Hi-plex deep amplicon sequencing for identification, high-resolution genotyping and multidrug resistance prediction of Mycobacterium leprae directly from patient biopsies by using Deeplex Myc-Lep.


Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Jul 2023
Historique:
received: 08 02 2023
revised: 25 05 2023
accepted: 29 05 2023
medline: 17 7 2023
pubmed: 17 6 2023
entrez: 16 6 2023
Statut: ppublish

Résumé

Expansion of antimicrobial resistance monitoring and epidemiological surveillance are key components of the WHO strategy towards zero leprosy. The inability to grow Mycobacterium leprae in vitro precludes routine phenotypic drug susceptibility testing, and only limited molecular tests are available. We evaluated a culture-free targeted deep sequencing assay, for mycobacterial identification, genotyping based on 18 canonical SNPs and 11 core variable-number tandem-repeat (VNTR) markers, and detection of rifampicin, dapsone and fluoroquinolone resistance-associated mutations in rpoB/ctpC/ctpI, folP1, gyrA/gyrB, respectively, and hypermutation-associated mutations in nth. The limit of detection (LOD) was determined using DNA of M. leprae reference strains and from 246 skin biopsies and 74 slit skin smears of leprosy patients, with genome copies quantified by RLEP qPCR. Sequencing results were evaluated versus whole genome sequencing (WGS) data of 14 strains, and versus VNTR-fragment length analysis (FLA) results of 89 clinical specimens. The LOD for sequencing success ranged between 80 and 3000 genome copies, depending on the sample type. The LOD for minority variants was 10%. All SNPs detected in targets by WGS were identified except in a clinical sample where WGS revealed two dapsone resistance-conferring mutations instead of one by Deeplex Myc-Lep, due to partial duplication of the sulfamide-binding domain in folP1. SNPs detected uniquely by Deeplex Myc-Lep were missed by WGS due to insufficient coverage. Concordance with VNTR-FLA results was 99.4% (926/932 alleles). Deeplex Myc-Lep may help improve the diagnosis and surveillance of leprosy. Gene domain duplication is an original putative drug resistance-related genetic adaptation in M. leprae. EDCTP2 programme supported by the European Union (grant number RIA2017NIM-1847 -PEOPLE). EDCTP, R2Stop: Effect:Hope, The Mission To End Leprosy, the Flemish Fonds Wetenschappelijk Onderzoek.

Sections du résumé

BACKGROUND BACKGROUND
Expansion of antimicrobial resistance monitoring and epidemiological surveillance are key components of the WHO strategy towards zero leprosy. The inability to grow Mycobacterium leprae in vitro precludes routine phenotypic drug susceptibility testing, and only limited molecular tests are available. We evaluated a culture-free targeted deep sequencing assay, for mycobacterial identification, genotyping based on 18 canonical SNPs and 11 core variable-number tandem-repeat (VNTR) markers, and detection of rifampicin, dapsone and fluoroquinolone resistance-associated mutations in rpoB/ctpC/ctpI, folP1, gyrA/gyrB, respectively, and hypermutation-associated mutations in nth.
METHODS METHODS
The limit of detection (LOD) was determined using DNA of M. leprae reference strains and from 246 skin biopsies and 74 slit skin smears of leprosy patients, with genome copies quantified by RLEP qPCR. Sequencing results were evaluated versus whole genome sequencing (WGS) data of 14 strains, and versus VNTR-fragment length analysis (FLA) results of 89 clinical specimens.
FINDINGS RESULTS
The LOD for sequencing success ranged between 80 and 3000 genome copies, depending on the sample type. The LOD for minority variants was 10%. All SNPs detected in targets by WGS were identified except in a clinical sample where WGS revealed two dapsone resistance-conferring mutations instead of one by Deeplex Myc-Lep, due to partial duplication of the sulfamide-binding domain in folP1. SNPs detected uniquely by Deeplex Myc-Lep were missed by WGS due to insufficient coverage. Concordance with VNTR-FLA results was 99.4% (926/932 alleles).
INTERPRETATION CONCLUSIONS
Deeplex Myc-Lep may help improve the diagnosis and surveillance of leprosy. Gene domain duplication is an original putative drug resistance-related genetic adaptation in M. leprae.
FUNDING BACKGROUND
EDCTP2 programme supported by the European Union (grant number RIA2017NIM-1847 -PEOPLE). EDCTP, R2Stop: Effect:Hope, The Mission To End Leprosy, the Flemish Fonds Wetenschappelijk Onderzoek.

