pubmed: 30818049
Clin Microbiol Infect. 2020 Nov;26(11):1453-1455
pubmed: 32768492

Auteurs

Patrick Beckert (P)

Molecular and Experimental Mycobacteriology, Research Center Borstel, Parkallee 1, 23845, Borstel, Germany.
German Center for Infection Research (DZIF), Partner Site Hamburg-Lübeck-Borstel-Riems, Borstel, Germany.

Elisabeth Sanchez-Padilla (E)

Epicentre, Paris, France.

Matthias Merker (M)

Molecular and Experimental Mycobacteriology, Research Center Borstel, Parkallee 1, 23845, Borstel, Germany.

Viola Dreyer (V)

Molecular and Experimental Mycobacteriology, Research Center Borstel, Parkallee 1, 23845, Borstel, Germany.

Thomas A Kohl (TA)

Molecular and Experimental Mycobacteriology, Research Center Borstel, Parkallee 1, 23845, Borstel, Germany.

Christian Utpatel (C)

Molecular and Experimental Mycobacteriology, Research Center Borstel, Parkallee 1, 23845, Borstel, Germany.

Claudio U Köser (CU)

Department of Genetics, University of Cambridge, Cambridge, UK.

Ivan Barilar (I)

Molecular and Experimental Mycobacteriology, Research Center Borstel, Parkallee 1, 23845, Borstel, Germany.

Nazir Ismail (N)

Centre for Tuberculosis, National TB Reference Laboratory, WHO TB Supranational Laboratory Network, National Institute for Communicable Diseases/National Health Laboratory Services, Johannesburg, South Africa.
Department of Medical Microbiology, University of Pretoria, Pretoria, South Africa.
Department of Internal Medicine, University of Witwatersrand, Johannesburg, South Africa.

Shaheed Vally Omar (SV)

Centre for Tuberculosis, National TB Reference Laboratory, WHO TB Supranational Laboratory Network, National Institute for Communicable Diseases/National Health Laboratory Services, Johannesburg, South Africa.

Marisa Klopper (M)

DST/NRF Centre of Excellence for Biomedical Tuberculosis Research, Faculty of Medicine and Health Sciences, Stellenbosch University, Cape Town, South Africa.
South African Medical Research Council Centre for Tuberculosis Research, Division of Molecular Biology and Human Genetics, Faculty of Medicine and Health Sciences, Stellenbosch University, Cape Town, South Africa.

Robin M Warren (RM)

DST/NRF Centre of Excellence for Biomedical Tuberculosis Research, Faculty of Medicine and Health Sciences, Stellenbosch University, Cape Town, South Africa.
South African Medical Research Council Centre for Tuberculosis Research, Division of Molecular Biology and Human Genetics, Faculty of Medicine and Health Sciences, Stellenbosch University, Cape Town, South Africa.

Harald Hoffmann (H)

SYNLAB Gauting, Gauting, Germany, IML red GmbH, Institute of Microbiology and Laboratory Medicine, WHO Supranational Reference Laboratory of TB, Gauting, Germany.

Gugu Maphalala (G)

National Tuberculosis Reference Laboratory (NTRL), Ministry of Health, Mbabane, Swaziland.

Elisa Ardizzoni (E)

Mycobacteriology Unit, Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium.

Bouke C de Jong (BC)

Mycobacteriology Unit, Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium.

Bernhard Kerschberger (B)

Médecins Sans Frontières (MSF) - Eswatini, Mbabane, Eswatini.

Birgit Schramm (B)

Epicentre, Paris, France.

Sönke Andres (S)

National and WHO Supranational Reference Center for Mycobacteria, Research Center Borstel, Borstel, Germany.

Katharina Kranzer (K)

National and WHO Supranational Reference Center for Mycobacteria, Research Center Borstel, Borstel, Germany.
London School of Hygiene and Tropical Medicine, London, United Kingdom of Great Britain and Northern Ireland, UK.

Florian P Maurer (FP)

National and WHO Supranational Reference Center for Mycobacteria, Research Center Borstel, Borstel, Germany.
Eppendorf, Institute of Medical Microbiology, Virology and Hygiene, University Medical Center Hamburg, Hamburg, Germany.

Maryline Bonnet (M)

Epicentre, Paris, France.
IRD UMI233/ INSERM U1175/Université de Montpellier, Montpellier, France.

Stefan Niemann (S)

Molecular and Experimental Mycobacteriology, Research Center Borstel, Parkallee 1, 23845, Borstel, Germany. sniemann@fz-borstel.de.
German Center for Infection Research (DZIF), Partner Site Hamburg-Lübeck-Borstel-Riems, Borstel, Germany. sniemann@fz-borstel.de.
National and WHO Supranational Reference Center for Mycobacteria, Research Center Borstel, Borstel, Germany. sniemann@fz-borstel.de.
Biochemistry & Microbiology, School of Medicine, University of Namibia, Windhoek, Namibia. sniemann@fz-borstel.de.

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