Transmission of Carbapenem Resistance Between Human and Animal NDM-Positive Escherichia coli Strains
Yingbo Shen,
Fupin Hu,
Yongqiang Wang,
Dandan Yin,
Lu Yang,
Yiqiang Chen,
Chunyan Xu,
Jiyun Li,
Junyao Jiang,
Xueyang Wang,
Yulin Fu,
Dongyan Shao,
Dejun Liu,
Tengfei Ma,
Chang Cai,
Zhangqi Shen,
Shaolin Wang,
Juan Li,
Rong Zhang,
Yuebin Ke,
Congming Wu,
Jianzhong Shen,
Timothy R. Walsh,
Yang Wang
Affiliations
Yingbo Shen
Beijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China; CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China
Fupin Hu
Institute of Antibiotics & Key Laboratory of Clinical Pharmacology of Antibiotics (MoH), Huashan Hospital, Fudan University, Shanghai 200040, China
Yongqiang Wang
Department of Preventive Veterinary Medicine, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China
Dandan Yin
Institute of Antibiotics & Key Laboratory of Clinical Pharmacology of Antibiotics (MoH), Huashan Hospital, Fudan University, Shanghai 200040, China
Lu Yang
Beijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China
Yiqiang Chen
State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, China
Chunyan Xu
Beijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China
Jiyun Li
Beijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China
Junyao Jiang
Beijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China
Xueyang Wang
Beijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China
Yulin Fu
Beijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China
Dongyan Shao
Beijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China
Dejun Liu
Beijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China
Tengfei Ma
Beijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China
Chang Cai
College of Animal Science and Technology, College of Veterinary Medicine, Zhejiang A and F University, Hangzhou 311300, China
Zhangqi Shen
Beijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China
Shaolin Wang
Beijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China
Juan Li
State Key Laboratory for Infectious Disease Prevention and Control, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Disease, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention (CDC), Beijing 102206, China
Rong Zhang
The Second Affiliated Hospital of Zhejiang University, Zhejiang University, Hangzhou 310009, China
Yuebin Ke
Key Laboratory of Genetics & Molecular Medicine of Shenzhen, Shenzhen Center for Disease Control and Prevention, Shenzhen 518055, China
Congming Wu
Beijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China
Jianzhong Shen
Beijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China; Corresponding authors.
Timothy R. Walsh
Department of Zoology, University of Oxford, Oxford OX1 3SZ, UK; Corresponding authors.
Yang Wang
Beijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China; Corresponding authors.
Although carbapenem use is prohibited in animals in China, carbapenem-resistant Escherichia coli (CREC), especially New Delhi metallo-β-lactamase (NDM)-producing strains, are widely prevalent in food-producing animals. At present, the impact of livestock-associated CREC strains on human populations at the national level is unknown. Here, we conduct a retrospective cross-sectional study to investigate the prevalence of CREC from clinical settings across 22 Chinese provinces or municipalities and analyze anthropogenic factors associated with their presence. We also ascertain the blaNDM and blaKPC abundance among pig and chicken farms and present a detailed genomic framework for CREC of animal and human origin. Overall, 631/29 799 (2.1%) clinical Escherichia coli (E. coli) isolates were identified as CREC. Multivariable analysis revealed that being male, an age below 1, an age between 13 and 18, provinces with greater chicken production, and provinces with higher pig production were associated with higher odds of CREC infection. In general, 73.8% (n = 45/61) of pig farms and 62.2% (n = 28/45) of chicken farms had a blaNDM abundance of 1 × 10−5 to 1 × 10−3 and 1 × 10−3 to 1 × 10−2, respectively. Among all the Chinese NDM-positive E. coli (n = 463) available at the National Center for Biotechnology Information (NCBI), the genomic analysis revealed that blaNDM-5 and IncX3 were the predominant carbapenemase gene-plasmid combination, while a highly homogeneous relationship between NDM-positive isolates from humans and animals was demonstrated at the plasmid and core genome levels. All the findings suggest frequent CREC transmission between humans and animals, indicating that further discussions on the use of antibiotics in animals and humans are needed, both in China and across the globe.
