Antimicrobial resistance in Escherichia coli and Staphylococcus aureus at human-animal interfaces on Chongming Island, Shanghai: A One Health perspective

Antimicrobial resistance (AMR) is a significant concern within the One Health framework due to its ability to spread across multiple interfaces. Phenotypic data remains the primary type for AMR surveillance, but exploring association across multiple interfaces poses certain challenges. In this study...

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Main Authors: Chao Lv, Jun Leng, Minjian Qian, Bingqing Sun, HuiPing Ye, Min Li, Nan Zhou, Zile Cheng, Yiwen Chen, Xiaokui Guo, Jun Shang, Li Zhang, Yongzhang Zhu
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:One Health
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Online Access:http://www.sciencedirect.com/science/article/pii/S2352771424002362
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author Chao Lv
Jun Leng
Minjian Qian
Bingqing Sun
HuiPing Ye
Min Li
Nan Zhou
Zile Cheng
Yiwen Chen
Xiaokui Guo
Jun Shang
Li Zhang
Yongzhang Zhu
author_facet Chao Lv
Jun Leng
Minjian Qian
Bingqing Sun
HuiPing Ye
Min Li
Nan Zhou
Zile Cheng
Yiwen Chen
Xiaokui Guo
Jun Shang
Li Zhang
Yongzhang Zhu
author_sort Chao Lv
collection DOAJ
description Antimicrobial resistance (AMR) is a significant concern within the One Health framework due to its ability to spread across multiple interfaces. Phenotypic data remains the primary type for AMR surveillance, but exploring association across multiple interfaces poses certain challenges. In this study, AMR phenotypic data of clinical and food animal E. coli and S. aureus from Chongming Island over the past five years were analyzed to determine key characteristics of AMR and explore its association at the human-animal interface.The clinical E. coli isolates showed significant resistance to penicillins (83.92 %), cephems (63.05 %), fluoroquinolones (62.21 %), and tetracyclines (57.77 %), while S. aureus exhibited high resistance to penicillinase-labile penicillins (90.89 %), macrolides (51.51 %), penicillinase-stable penicillins (43.96 %), and lincosamides (43.55 %). Extended-spectrum β-lactamase (ESBL)-producing E. coli isolates accounted for 53.26 % (1398/2526), while methicillin-resistant Staphylococcus aureus (MRSA) prevalence was 43.81 % (435/993). Notably, there has been an increase in the proportion of E. coli isolates resistant to 8 to 12 antimicrobial classes, and in the proportion of S. aureus isolates resistant to 5 to 9 classes. Certain multi-drug resistance (MDR) phenotypes were first identified in food animal isolates and later emerged in clinical settings. Meanwhile, several MDR phenotypes were shared between the two interfaces, with 44 identified in E. coli and 12 in S. aureus. Further co-occurrence analysis in E. coli and S. aureus identified several co-occurrence phenotypic pairs or clusters, potentially mediated by a single plasmid or multiple plasmids within a bacterium, indicating potential associations at the human-animal interface.To summarize, a heightened prevalence of MDR in clinical E. coli and S. aureus has been observed, with some MDR profiles appearing in food animals before emerging in clinical settings. The co-occurrence of phenotypic pairs or clusters underscores the potential for AMR association and transmission between humans and food animals. Within the One Health framework, integrating genomic data into AMR monitoring is a crucial next step.
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spelling doaj-art-835a87f7d20148baa969c97301b6d6a52024-12-18T08:49:29ZengElsevierOne Health2352-77142024-12-0119100910Antimicrobial resistance in Escherichia coli and Staphylococcus aureus at human-animal interfaces on Chongming Island, Shanghai: A One Health perspectiveChao Lv0Jun Leng1Minjian Qian2Bingqing Sun3HuiPing Ye4Min Li5Nan Zhou6Zile Cheng7Yiwen Chen8Xiaokui Guo9Jun Shang10Li Zhang11Yongzhang Zhu12School of Global Health, Chinese Center for Tropical Diseases Research, Shanghai Jiao Tong University School of Medicine, Shanghai, China; National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research), National Health Commission Key Laboratory of Parasite and Vector Biology, WHO Collaborating Centre for Tropical Diseases, National Center for International Research on Tropical Diseases, Shanghai, China; School of Public Health, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Clinical Laboratory, Chongming Hospital Affiliated to Shanghai University of Medicine and Health Sciences, Shanghai, ChinaDepartment of Clinical Laboratory, Chongming Hospital Affiliated to Shanghai University of Medicine and Health Sciences, Shanghai, ChinaShanghai Center for Animal Diseases Prevention and Control, Shanghai Institute for Veterinary Drugs and Feeds Control, Shanghai, ChinaChongming District Center for Animal Disease Prevention and Control, Shanghai, ChinaSchool of Global Health, Chinese Center for Tropical Diseases Research, Shanghai Jiao Tong University School of Medicine, Shanghai, China; School of Public Health, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaSchool of Global Health, Chinese Center for Tropical Diseases Research, Shanghai Jiao Tong University