Evolution and transmission of antibiotic resistance is driven by Beijing lineage Mycobacterium tuberculosis in Vietnam

Drug-resistant tuberculosis (TB) infection is a growing and potent concern, and combating it will be necessary to achieve the WHO's goal of a 95% reduction in TB deaths by 2035. While prior studies have explored the evolution and spread of drug resistance, we still lack a clear understanding of...

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Published inMicrobiology spectrum Vol. 11; no. 6; p. e0256223
Main Authors Silcocks, Matthew, Chang, Xuling, Thuong Thuong, Nguyen Thuy, Qin, Youwen, Minh Ha, Dang Thi, Khac Thai, Phan Vuong, Vijay, Srinivasan, Anh Thu, Do Dang, Ngoc Ha, Vu Thi, Ngoc Nhung, Hoang, Huu Lan, Nguyen, Quynh Nhu, Nguyen Thi, Edwards, David, Nath, Artika, Pham, Kym, Duc Bang, Nguyen, Hong Chau, Tran Thi, Thwaites, Guy, Heemskerk, A Dorothee, Chuen Khor, Chiea, Teo, Yik Ying, Inouye, Michael, Ong, Rick Twee-Hee, Caws, Maxine, Holt, Kathryn E, Dunstan, Sarah J
Format Journal Article
LanguageEnglish
Published United States American Society for Microbiology 12.12.2023
Subjects
Antimicrobial Chemotherapy
antimicrobial resistance
Mycobacterium tuberculosis
pathogen genomics
Research Article
Mycobacterium tuberculosis
antimicrobial resistance
pathogen genomics
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Abstract Drug-resistant tuberculosis (TB) infection is a growing and potent concern, and combating it will be necessary to achieve the WHO's goal of a 95% reduction in TB deaths by 2035. While prior studies have explored the evolution and spread of drug resistance, we still lack a clear understanding of the fitness costs (if any) imposed by resistance-conferring mutations and the role that genetic lineage plays in determining the likelihood of resistance evolution. This study offers insight into these questions by assessing the dynamics of resistance evolution in a high-burden Southeast Asian setting with a diverse lineage composition. It demonstrates that there are clear lineage-specific differences in the dynamics of resistance acquisition and transmission and shows that different lineages evolve resistance via characteristic mutational pathways.
AbstractList Drug-resistant tuberculosis (TB) infection is a growing and potent concern, and combating it will be necessary to achieve the WHO's goal of a 95% reduction in TB deaths by 2035. While prior studies have explored the evolution and spread of drug resistance, we still lack a clear understanding of the fitness costs (if any) imposed by resistance-conferring mutations and the role that genetic lineage plays in determining the likelihood of resistance evolution. This study offers insight into these questions by assessing the dynamics of resistance evolution in a high-burden Southeast Asian setting with a diverse lineage composition. It demonstrates that there are clear lineage-specific differences in the dynamics of resistance acquisition and transmission and shows that different lineages evolve resistance via characteristic mutational pathways.
