Genomic epidemiology of erythromycin-resistant Bordetella pertussis in China

Macrolides such as erythromycin are the empirical treatment of Bordetella pertussis infections. China has experienced an increase in erythromycin-resistant B. pertussis isolates since they were first reported in 2013. Here, we undertook a genomic study on Chinese B. pertussis isolates from 2012 to 2...

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Main Authors: Zheng Xu, Zengguo Wang, Yang Luan, Yarong Li, Xiaoguai Liu, Xiaokang Peng, Sophie Octavia, Michael Payne, Ruiting Lan
Format: Article
Language:English
Published: Taylor & Francis Group 2019-01-01
Series:Emerging Microbes and Infections
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Online Access:https://www.tandfonline.com/doi/10.1080/22221751.2019.1587315
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author Zheng Xu
Zengguo Wang
Yang Luan
Yarong Li
Xiaoguai Liu
Xiaokang Peng
Sophie Octavia
Michael Payne
Ruiting Lan
author_facet Zheng Xu
Zengguo Wang
Yang Luan
Yarong Li
Xiaoguai Liu
Xiaokang Peng
Sophie Octavia
Michael Payne
Ruiting Lan
author_sort Zheng Xu
collection DOAJ
description Macrolides such as erythromycin are the empirical treatment of Bordetella pertussis infections. China has experienced an increase in erythromycin-resistant B. pertussis isolates since they were first reported in 2013. Here, we undertook a genomic study on Chinese B. pertussis isolates from 2012 to 2015 to elucidate the origins and phylogenetic relationships of erythromycin-resistant B. pertussis isolates in China. A total of 167 Chinese B. pertussis isolates were used for antibiotic sensitivity testing and multiple locus variable-number tandem repeat (VNTR) analysis (MLVA). All except four isolates were erythromycin-resistant and of the four erythromycin-sensitive isolates, three were non-ptxP1. MLVA types (MT), MT55, MT104 and MT195 were the predominant types. Fifty of those isolates were used for whole genome sequencing and phylogenetic analysis. Genome sequencing and phylogenetic analysis revealed three independent erythromycin-resistant lineages and all resistant isolates carried a mutation in the 23S rRNA gene. A novel fhaB3 allele was found uniquely in Chinese ptxP1 isolates and these Chinese ptxP1-ptxA1-fhaB3 had a 5-fold higher mutation rate than the global ptxP1-ptxA1 B. pertussis population. Our results suggest that the evolution of Chinese B. pertussis is likely to be driven by selection pressure from both vaccination and antibiotics. The emergence of the new non-vaccine fhaB3 allele in Chinese B. pertussis population may be a result of selection from vaccination, whereas the expansion of ptxP1-fhaB3 lineages was most likely to be the result of selection pressure from antibiotics. Further monitoring of B. pertussis in China is required to better understand the evolution of the pathogen.
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spelling doaj-art-cd6eb32a10e14bde888adf843d28742d2025-08-20T02:08:14ZengTaylor & Francis GroupEmerging Microbes and Infections2222-17512019-01-018146147010.1080/22221751.2019.1587315Genomic epidemiology of erythromycin-resistant Bordetella pertussis in ChinaZheng Xu0Zengguo Wang1Yang Luan2Yarong Li3Xiaoguai Liu4Xiaokang Peng5Sophie Octavia6Michael Payne7Ruiting Lan8School of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, AustraliaXi’an Center for Disease Prevention and Control, Xi’an, People’s Republic of ChinaXi’an Center for Disease Prevention and Control, Xi’an, People’s Republic of ChinaDepartment of Infectious Diseases, Xi’an Children’s Hospital, Xi’an, People’s Republic of ChinaDepartment of Infectious Diseases, Xi’an Children’s Hospital, Xi’an, People’s Republic of ChinaDepartment of Infectious Diseases, Xi’an Children’s Hospital, Xi’an, People’s Republic of ChinaSchool of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, AustraliaSchool of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, AustraliaSchool of Biotechnology and Biomolecular Sciences, University of New South Wales, Sydney, AustraliaMacrolides such as erythromycin are the empirical treatment of Bordetella pertussis infections. China has experienced an increase in erythromycin-resistant B. pertussis isolates since they were first reported in 2013. Here, we undertook a genomic study on Chinese B. pertussis isolates from 2012 to 2015 to elucidate the origins and phylogenetic relationships of erythromycin-resistant B. pertussis isolates in China. A total of 167 Chinese B. pertussis isolates were used for antibiotic sensitivity testing and multiple locus variable-number tandem repeat (VNTR) analysis (MLVA). All except four isolates were erythromycin-resistant and of the four erythromycin-sensitive isolates, three were non-ptxP1. MLVA types (MT), MT55, MT104 and MT195 were the predominant types. Fifty of those isolates were used for whole genome sequencing and phylogenetic analysis. Genome sequencing and phylogenetic analysis revealed three independent erythromycin-resistant lineages and all resistant isolates carried a mutation in the 23S rRNA gene. A novel fhaB3 allele was found uniquely in Chinese ptxP1 isolates and these Chinese ptxP1-ptxA1-fhaB3 had a 5-fold higher mutation rate than the global ptxP1-ptxA1 B. pertussis population. Our results suggest that the evolution of Chinese B. pertussis is likely to be driven by selection pressure from both vaccination and antibiotics. The emergence of the new non-vaccine fhaB3 allele in Chinese B. pertussis population may be a result of selection from vaccination, whereas the expansion of ptxP1-fhaB3 lineages was most likely to be the result of selection pressure from antibiotics. Further monitoring of B. pertussis in China is required to better understand the evolution of the pathogen.https://www.tandfonline.com/doi/10.1080/22221751.2019.1587315Bordetella pertussiserythromycin-resistantgenomic epidemiologyfhaBptxP1
spellingShingle Zheng Xu
Zengguo Wang
Yang Luan
Yarong Li
Xiaoguai Liu
Xiaokang Peng
Sophie Octavia
Michael Payne
Ruiting Lan
Genomic epidemiology of erythromycin-resistant Bordetella pertussis in China
Emerging Microbes and Infections
Bordetella pertussis
erythromycin-resistant
genomic epidemiology
fhaB
ptxP1
title Genomic epidemiology of erythromycin-resistant Bordetella pertussis in China
title_full Genomic epidemiology of erythromycin-resistant Bordetella pertussis in China
title_fullStr Genomic epidemiology of erythromycin-resistant Bordetella pertussis in China
title_full_unstemmed Genomic epidemiology of erythromycin-resistant Bordetella pertussis in China
title_short Genomic epidemiology of erythromycin-resistant Bordetella pertussis in China
title_sort genomic epidemiology of erythromycin resistant bordetella pertussis in china
topic Bordetella pertussis
erythromycin-resistant
genomic epidemiology
fhaB
ptxP1
url https://www.tandfonline.com/doi/10.1080/22221751.2019.1587315
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