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Analysis of isolates from Bangladesh highlights multiple ways to carry resistance genes in Salmonella Typhi

BACKGROUND: Typhoid fever, caused by Salmonella Typhi, follows a fecal-oral transmission route and is a major global public health concern, especially in developing countries like Bangladesh. Increasing emergence of antimicrobial resistance (AMR) is a serious issue; the list of treatments for typhoi...

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Autores principales: Lima, Nicholas Costa Barroso, Tanmoy, Arif M., Westeel, Emilie, de Almeida, Luiz Gonzaga Paula, Rajoharison, Alain, Islam, Maksuda, Endtz, Hubert P., Saha, Samir K., de Vasconcelos, Ana Tereza Ribeiro, Komurian-Pradel, Florence
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6599262/
https://www.ncbi.nlm.nih.gov/pubmed/31253105
http://dx.doi.org/10.1186/s12864-019-5916-6
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author Lima, Nicholas Costa Barroso
Tanmoy, Arif M.
Westeel, Emilie
de Almeida, Luiz Gonzaga Paula
Rajoharison, Alain
Islam, Maksuda
Endtz, Hubert P.
Saha, Samir K.
de Vasconcelos, Ana Tereza Ribeiro
Komurian-Pradel, Florence
author_facet Lima, Nicholas Costa Barroso
Tanmoy, Arif M.
Westeel, Emilie
de Almeida, Luiz Gonzaga Paula
Rajoharison, Alain
Islam, Maksuda
Endtz, Hubert P.
Saha, Samir K.
de Vasconcelos, Ana Tereza Ribeiro
Komurian-Pradel, Florence
author_sort Lima, Nicholas Costa Barroso
collection PubMed
description BACKGROUND: Typhoid fever, caused by Salmonella Typhi, follows a fecal-oral transmission route and is a major global public health concern, especially in developing countries like Bangladesh. Increasing emergence of antimicrobial resistance (AMR) is a serious issue; the list of treatments for typhoid fever is ever-decreasing. In addition to IncHI1-type plasmids, Salmonella genomic island (SGI) 11 has been reported to carry AMR genes. Although reports suggest a recent reduction in multidrug resistance (MDR) in the Indian subcontinent, the corresponding genomic changes in the background are unknown. RESULTS: Here, we assembled and annotated complete closed chromosomes and plasmids for 73 S. Typhi isolates using short-length Illumina reads. S. Typhi had an open pan-genome, and the core genome was smaller than previously reported. Considering AMR genes, we identified five variants of SGI11, including the previously reported reference sequence. Five plasmids were identified, including the new plasmids pK91 and pK43; pK43and pHCM2 were not related to AMR. The pHCM1, pPRJEB21992 and pK91 plasmids carried AMR genes and, along with the SGI11 variants, were responsible for resistance phenotypes. pK91 also contained qnr genes, conferred high ciprofloxacin resistance and was related to the H58-sublineage Bdq, which shows the same phenotype. The presence of plasmids (pHCM1 and pK91) and SGI11 were linked to two H58-lineages, Ia and Bd. Loss of plasmids and integration of resistance genes in genomic islands could contribute to the fitness advantage of lineage Ia isolates. CONCLUSIONS: Such events may explain why lineage Ia is globally widespread, while the Bd lineage is locally restricted. Further studies are required to understand how these S. Typhi AMR elements spread and generate new variants. Preventive measures such as vaccination programs should also be considered in endemic countries; such initiatives could potentially reduce the spread of AMR. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5916-6) contains supplementary material, which is available to authorized users.
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spelling pubmed-65992622019-07-11 Analysis of isolates from Bangladesh highlights multiple ways to carry resistance genes in Salmonella Typhi Lima, Nicholas Costa Barroso Tanmoy, Arif M. Westeel, Emilie de Almeida, Luiz Gonzaga Paula Rajoharison, Alain Islam, Maksuda Endtz, Hubert P. Saha, Samir K. de Vasconcelos, Ana Tereza Ribeiro Komurian-Pradel, Florence BMC Genomics Research Article BACKGROUND: Typhoid fever, caused by Salmonella Typhi, follows a fecal-oral transmission route and is a major global public health concern, especially in developing countries like Bangladesh. Increasing emergence of antimicrobial resistance (AMR) is a serious issue; the list of treatments for typhoid fever is ever-decreasing. In addition to IncHI1-type plasmids, Salmonella genomic island (SGI) 11 has been reported to carry AMR genes. Although reports suggest a recent reduction in multidrug resistance (MDR) in the Indian subcontinent, the corresponding genomic changes in the background are unknown. RESULTS: Here, we assembled and annotated complete closed chromosomes and plasmids for 73 S. Typhi isolates using short-length Illumina reads. S. Typhi had an open pan-genome, and the core genome was smaller than previously reported. Considering AMR genes, we identified five variants of SGI11, including the previously reported reference sequence. Five plasmids were identified, including the new plasmids pK91 and pK43; pK43and pHCM2 were not related to AMR. The pHCM1, pPRJEB21992 and pK91 plasmids carried AMR genes and, along with the SGI11 variants, were responsible for resistance phenotypes. pK91 also contained qnr genes, conferred high ciprofloxacin resistance and was related to the H58-sublineage Bdq, which shows the same phenotype. The presence of plasmids (pHCM1 and pK91) and SGI11 were linked to two H58-lineages, Ia and Bd. Loss of plasmids and integration of resistance genes in genomic islands could contribute to the fitness advantage of lineage Ia isolates. CONCLUSIONS: Such events may explain why lineage Ia is globally widespread, while the Bd lineage is locally restricted. Further studies are required to understand how these S. Typhi AMR elements spread and generate new variants. Preventive measures such as vaccination programs should also be considered in endemic countries; such initiatives could potentially reduce the spread of AMR. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5916-6) contains supplementary material, which is available to authorized users. BioMed Central 2019-06-28 /pmc/articles/PMC6599262/ /pubmed/31253105 http://dx.doi.org/10.1186/s12864-019-5916-6 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Lima, Nicholas Costa Barroso
Tanmoy, Arif M.
Westeel, Emilie
de Almeida, Luiz Gonzaga Paula
Rajoharison, Alain
Islam, Maksuda
Endtz, Hubert P.
Saha, Samir K.
de Vasconcelos, Ana Tereza Ribeiro
Komurian-Pradel, Florence
Analysis of isolates from Bangladesh highlights multiple ways to carry resistance genes in Salmonella Typhi
title Analysis of isolates from Bangladesh highlights multiple ways to carry resistance genes in Salmonella Typhi
title_full Analysis of isolates from Bangladesh highlights multiple ways to carry resistance genes in Salmonella Typhi
title_fullStr Analysis of isolates from Bangladesh highlights multiple ways to carry resistance genes in Salmonella Typhi
title_full_unstemmed Analysis of isolates from Bangladesh highlights multiple ways to carry resistance genes in Salmonella Typhi
title_short Analysis of isolates from Bangladesh highlights multiple ways to carry resistance genes in Salmonella Typhi
title_sort analysis of isolates from bangladesh highlights multiple ways to carry resistance genes in salmonella typhi
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6599262/
https://www.ncbi.nlm.nih.gov/pubmed/31253105
http://dx.doi.org/10.1186/s12864-019-5916-6
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