School of Medicine, Shanghai, China; School of Public Health, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaSchool of Global Health, Chinese Center for Tropical Diseases Research, Shanghai Jiao Tong University School of Medicine, Shanghai, China; School of Public Health, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaSchool of Global Health, Chinese Center for Tropical Diseases Research, Shanghai Jiao Tong University School of Medicine, Shanghai, China; School of Public Health, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaSchool of Global Health, Chinese Center for Tropical Diseases Research, Shanghai Jiao Tong University School of Medicine, Shanghai, China; School of Public Health, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaShanghai Center for Animal Diseases Prevention and Control, Shanghai Institute for Veterinary Drugs and Feeds Control, Shanghai, China; Corresponding authors.Department of Clinical Laboratory, Chongming Hospital Affiliated to Shanghai University of Medicine and Health Sciences, Shanghai, China; Corresponding authors.School of Global Health, Chinese Center for Tropical Diseases Research, Shanghai Jiao Tong University School of Medicine, Shanghai, China; Corresponding authors.Antimicrobial resistance (AMR) is a significant concern within the One Health framework due to its ability to spread across multiple interfaces. Phenotypic data remains the primary type for AMR surveillance, but exploring association across multiple interfaces poses certain challenges. In this study, AMR phenotypic data of clinical and food animal E. coli and S. aureus from Chongming Island over the past five years were analyzed to determine key characteristics of AMR and explore its association at the human-animal interface.The clinical E. coli isolates showed significant resistance to penicillins (83.92 %), cephems (63.05 %), fluoroquinolones (62.21 %), and tetracyclines (57.77 %), while S. aureus exhibited high resistance to penicillinase-labile penicillins (90.89 %), macrolides (51.51 %), penicillinase-stable penicillins (43.96 %), and lincosamides (43.55 %). Extended-spectrum β-lactamase (ESBL)-producing E. coli isolates accounted for 53.26 % (1398/2526), while methicillin-resistant Staphylococcus aureus (MRSA) prevalence was 43.81 % (435/993). Notably, there has been an increase in the proportion of E. coli isolates resistant to 8 to 12 antimicrobial classes, and in the proportion of S. aureus isolates resistant to 5 to 9 classes. Certain multi-drug resistance (MDR) phenotypes were first identified in food animal isolates and later emerged in clinical settings. Meanwhile, several MDR phenotypes were shared between the two interfaces, with 44 identified in E. coli and 12 in S. aureus. Further co-occurrence analysis in E. coli and S. aureus identified several co-occurrence phenotypic pairs or clusters, potentially mediated by a single plasmid or multiple plasmids within a bacterium, indicating potential associations at the human-animal interface.To summarize, a heightened prevalence of MDR in clinical E. coli and S. aureus has been observed, with some MDR profiles appearing in food animals before emerging in clinical settings. The co-occurrence of phenotypic pairs or clusters underscores the potential for AMR association and transmission between humans and food animals. Within the One Health framework, integrating genomic data into AMR monitoring is a crucial next step.http://www.sciencedirect.com/science/article/pii/S2352771424002362Multidrug resistanceEscherichia coliStaphylococcus aureusClinical isolatesFood animals
spellingShingle Chao Lv
Jun Leng
Minjian Qian
Bingqing Sun
HuiPing Ye
Min Li
Nan Zhou
Zile Cheng
Yiwen Chen
Xiaokui Guo
Jun Shang
Li Zhang
Yongzhang Zhu
Antimicrobial resistance in Escherichia coli and Staphylococcus aureus at human-animal interfaces on Chongming Island, Shanghai: A One Health perspective
One Health
Multidrug resistance
Escherichia coli
Staphylococcus aureus
Clinical isolates
Food animals
title Antimicrobial resistance in Escherichia coli and Staphylococcus aureus at human-animal interfaces on Chongming Island, Shanghai: A One Health perspective
title_full Antimicrobial resistance in Escherichia coli and Staphylococcus aureus at human-animal interfaces on Chongming Island, Shanghai: A One Health perspective
title_fullStr Antimicrobial resistance in Escherichia coli and Staphylococcus aureus at human-animal interfaces on Chongming Island, Shanghai: A One Health perspective
title_full_unstemmed Antimicrobial resistance in Escherichia coli and Staphylococcus aureus at human-animal interfaces on Chongming Island, Shanghai: A One Health perspective
title_short Antimicrobial resistance in Escherichia coli and Staphylococcus aureus at human-animal interfaces on Chongming Island, Shanghai: A One Health perspective
title_sort antimicrobial resistance in escherichia coli and staphylococcus aureus at human animal interfaces on chongming island shanghai a one health perspective
topic Multidrug resistance
Escherichia coli
Staphylococcus aureus
Clinical isolates
Food animals
url http://www.sciencedirect.com/science/article/pii/S2352771424002362
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