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The prevalence and mechanism of fluoroquinolone resistance in Escherichia coli isolated from swine farms in China

BACKGROUND: It has been demonstrated that swine waste is an important reservoir for resistant genes. Moreover, the bacteria carrying resistant genes and originating from swine feces and wastewater could spread to the external environment. Fluoroquinolones (FQs) are widely used in livestock and poult...

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Autores principales: Cheng, Ping, Yang, Yuqi, Li, Fulei, Li, Xiaoting, Liu, Haibin, Fazilani, Saqib Ali, Guo, Wenxin, Xu, Guofeng, Zhang, Xiuying
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7388466/
https://www.ncbi.nlm.nih.gov/pubmed/32723358
http://dx.doi.org/10.1186/s12917-020-02483-4
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author Cheng, Ping
Yang, Yuqi
Li, Fulei
Li, Xiaoting
Liu, Haibin
Fazilani, Saqib Ali
Guo, Wenxin
Xu, Guofeng
Zhang, Xiuying
author_facet Cheng, Ping
Yang, Yuqi
Li, Fulei
Li, Xiaoting
Liu, Haibin
Fazilani, Saqib Ali
Guo, Wenxin
Xu, Guofeng
Zhang, Xiuying
author_sort Cheng, Ping
collection PubMed
description BACKGROUND: It has been demonstrated that swine waste is an important reservoir for resistant genes. Moreover, the bacteria carrying resistant genes and originating from swine feces and wastewater could spread to the external environment. Fluoroquinolones (FQs) are widely used in livestock and poultry for the treatment of bacterial infection. However, resistance to FQs has increased markedly. RESULTS: In this study, swine feces and wastewater were sampled from 21 swine farms of seven provinces in China to investigate the prevalence of FQ resistance, including plasmid-mediated fluoroquinolone resistance (PMQR) genes and the occurrence of target mutations. All isolates showed moderate rate of resistance to norfloxacin (43.0%), ciprofloxacin (47.6%), ofloxacin (47.0%) and levofloxacin (38.8%). The percentage of strains resistant to the four FQs antimicrobials was positively correlated with the danofloxacin (DANO) MIC. Among the 74 FQ-resistant isolates, 39 (52.70%) had mutations in gyrA (S83L and D87 to N, Y, G, or H), 21 (28.38%) had mutations in parC (S80I and E84K), 2 (2.70%) had mutations in parE (I355T and L416F), 26 (35.14%) had mutations in marR (D67N and G103S), 1 (1.35%) had mutations in acrR (V29G). While, no mutation was found in gyrB. There were 7 (9.46%) strains carried the qnrS gene, 29 (39.19%) strains carried the oqxAB gene, and 9 (12.16%) strains carried the aac (6′)-Ib-cr gene. In addition, the conjugation assays showed that qnrS, oqxAB and aac (6′)-Ib-cr could be successfully transferred to E. coli J53 from 4 (57.1%), 20 (69.0%) and 5 (55.6%) donor strains, respectively. There were no qnrA, qnrB, qnrC, qnrD and qepA genes detected. CONCLUSION: The present study showed that DANO-resistant E. coli strains isolated from swine farms had significant cross-resistance to other four FQs antimicrobials. Further study revealed that the resistance mechanisms of swine-derived E. coli to FQs may be attributable to the occurrence of chromosomal mutations (gyrA, parC, parE, marR and acrR genes double-site or single-site mutation) and the presence of PMQR genes (qnrS, oqxAB and aac (6′)-Ib-cr). To the best of our knowledge, one novel mutation marR-D67N was found to be associated with FQ resistance, two mutations parE-L416F and acrR-V29G have never been reported in China.
