Prevalence and Genomic Characteristics of mcr-Positive Escherichia coli Strains Isolated from Humans, Pigs, and Foods in China
ABSTRACT Colistin is one of the last-resort antibiotics for treating infections caused by multidrug-resistant (MDR) Gram-negative bacteria. However, mcr genes conferring resistance to colistin have been widely identified, which is considered a global threat to public health. Here, we investigated th...
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2023-06-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.04569-22 |
| _version_ | 1797803388888416256 |
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| author | Xiaoyu Lu Pei Zhang Pengcheng Du Xiuli Zhang Juan Wang Yingying Yang Honghu Sun Zhiqiang Wang Shenghui Cui Ruichao Li Li Bai |
| author_facet | Xiaoyu Lu Pei Zhang Pengcheng Du Xiuli Zhang Juan Wang Yingying Yang Honghu Sun Zhiqiang Wang Shenghui Cui Ruichao Li Li Bai |
| author_sort | Xiaoyu Lu |
| collection | DOAJ |
| description | ABSTRACT Colistin is one of the last-resort antibiotics for treating infections caused by multidrug-resistant (MDR) Gram-negative bacteria. However, mcr genes conferring resistance to colistin have been widely identified, which is considered a global threat to public health. Here, we investigated the prevalence and characteristics of mcr-harboring Escherichia coli strains isolated from humans, animals, and foods in China by PCR, antimicrobial susceptibility testing, conjugation experiments, molecular typing, genome sequencing, and bioinformatics analysis. In total, 135 mcr-1-harboring E. coli isolates were acquired from 847 samples, and 6 isolates carried mcr-3. Among them, 131 isolates were MDR bacteria. Sixty-five resistance genes conferring resistance to multiple antimicrobials were identified in 135 isolates. The diverse pulsed-field gel electrophoresis (PFGE) patterns and sequence types (STs) of mcr-1-carrying isolates demonstrated that clonal dissemination was not the dominant mode of mcr-1 transmission. Seven types of plasmids were able to carry mcr-1 in this study, including IncI2, IncX4, IncHI2, p0111, IncY, and two hybrid plasmids. The genetic structures carrying mcr-1 of 60 isolates were successfully transferred into the recipient, including 25 IncI2 plasmids, 23 IncX4 plasmids, and an IncHI2 plasmid. mcr-1–pap2 was the dominant mcr-1-bearing structure, followed by ISApl1–mcr-1–pap2–ISApl1 (Tn6330) and ISApl1–mcr-1–pap2, among 7 mcr-1-bearing structures of 135 isolates. In conclusion, IncI2, IncX4, and IncHI2 plasmids were the major vectors spreading mcr-1 from different geographical locations and sources. The prevalence of Tn6330 may accelerate the transmission of mcr-1. Continuous surveillance of mcr-1 and variants in bacteria is vital for evaluating the public health risk posed by mcr genes. IMPORTANCE The spread of polymyxin-resistant Enterobacteriaceae poses a significant threat to public health and challenges the therapeutic options for treating infections on a global level. In this study, mcr-1-bearing ST10 E. coli was isolated from pigs, pork, and humans simultaneously, which demonstrated that ST10 E. coli was an important vehicle for the spread of mcr-1 among animals, foods, and humans. The high prevalence of mcr-1-positive E. coli strains in pigs and pork and the horizontal transmission of mcr-1-bearing plasmids in diverse E. coli strains suggest that pigs and pork are important sources of mcr-1-positive strains in humans and pose a potential threat to public health. Additional research on the prevalence and characteristics of mcr-1-positive E. coli is still required to facilitate early warning to improve polymyxin management in hospitals. |
| first_indexed | 2024-03-13T05:20:04Z |
| format | Article |
| id | doaj.art-55c59fc07e9645ecb3d208167121518d |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-13T05:20:04Z |
| publishDate | 2023-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-55c59fc07e9645ecb3d208167121518d2023-06-15T13:18:33ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-06-0111310.1128/spectrum.04569-22Prevalence and Genomic Characteristics of mcr-Positive Escherichia coli Strains Isolated from Humans, Pigs, and Foods in ChinaXiaoyu Lu0Pei Zhang1Pengcheng Du2Xiuli Zhang3Juan Wang4Yingying Yang5Honghu Sun6Zhiqiang Wang7Shenghui Cui8Ruichao Li9Li Bai10Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaKey Laboratory of Food Safety Risk Assessment, National Health Commission of the People’s Republic of China, China National Center for Food Safety Risk Assessment, Beijing, ChinaInstitute of Infectious Diseases, Beijing Ditan Hospital, Capital Medical University, Beijing, ChinaCenter for Disease Control and Prevention of Henan Province, Zhengzhou, ChinaCollege of Veterinary Medicine, Northwest