ABSTRACT A previous investigation has elucidated the landscape of Mtb genomic diversity and transmission dynamics in Ho Chi Minh City, Vietnam. Here, we expand the scope of this survey by adding a substantial number of additional genomes (total sample size: 2,542) and phenotypic drug susceptibility data for the majority of isolates. We aim to explore the prevalence and evolutionary dynamics of drug resistance and our ability to predict drug resistance from sequencing data. Among isolates tested phenotypically against first-line drugs, we observed high rates of streptomycin [STR, 37.7% (N = 573/1,520)] and isoniazid resistance [INH, 25.7% (N = 459/1,786)] and lower rates of resistance to rifampicin [RIF, 4.9% (N = 87/1,786)] and ethambutol [EMB, 4.2% (N = 75/1,785)]. Relative to global benchmarks, resistance to STR and INH was predicted accurately when applying the TB-Profiler algorithm to whole genome sequencing data (sensitivities of 0.81 and 0.87, respectively), while resistance to RIF and EMB was predicted relatively poorly (sensitivities of 0.70 and 0.44, respectively). Exploring the evolution of drug resistance revealed the main phylogenetic lineages to display differing dynamics and tendencies to evolve resistance via mutations in certain genes. The Beijing sublineage L2.2.1 was found to acquire de novo resistance mutations more frequently than isolates from other lineages and to suffer no apparent fitness cost acting to impede the transmission of resistance. Mutations conferring resistance to INH and STR arose earlier, on average, than those conferring resistance to RIF and are now more widespread across the phylogeny. The high prevalence of “background” INH resistance, combined with high rates of RIF mono-resistance (20.7%, N = 18/87), suggests that rapid assays for INH resistance will be valuable in this setting. These tests will allow the detection of INH mono-resistance and will allow multi-drug-resistant isolates to be distinguished from isolates with RIF mono-resistance. IMPORTANCE Drug-resistant tuberculosis (TB) infection is a growing and potent concern, and combating it will be necessary to achieve the WHO’s goal of a 95% reduction in TB deaths by 2035. While prior studies have explored the evolution and spread of drug resistance, we still lack a clear understanding of the fitness costs (if any) imposed by resistance-conferring mutations and the role that Mtb genetic lineage plays in determining the likelihood of resistance evolution. This study offers insight into these questions by assessing the dynamics of resistance evolution in a high-burden Southeast Asian setting with a diverse lineage composition. It demonstrates that there are clear lineage-specific differences in the dynamics of resistance acquisition and transmission and shows that different lineages evolve resistance via characteristic mutational pathways.
IMPORTANCEDrug-resistant tuberculosis (TB) infection is a growing and potent concern, and combating it will be necessary to achieve the WHO's goal of a 95% reduction in TB deaths by 2035. While prior studies have explored the evolution and spread of drug resistance, we still lack a clear understanding of the fitness costs (if any) imposed by resistance-conferring mutations and the role that Mtb genetic lineage plays in determining the likelihood of resistance evolution. This study offers insight into these questions by assessing the dynamics of resistance evolution in a high-burden Southeast Asian setting with a diverse lineage composition. It demonstrates that there are clear lineage-specific differences in the dynamics of resistance acquisition and transmission and shows that different lineages evolve resistance via characteristic mutational pathways.
A previous investigation has elucidated the landscape of Mtb genomic diversity and transmission dynamics in Ho Chi Minh City, Vietnam. Here, we expand the scope of this survey by adding a substantial number of additional genomes (total sample size: 2,542) and phenotypic drug susceptibility data for the majority of isolates. We aim to explore the prevalence and evolutionary dynamics of drug resistance and our ability to predict drug resistance from sequencing data. Among isolates tested phenotypically against first-line drugs, we observed high rates of streptomycin [STR, 37.7% ( N = 573/1,520)] and isoniazid resistance [INH, 25.7% ( N = 459/1,786)] and lower rates of resistance to rifampicin [RIF, 4.9% ( N = 87/1,786)] and ethambutol [EMB, 4.2% ( N = 75/1,785)]. Relative to global benchmarks, resistance to STR and INH was predicted accurately when applying the TB-Profiler algorithm to whole genome sequencing data (sensitivities of 0.81 and 0.87, respectively), while resistance to RIF and EMB was predicted relatively poorly (sensitivities of 0.70 and 0.44, respectively). Exploring the evolution of drug resistance revealed the main phylogenetic lineages to display differing dynamics and tendencies to evolve resistance via mutations in certain genes. The Beijing sublineage L2.2.1 was found to acquire de novo resistance mutations more frequently than isolates from other lineages and to suffer no apparent fitness cost acting to impede the transmission of resistance. Mutations conferring resistance to INH and STR arose earlier, on average, than those conferring resistance to RIF and are now more widespread across the phylogeny. The high prevalence of “background” INH resistance, combined with high rates of RIF mono-resistance (20.7%, N = 18/87), suggests that rapid assays for INH resistance will be valuable in this setting. These tests will allow the detection of INH mono-resistance and will allow multi-drug-resistant isolates to be distinguished from isolates with RIF mono-resistance. Drug-resistant tuberculosis (TB) infection is a growing and potent concern, and combating it will be necessary to achieve the WHO’s goal of a 95% reduction in TB deaths by 2035. While prior studies have explored the evolution and spread of drug resistance, we still lack a clear understanding of the fitness costs (if any) imposed by resistance-conferring mutations and the role that Mtb genetic lineage plays in determining the likelihood of resistance evolution. This study offers insight into these questions by assessing the dynamics of resistance evolution in a high-burden Southeast Asian setting with a diverse lineage composition. It demonstrates that there are clear lineage-specific differences in the dynamics of resistance acquisition and transmission and shows that different lineages evolve resistance via characteristic mutational pathways.