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spelling pubmed-73884662020-07-31 The prevalence and mechanism of fluoroquinolone resistance in Escherichia coli isolated from swine farms in China Cheng, Ping Yang, Yuqi Li, Fulei Li, Xiaoting Liu, Haibin Fazilani, Saqib Ali Guo, Wenxin Xu, Guofeng Zhang, Xiuying BMC Vet Res Research Article BACKGROUND: It has been demonstrated that swine waste is an important reservoir for resistant genes. Moreover, the bacteria carrying resistant genes and originating from swine feces and wastewater could spread to the external environment. Fluoroquinolones (FQs) are widely used in livestock and poultry for the treatment of bacterial infection. However, resistance to FQs has increased markedly. RESULTS: In this study, swine feces and wastewater were sampled from 21 swine farms of seven provinces in China to investigate the prevalence of FQ resistance, including plasmid-mediated fluoroquinolone resistance (PMQR) genes and the occurrence of target mutations. All isolates showed moderate rate of resistance to norfloxacin (43.0%), ciprofloxacin (47.6%), ofloxacin (47.0%) and levofloxacin (38.8%). The percentage of strains resistant to the four FQs antimicrobials was positively correlated with the danofloxacin (DANO) MIC. Among the 74 FQ-resistant isolates, 39 (52.70%) had mutations in gyrA (S83L and D87 to N, Y, G, or H), 21 (28.38%) had mutations in parC (S80I and E84K), 2 (2.70%) had mutations in parE (I355T and L416F), 26 (35.14%) had mutations in marR (D67N and G103S), 1 (1.35%) had mutations in acrR (V29G). While, no mutation was found in gyrB. There were 7 (9.46%) strains carried the qnrS gene, 29 (39.19%) strains carried the oqxAB gene, and 9 (12.16%) strains carried the aac (6′)-Ib-cr gene. In addition, the conjugation assays showed that qnrS, oqxAB and aac (6′)-Ib-cr could be successfully transferred to E. coli J53 from 4 (57.1%), 20 (69.0%) and 5 (55.6%) donor strains, respectively. There were no qnrA, qnrB, qnrC, qnrD and qepA genes detected. CONCLUSION: The present study showed that DANO-resistant E. coli strains isolated from swine farms had significant cross-resistance to other four FQs antimicrobials. Further study revealed that the resistance mechanisms of swine-derived E. coli to FQs may be attributable to the occurrence of chromosomal mutations (gyrA, parC, parE, marR and acrR genes double-site or single-site mutation) and the presence of PMQR genes (qnrS, oqxAB and aac (6′)-Ib-cr). To the best of our knowledge, one novel mutation marR-D67N was found to be associated with FQ resistance, two mutations parE-L416F and acrR-V29G have never been reported in China. BioMed Central 2020-07-28 /pmc/articles/PMC7388466/ /pubmed/32723358 http://dx.doi.org/10.1186/s12917-020-02483-4 Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.
spellingShingle Research Article
Cheng, Ping
Yang, Yuqi
Li, Fulei
Li, Xiaoting
Liu, Haibin
Fazilani, Saqib Ali
Guo, Wenxin
Xu, Guofeng
Zhang, Xiuying
The prevalence and mechanism of fluoroquinolone resistance in Escherichia coli isolated from swine farms in China
title The prevalence and mechanism of fluoroquinolone resistance in Escherichia coli isolated from swine farms in China
title_full The prevalence and mechanism of fluoroquinolone resistance in Escherichia coli isolated from swine farms in China
title_fullStr The prevalence and mechanism of fluoroquinolone resistance in Escherichia coli isolated from swine farms in China
title_full_unstemmed The prevalence and mechanism of fluoroquinolone resistance in Escherichia coli isolated from swine farms in China
title_short The prevalence and mechanism of fluoroquinolone resistance in Escherichia coli isolated from swine farms in China
title_sort prevalence and mechanism of fluoroquinolone resistance in escherichia coli isolated from swine farms in china
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7388466/
https://www.ncbi.nlm.nih.gov/pubmed/32723358
http://dx.doi.org/10.1186/s12917-020-02483-4
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