Transmission of blaNDM in Enterobacteriaceae among animals, food and human

ABSTRACTDespite carbapenems not being used in animals, carbapenem-resistant Enterobacterales (CRE), particularly New Delhi metallo-β-lactamase-producing CRE (NDM-CRE), are prevalent in livestock. Concurrently, the incidence of human infections caused by NDM-CRE is rising, particularly in children. A...

Full description

Bibliographic Details
Main Authors: Bo Fu, Jian Xu, Dandan Yin, Chengtao Sun, Dejun Liu, Weishuai Zhai, Rina Bai, Yue Cao, Qin Zhang, Shizhen Ma, Timothy R. Walsh, Fupin Hu, Yang Wang, Congming Wu, Jianzhong Shen
Format: Article
Language:English
Published: Taylor & Francis Group 2024-12-01
Series:Emerging Microbes and Infections
Subjects:
Online Access:https://www.tandfonline.com/doi/10.1080/22221751.2024.2337678
_version_ 1797199926470377472
author Bo Fu
Jian Xu
Dandan Yin
Chengtao Sun
Dejun Liu
Weishuai Zhai
Rina Bai
Yue Cao
Qin Zhang
Shizhen Ma
Timothy R. Walsh
Fupin Hu
Yang Wang
Congming Wu
Jianzhong Shen
author_facet Bo Fu
Jian Xu
Dandan Yin
Chengtao Sun
Dejun Liu
Weishuai Zhai
Rina Bai
Yue Cao
Qin Zhang
Shizhen Ma
Timothy R. Walsh
Fupin Hu
Yang Wang
Congming Wu
Jianzhong Shen
author_sort Bo Fu
collection DOAJ
description ABSTRACTDespite carbapenems not being used in animals, carbapenem-resistant Enterobacterales (CRE), particularly New Delhi metallo-β-lactamase-producing CRE (NDM-CRE), are prevalent in livestock. Concurrently, the incidence of human infections caused by NDM-CRE is rising, particularly in children. Although a positive association between livestock production and human NDM-CRE infections at the national level was identified, the evidence of direct transmission of NDM originating from livestock to humans remains largely unknown. Here, we conducted a cross-sectional study in Chengdu, Sichuan Province, to examine the prevalence of NDM-CRE in chickens and pigs along the breeding–slaughtering–retail chains, in pork in cafeterias of schools, and in colonizations and infections from children's hospital and examined the correlation of NDM-CRE among animals, foods and humans. Overall, the blaNDM increases gradually along the chicken and pig breeding (4.70%/2.0%) –slaughtering (7.60%/22.40%) –retail (65.56%/34.26%) chains. The slaughterhouse has become a hotspot for cross-contamination and amplifier of blaNDM. Notably, 63.11% of pork from the school cafeteria was positive for blaNDM. The prevalence of blaNDM in intestinal and infection samples from children's hospitals was 21.68% and 19.80%, respectively. whole genome sequencing (WGS) analysis revealed the sporadic, not large-scale, clonal spread of NDM-CRE along the chicken and pig breeding–slaughtering–retail chain, with further spreading via IncX3-blaNDM plasmid within each stage of whole chains. Clonal transmission of NDM-CRE is predominant in children's hospitals. The IncX3-blaNDM plasmid was highly prevalent among animals and humans and accounted for 57.7% of Escherichia coli and 91.3% of Klebsiella pneumoniae. Attention should be directed towards the IncX3 plasmid to control the transmission of blaNDM between animals and humans.
first_indexed 2024-04-24T07:23:31Z
format Article
id doaj.art-a141bb1d016f458994a2d9acbb3f7ea2
institution Directory Open Access Journal
issn 2222-1751
language English
last_indexed 2024-04-24T07:23:31Z
publishDate 2024-12-01
publisher Taylor & Francis Group
record_format Article
series Emerging Microbes and Infections
spelling doaj.art-a141bb1d016f458994a2d9acbb3f7ea22024-04-20T19:55:59ZengTaylor & Francis GroupEmerging Microbes and Infections2222-17512024-12-0113110.1080/22221751.2024.2337678Transmission of blaNDM in Enterobacteriaceae among animals, food and humanBo Fu0Jian Xu1Dandan Yin2Chengtao Sun3Dejun Liu4Weishuai Zhai5Rina Bai6Yue Cao7Qin Zhang8Shizhen Ma9Timothy R. Walsh10Fupin Hu11Yang Wang12Congming Wu13Jianzhong Shen14National Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, People’s Republic of ChinaChengdu Women’s and Children’s Central Hospital, School of Medicine, University of Electronic Science and Technology of China, Chengdu, People’s Republic of ChinaInstitute of Antibiotics, Huashan Hospital, Fudan University, Shanghai, People’s Republic of ChinaNational Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, People’s Republic of ChinaNational Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, People’s Republic of ChinaNational Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, People’s Republic of ChinaNational Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, People’s Republic of ChinaNational Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, People’s Republic of ChinaChengdu Women’s and Children’s Central Hospital, School of Medicine, University of