Identifiants

pubmed: 37327675
pii: S2352-3964(23)00214-1
doi: 10.1016/j.ebiom.2023.104649
pmc: PMC10279541
pii:
doi:

Substances chimiques

Dapsone 8W5C518302

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104649

Informations de copyright

Copyright © 2023 The Author(s). Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests A.J., C.G., G.B., N.B., E.L., A.F., M.C. and Y.L. are employees of GenoScreen (Lille, France). P.S. is a scientific consultant for the same company. Other authors declare that they have no other competing interests.

Auteurs

Agathe Jouet (A)

GenoScreen, Lille, France.

Sofie Marijke Braet (SM)

Institute of Tropical Medicine, Antwerp, Belgium; Department of Pharmaceutical, Biomedical and Veterinary Sciences, University of Antwerp, Antwerp, Belgium; Research Foundation Flanders, Brussels, Belgium.

Cyril Gaudin (C)

GenoScreen, Lille, France.

Gaëlle Bisch (G)

GenoScreen, Lille, France.

Sidra Vasconcellos (S)

Laboratório de Biologia Molecular Aplicada a Micobactérias, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, Brazil.

Rebecca Emmanuela Epaminondas Nicacio de Oliveira do Livramento (RE)

Laboratório de Biologia Molecular Aplicada a Micobactérias, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, Brazil.

Yrneh Yadamis Prado Palacios (YY)

Laboratório de Biologia Molecular Aplicada a Micobactérias, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, Brazil.

Amanda Brum Fontes (AB)

CPqAM/Fiocruz Recife, Pernambuco, Brazil.

Norma Lucena (N)

CPqAM/Fiocruz Recife, Pernambuco, Brazil.

Patricia Rosa (P)

Instituto Lauro de Souza Lima, Bauru, São Paulo, Brazil.

Milton Moraes (M)

Laboratório de Hanseníase, IOC, Fiocruz RJ, Brazil.

Kevin La (K)

APHP-GHU Paris Nord Hôpital Bichat, Service de mycobactériologie spécialisée et de référence, Centre National de Référence des Mycobactéries et de la Résistance des Mycobactéries aux Antituberculeux - Laboratoire Associé, Paris, France; Université Paris Cité, INSERM, IAME UMR1137, Paris, France.

Nelly Badalato (N)

GenoScreen, Lille, France.

Esteban Lenoir (E)

GenoScreen, Lille, France.

Alice Ferré (A)

GenoScreen, Lille, France.

Marie Clément (M)

GenoScreen, Lille, France.

Epco Hasker (E)

Institute of Tropical Medicine, Antwerp, Belgium.

Silahi Halifa Grillone (SH)

Damien Foundation, Comoros.

Wirdane Abdou (W)

Damien Foundation, Comoros.

Aouladi Said (A)

Damien Foundation, Comoros.

Younoussa Assoumani (Y)

Damien Foundation, Comoros; National Tuberculosis and Leprosy Control Program, Moroni, Comoros.

Nissad Attoumani (N)

Damien Foundation, Comoros.

Yannick Laurent (Y)

GenoScreen, Lille, France.

Emmanuelle Cambau (E)

APHP-GHU Paris Nord Hôpital Bichat, Service de mycobactériologie spécialisée et de référence, Centre National de Référence des Mycobactéries et de la Résistance des Mycobactéries aux Antituberculeux - Laboratoire Associé, Paris, France; Université Paris Cité, INSERM, IAME UMR1137, Paris, France.

Bouke Catherine de Jong (BC)

Institute of Tropical Medicine, Antwerp, Belgium.

Philip Noël Suffys (PN)

Laboratório de Biologia Molecular Aplicada a Micobactérias, Instituto Oswaldo Cruz, Fiocruz, Rio de Janeiro, Brazil.

Philip Supply (P)

Univ. Lille, CNRS, INSERM, CHU Lille, Institut Pasteur de Lille, U1019 - UMR 8204 - CIIL - Center for Infection and Immunity of Lille, F-59000 Lille, France. Electronic address: philip.supply@ibl.cnrs.fr.

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