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A survey of Chinese pig farms and human healthcare isolates reveals separate human and animal MRSA populations

Geng Zou, Marta Matuszewska, Ming Jia, Jianwei Zhou, Xiaoliang Ba, Juan Duan, Caishi Zhang, Jian Zhao, Meng Tao, Jingyan Fan, Xiangming Zhang, Wenping Jin, Tianpen Cui, Xianyu Zeng, Min Jia, Xiaojuan Qian, Chao Huang, Wenxiao Zhuo, Zhiming Yao, Lijun Zhang, Shaowen Li, Lu Li, Qi Huang, View ORCID ProfileBin Wu, Huanchun Chen, Alexander W. Tucker, View ORCID ProfileAndrew J. Grant, Mark A. Holmes, View ORCID ProfileRui Zhou
doi: https://doi.org/10.1101/2021.08.02.454852
Geng Zou
1State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan 430070, China
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Marta Matuszewska
2Department of Veterinary Medicine, University of Cambridge, Cambridge, UK
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Ming Jia
1State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan 430070, China
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Jianwei Zhou
1State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan 430070, China
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Xiaoliang Ba
2Department of Veterinary Medicine, University of Cambridge, Cambridge, UK
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Juan Duan
1State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan 430070, China
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Caishi Zhang
3Jianli People’s Hospital, Jianli 433300, China
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Jian Zhao
1State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan 430070, China
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Meng Tao
1State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan 430070, China
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Jingyan Fan
1State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan 430070, China
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Xiangming Zhang
4Wuhan Third Hospital, Wuhan 430060, China
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Wenping Jin
4Wuhan Third Hospital, Wuhan 430060, China
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Tianpen Cui
5Wuhan First Hospital, Wuhan 430014, China
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Xianyu Zeng
5Wuhan First Hospital, Wuhan 430014, China
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Min Jia
5Wuhan First Hospital, Wuhan 430014, China
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Xiaojuan Qian
6Huangmei People’s Hospital, Huangmei 435500, China
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Chao Huang
1State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan 430070, China
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Wenxiao Zhuo
1State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan 430070, China
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Zhiming Yao
1State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan 430070, China
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Lijun Zhang
1State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan 430070, China
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Shaowen Li
1State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan 430070, China
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Lu Li
1State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan 430070, China
7Cooperative Innovation Center of Sustainable Pig Production, Wuhan 430070, China
8International Research Center for Animal Diseases (MOST), Wuhan 430070, China
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Qi Huang
1State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan 430070, China
7Cooperative Innovation Center of Sustainable Pig Production, Wuhan 430070, China
8International Research Center for Animal Diseases (MOST), Wuhan 430070, China
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Bin Wu
1State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan 430070, China
7Cooperative Innovation Center of Sustainable Pig Production, Wuhan 430070, China
8International Research Center for Animal Diseases (MOST), Wuhan 430070, China
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  • ORCID record for Bin Wu
Huanchun Chen
1State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan 430070, China
7Cooperative Innovation Center of Sustainable Pig Production, Wuhan 430070, China
8International Research Center for Animal Diseases (MOST), Wuhan 430070, China
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Alexander W. Tucker
2Department of Veterinary Medicine, University of Cambridge, Cambridge, UK
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Andrew J. Grant
2Department of Veterinary Medicine, University of Cambridge, Cambridge, UK
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Mark A. Holmes
2Department of Veterinary Medicine, University of Cambridge, Cambridge, UK
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  • For correspondence: rzhou@mail.hzau.edu.cn mah1@cam.ac.uk
Rui Zhou
1State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan 430070, China
7Cooperative Innovation Center of Sustainable Pig Production, Wuhan 430070, China
8International Research Center for Animal Diseases (MOST), Wuhan 430070, China
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  • For correspondence: rzhou@mail.hzau.edu.cn mah1@cam.ac.uk
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Abstract

There has been increasing concern that the overuse of antibiotics in livestock farming is contributing to the burden of antimicrobial resistance in people. Farmed animals in Europe and North America, particularly pigs, provide a reservoir for livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA, ST398) found in people. This study was designed to investigate the contribution of MRSA from Chinese pig farms to human infection and carriage.A collection of 603 S. aureus were isolated from 55 pig farms and 4 hospitals (MRSA= 285, 198; MSSA= 50, 70) in central China, a high pig farming density area, during 2017-2018. CC9 MRSA accounting for 93% of all farm MRSA isolates, while no was found in hospitals. ST398 isolates were found on three farms (n = 23) and three hospitals (n = 12). None of the ST398 from this study belong to the livestock clade of the LA-MRSA commonly found in Europe and North America. The hospital ST398 MRSA isolates formed a clade that was clearly separate from the farm ST398 MRSA and MSSA isolates, and all possessed human immune evasion cluster genes which were absent from all the pig farm ST398 isolates. Despite the presence of high levels of MRSA found on Chinese pig farms we found no evidence of them spilling over to the human population. Nevertheless, the ST398 MRSA obtained from human samples appear to be part of a widely distributed lineage in China. And the new animal adapted ST398 lineage that emerged in China should also be alarmed.

Importance We disclosed the fact that although the high MRSA positive rate in Chinese hospitals and pig farms should be alarmed, they might be two separate issues. The new CC398 clades we identified highlight that the host adaption of the MRSA lineage is kept changing. These results suggest that continued surveillance of MRSA in livestock is necessary. We found that the pig farm MRSA isolates had unique antimicrobial resistance genes while most of the hospital MRSA isolates had human immune evasion cluster genes. These features could be used to distinguish the pig farm associated S. aureus in clinical laboratories. The policies of reducing antimicrobials use in livestock were implemented in China since 2020. Our study described the situation of MRSA populations in pig farms and hospitals in Central China before 2020, which provides a potential opportunity for future studies to evaluate the effects of the policies.

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Posted August 03, 2021.
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A survey of Chinese pig farms and human healthcare isolates reveals separate human and animal MRSA populations
Geng Zou, Marta Matuszewska, Ming Jia, Jianwei Zhou, Xiaoliang Ba, Juan Duan, Caishi Zhang, Jian Zhao, Meng Tao, Jingyan Fan, Xiangming Zhang, Wenping Jin, Tianpen Cui, Xianyu Zeng, Min Jia, Xiaojuan Qian, Chao Huang, Wenxiao Zhuo, Zhiming Yao, Lijun Zhang, Shaowen Li, Lu Li, Qi Huang, Bin Wu, Huanchun Chen, Alexander W. Tucker, Andrew J. Grant, Mark A. Holmes, Rui Zhou
bioRxiv 2021.08.02.454852; doi: https://doi.org/10.1101/2021.08.02.454852
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A survey of Chinese pig farms and human healthcare isolates reveals separate human and animal MRSA populations
Geng Zou, Marta Matuszewska, Ming Jia, Jianwei Zhou, Xiaoliang Ba, Juan Duan, Caishi Zhang, Jian Zhao, Meng Tao, Jingyan Fan, Xiangming Zhang, Wenping Jin, Tianpen Cui, Xianyu Zeng, Min Jia, Xiaojuan Qian, Chao Huang, Wenxiao Zhuo, Zhiming Yao, Lijun Zhang, Shaowen Li, Lu Li, Qi Huang, Bin Wu, Huanchun Chen, Alexander W. Tucker, Andrew J. Grant, Mark A. Holmes, Rui Zhou
bioRxiv 2021.08.02.454852; doi: https://doi.org/10.1101/2021.08.02.454852

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