Electronic Science and Technology of China, Chengdu, People’s Republic of ChinaNational Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, People’s Republic of ChinaNational Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, People’s Republic of ChinaInstitute of Antibiotics, Huashan Hospital, Fudan University, Shanghai, People’s Republic of ChinaNational Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, People’s Republic of ChinaNational Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, People’s Republic of ChinaNational Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, People’s Republic of ChinaABSTRACTDespite carbapenems not being used in animals, carbapenem-resistant Enterobacterales (CRE), particularly New Delhi metallo-β-lactamase-producing CRE (NDM-CRE), are prevalent in livestock. Concurrently, the incidence of human infections caused by NDM-CRE is rising, particularly in children. Although a positive association between livestock production and human NDM-CRE infections at the national level was identified, the evidence of direct transmission of NDM originating from livestock to humans remains largely unknown. Here, we conducted a cross-sectional study in Chengdu, Sichuan Province, to examine the prevalence of NDM-CRE in chickens and pigs along the breeding–slaughtering–retail chains, in pork in cafeterias of schools, and in colonizations and infections from children's hospital and examined the correlation of NDM-CRE among animals, foods and humans. Overall, the blaNDM increases gradually along the chicken and pig breeding (4.70%/2.0%) –slaughtering (7.60%/22.40%) –retail (65.56%/34.26%) chains. The slaughterhouse has become a hotspot for cross-contamination and amplifier of blaNDM. Notably, 63.11% of pork from the school cafeteria was positive for blaNDM. The prevalence of blaNDM in intestinal and infection samples from children's hospitals was 21.68% and 19.80%, respectively. whole genome sequencing (WGS) analysis revealed the sporadic, not large-scale, clonal spread of NDM-CRE along the chicken and pig breeding–slaughtering–retail chain, with further spreading via IncX3-blaNDM plasmid within each stage of whole chains. Clonal transmission of NDM-CRE is predominant in children's hospitals. The IncX3-blaNDM plasmid was highly prevalent among animals and humans and accounted for 57.7% of Escherichia coli and 91.3% of Klebsiella pneumoniae. Attention should be directed towards the IncX3 plasmid to control the transmission of blaNDM between animals and humans.https://www.tandfonline.com/doi/10.1080/22221751.2024.2337678NDM-CREfood chainIncX3livestockchild
spellingShingle Bo Fu
Jian Xu
Dandan Yin
Chengtao Sun
Dejun Liu
Weishuai Zhai
Rina Bai
Yue Cao
Qin Zhang
Shizhen Ma
Timothy R. Walsh
Fupin Hu
Yang Wang
Congming Wu
Jianzhong Shen
Transmission of blaNDM in Enterobacteriaceae among animals, food and human
Emerging Microbes and Infections
NDM-CRE
food chain
IncX3
livestock
child
title Transmission of blaNDM in Enterobacteriaceae among animals, food and human
title_full Transmission of blaNDM in Enterobacteriaceae among animals, food and human
title_fullStr Transmission of blaNDM in Enterobacteriaceae among animals, food and human
title_full_unstemmed Transmission of blaNDM in Enterobacteriaceae among animals, food and human
title_short Transmission of blaNDM in Enterobacteriaceae among animals, food and human
title_sort transmission of blandm in enterobacteriaceae among animals food and human
topic NDM-CRE
food chain
IncX3
livestock
child
url https://www.tandfonline.com/doi/10.1080/22221751.2024.2337678
work_keys_str_mv AT bofu transmissionofblandminenterobacteriaceaeamonganimalsfoodandhuman
AT jianxu transmissionofblandminenterobacteriaceaeamonganimalsfoodandhuman
AT dandanyin transmissionofblandminenterobacteriaceaeamonganimalsfoodandhuman
AT chengtaosun transmissionofblandminenterobacteriaceaeamonganimalsfoodandhuman
AT dejunliu transmissionofblandminenterobacteriaceaeamonganimalsfoodandhuman
AT weishuaizhai transmissionofblandminenterobacteriaceaeamonganimalsfoodandhuman
AT rinabai transmissionofblandminenterobacteriaceaeamonganimalsfoodandhuman
AT yuecao transmissionofblandminenterobacteriaceaeamonganimalsfoodandhuman
AT qinzhang transmissionofblandminenterobacteriaceaeamonganimalsfoodandhuman
AT shizhenma transmissionofblandminenterobacteriaceaeamonganimalsfoodandhuman
AT timothyrwalsh transmissionofblandminenterobacteriaceaeamonganimalsfoodandhuman
AT fupinhu transmissionofblandminenterobacteriaceaeamonganimalsfoodandhuman
AT yangwang transmissionofblandminenterobacteriaceaeamonganimalsfoodandhuman
AT congmingwu transmissionofblandminenterobacteriaceaeamonganimalsfoodandhuman
AT jianzhongshen transmissionofblandminenterobacteriaceaeamonganimalsfoodandhuman