A previous investigation has elucidated the landscape of Mtb genomic diversity and transmission dynamics in Ho Chi Minh City, Vietnam. Here, we expand the scope of this survey by adding a substantial number of additional genomes (total sample size: 2,542) and phenotypic drug susceptibility data for the majority of isolates. We aim to explore the prevalence and evolutionary dynamics of drug resistance and our ability to predict drug resistance from sequencing data. Among isolates tested phenotypically against first-line drugs, we observed high rates of streptomycin [STR, 37.7% (N = 573/1,520)] and isoniazid resistance [INH, 25.7% (N = 459/1,786)] and lower rates of resistance to rifampicin [RIF, 4.9% (N = 87/1,786)] and ethambutol [EMB, 4.2% (N = 75/1,785)]. Relative to global benchmarks, resistance to STR and INH was predicted accurately when applying the TB-Profiler algorithm to whole genome sequencing data (sensitivities of 0.81 and 0.87, respectively), while resistance to RIF and EMB was predicted relatively poorly (sensitivities of 0.70 and 0.44, respectively). Exploring the evolution of drug resistance revealed the main phylogenetic lineages to display differing dynamics and tendencies to evolve resistance via mutations in certain genes. The Beijing sublineage L2.2.1 was found to acquire de novo resistance mutations more frequently than isolates from other lineages and to suffer no apparent fitness cost acting to impede the transmission of resistance. Mutations conferring resistance to INH and STR arose earlier, on average, than those conferring resistance to RIF and are now more widespread across the phylogeny. The high prevalence of “background” INH resistance, combined with high rates of RIF mono-resistance (20.7%, N = 18/87), suggests that rapid assays for INH resistance will be valuable in this setting. These tests will allow the detection of INH mono-resistance and will allow multi-drug-resistant isolates to be distinguished from isolates with RIF mono-resistance. IMPORTANCE Drug-resistant tuberculosis (TB) infection is a growing and potent concern, and combating it will be necessary to achieve the WHO’s goal of a 95% reduction in TB deaths by 2035. While prior studies have explored the evolution and spread of drug resistance, we still lack a clear understanding of the fitness costs (if any) imposed by resistance-conferring mutations and the role that Mtb genetic lineage plays in determining the likelihood of resistance evolution. This study offers insight into these questions by assessing the dynamics of resistance evolution in a high-burden Southeast Asian setting with a diverse lineage composition. It demonstrates that there are clear lineage-specific differences in the dynamics of resistance acquisition and transmission and shows that different lineages evolve resistance via characteristic mutational pathways.
A previous investigation has elucidated the landscape of Mtb genomic diversity and transmission dynamics in Ho Chi Minh City, Vietnam. Here, we expand the scope of this survey by adding a substantial number of additional genomes (total sample size: 2,542) and phenotypic drug susceptibility data for the majority of isolates. We aim to explore the prevalence and evolutionary dynamics of drug resistance and our ability to predict drug resistance from sequencing data. Among isolates tested phenotypically against first-line drugs, we observed high rates of streptomycin [STR, 37.7% ( N = 573/1,520)] and isoniazid resistance [INH, 25.7% ( N = 459/1,786)] and lower rates of resistance to rifampicin [RIF, 4.9% ( N = 87/1,786)] and ethambutol [EMB, 4.2% ( N = 75/1,785)]. Relative to global benchmarks, resistance to STR and INH was predicted accurately when applying the TB-Profiler algorithm to whole genome sequencing data (sensitivities of 0.81 and 0.87, respectively), while resistance to RIF and EMB was predicted relatively poorly (sensitivities of 0.70 and 0.44, respectively). Exploring the evolution of drug resistance revealed the main phylogenetic lineages to display differing dynamics and tendencies to evolve resistance via mutations in certain genes. The Beijing sublineage L2.2.1 was found to acquire de novo resistance mutations more frequently than isolates from other lineages and to suffer no apparent fitness cost acting to impede the transmission of resistance. Mutations conferring resistance to INH and STR arose earlier, on average, than those conferring resistance to RIF and are now more widespread across the phylogeny. The high prevalence of “background” INH resistance, combined with high rates of RIF mono-resistance (20.7%, N = 18/87), suggests that rapid assays for INH resistance will be valuable in this setting. These tests will allow the detection of INH mono-resistance and will allow multi-drug-resistant isolates to be distinguished from isolates with RIF mono-resistance.