A&F University, Yangling, Shaanxi, ChinaDepartment of Neurology, Gaotang County People's Hospital, Gaotang, Shandong, ChinaChengdu Institute for Food and Drug Control, Chengdu, ChinaJiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaDepartment of Food Science, National Institutes for Food and Drug Control, Beijing, ChinaJiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Yangzhou, Jiangsu, ChinaKey Laboratory of Food Safety Risk Assessment, National Health Commission of the People’s Republic of China, China National Center for Food Safety Risk Assessment, Beijing, ChinaABSTRACT Colistin is one of the last-resort antibiotics for treating infections caused by multidrug-resistant (MDR) Gram-negative bacteria. However, mcr genes conferring resistance to colistin have been widely identified, which is considered a global threat to public health. Here, we investigated the prevalence and characteristics of mcr-harboring Escherichia coli strains isolated from humans, animals, and foods in China by PCR, antimicrobial susceptibility testing, conjugation experiments, molecular typing, genome sequencing, and bioinformatics analysis. In total, 135 mcr-1-harboring E. coli isolates were acquired from 847 samples, and 6 isolates carried mcr-3. Among them, 131 isolates were MDR bacteria. Sixty-five resistance genes conferring resistance to multiple antimicrobials were identified in 135 isolates. The diverse pulsed-field gel electrophoresis (PFGE) patterns and sequence types (STs) of mcr-1-carrying isolates demonstrated that clonal dissemination was not the dominant mode of mcr-1 transmission. Seven types of plasmids were able to carry mcr-1 in this study, including IncI2, IncX4, IncHI2, p0111, IncY, and two hybrid plasmids. The genetic structures carrying mcr-1 of 60 isolates were successfully transferred into the recipient, including 25 IncI2 plasmids, 23 IncX4 plasmids, and an IncHI2 plasmid. mcr-1–pap2 was the dominant mcr-1-bearing structure, followed by ISApl1–mcr-1–pap2–ISApl1 (Tn6330) and ISApl1–mcr-1–pap2, among 7 mcr-1-bearing structures of 135 isolates. In conclusion, IncI2, IncX4, and IncHI2 plasmids were the major vectors spreading mcr-1 from different geographical locations and sources. The prevalence of Tn6330 may accelerate the transmission of mcr-1. Continuous surveillance of mcr-1 and variants in bacteria is vital for evaluating the public health risk posed by mcr genes. IMPORTANCE The spread of polymyxin-resistant Enterobacteriaceae poses a significant threat to public health and challenges the therapeutic options for treating infections on a global level. In this study, mcr-1-bearing ST10 E. coli was isolated from pigs, pork, and humans simultaneously, which demonstrated that ST10 E. coli was an important vehicle for the spread of mcr-1 among animals, foods, and humans. The high prevalence of mcr-1-positive E. coli strains in pigs and pork and the horizontal transmission of mcr-1-bearing plasmids in diverse E. coli strains suggest that pigs and pork are important sources of mcr-1-positive strains in humans and pose a potential threat to public health. Additional research on the prevalence and characteristics of mcr-1-positive E. coli is still required to facilitate early warning to improve polymyxin management in hospitals.https://journals.asm.org/doi/10.1128/spectrum.04569-22Escherichia colipolymyxin Bmcr-1humanspigsfoods |
| spellingShingle | Xiaoyu Lu Pei Zhang Pengcheng Du Xiuli Zhang Juan Wang Yingying Yang Honghu Sun Zhiqiang Wang Shenghui Cui Ruichao Li Li Bai Prevalence and Genomic Characteristics of mcr-Positive Escherichia coli Strains Isolated from Humans, Pigs, and Foods in China Microbiology Spectrum Escherichia coli polymyxin B mcr-1 humans pigs foods |
| title | Prevalence and Genomic Characteristics of mcr-Positive Escherichia coli Strains Isolated from Humans, Pigs, and Foods in China |
| title_full | Prevalence and Genomic Characteristics of mcr-Positive Escherichia coli Strains Isolated from Humans, Pigs, and Foods in China |
| title_fullStr | Prevalence and Genomic Characteristics of mcr-Positive Escherichia coli Strains Isolated from Humans, Pigs, and Foods in China |
| title_full_unstemmed | Prevalence and Genomic Characteristics of mcr-Positive Escherichia coli Strains Isolated from Humans, Pigs, and Foods in China |
| title_short | Prevalence and Genomic Characteristics of mcr-Positive Escherichia coli Strains Isolated from Humans, Pigs, and Foods in China |
| title_sort | prevalence and genomic characteristics of mcr positive escherichia coli strains isolated from humans pigs and foods in china |
| topic | Escherichia coli polymyxin B mcr-1 humans pigs foods |
| url | https://journals.asm.org/doi/10.1128/spectrum.04569-22 |
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