Author Chang, Xuling
Teo, Yik Ying
Vijay, Srinivasan
Thwaites, Guy
Inouye, Michael
Anh Thu, Do Dang
Huu Lan, Nguyen
Quynh Nhu, Nguyen Thi
Caws, Maxine
Khac Thai, Phan Vuong
Nath, Artika
Edwards, David
Thuong Thuong, Nguyen Thuy
Ong, Rick Twee-Hee
Duc Bang, Nguyen
Hong Chau, Tran Thi
Silcocks, Matthew
Pham, Kym
Chuen Khor, Chiea
Ngoc Nhung, Hoang
Minh Ha, Dang Thi
Heemskerk, A Dorothee
Holt, Kathryn E
Ngoc Ha, Vu Thi
Qin, Youwen
Dunstan, Sarah J
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  fullname: Duc Bang, Nguyen
  organization: Pham Ngoc Thach Hospital for TB and Lung Disease, District 5 , Ho Chi Minh City, Vietnam
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  surname: Dunstan
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  organization: Department of Infectious Diseases, University of Melbourne at the Peter Doherty Institute for Infection and Immunity , Parkville, Victoria, Australia
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Issue 6
Keywords Mycobacterium tuberculosis
antimicrobial resistance
pathogen genomics
Language English
License This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. https://creativecommons.org/licenses/by/4.0
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.
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content type line 23
Matthew Silcocks, Xuling Chang, and Nguyen Thuy Thuong Thuong contributed equally to this article. Author order was determined by the level of contribution.
Kathryn E. Holt and Sarah J. Dunstan contributed equally to this article.
The authors declare no conflict of interest.
Deceased: David Edwards passed away during the preparation of this manuscript.
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PublicationCentury 2000
PublicationDate 2023-Dec-12
PublicationDateYYYYMMDD 2023-12-12
PublicationDate_xml – month: 12
  year: 2023
  text: 2023-Dec-12
  day: 12
PublicationDecade 2020
PublicationPlace United States
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– name: 1752 N St., N.W., Washington, DC
PublicationTitle Microbiology spectrum
PublicationTitleAbbrev Spectrum
PublicationTitleAlternate Microbiol Spectr
PublicationYear 2023
Publisher American Society for Microbiology
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  doi: 10.1016/S2666-5247(21)00301-3
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  doi: 10.1016/s2666-5247(20)30195-6
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  doi: 10.1186/1471-2334-8-166
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Snippet Drug-resistant tuberculosis (TB) infection is a growing and potent concern, and combating it will be necessary to achieve the WHO's goal of a 95% reduction in...
A previous investigation has elucidated the landscape of Mtb genomic diversity and transmission dynamics in Ho Chi Minh City, Vietnam. Here, we expand the...
A previous investigation has elucidated the landscape of Mtb genomic diversity and transmission dynamics in Ho Chi Minh City, Vietnam. Here, we expand the...
IMPORTANCEDrug-resistant tuberculosis (TB) infection is a growing and potent concern, and combating it will be necessary to achieve the WHO's goal of a 95%...
ABSTRACT A previous investigation has elucidated the landscape of Mtb genomic diversity and transmission dynamics in Ho Chi Minh City, Vietnam. Here, we expand...
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SubjectTerms Antimicrobial Chemotherapy
antimicrobial resistance
Mycobacterium tuberculosis
pathogen genomics
Research Article
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Title Evolution and transmission of antibiotic resistance is driven by Beijing lineage Mycobacterium tuberculosis in Vietnam
URI https://www.ncbi.nlm.nih.gov/pubmed/37971428
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