Prevalence of tet(X4) in Escherichia coli From Duck Farms in Southeast China.

Yang Yu,Chong Chen,Chao-Yue Cui,Jian Sun,Ya-Hong Liu,Xu Kuang,Xiao-Ping Liao,Min-Ge Wang

doi:10.3389/fmicb.2021.716393

Yang Yu, Chong Chen + Show 6 more

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https://doi.org/10.3389/fmicb.2021.716393

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Abstract

ObjectivesCarbapenems, colistin, and tigecycline are critically important antibiotics in clinics. After the global appearance of blaNDM and mcr mediating the resistance to carbapenems and colistin, respectively, tigecycline becomes the last-resort drug against severe human infections caused by multidrug-resistant bacteria. Recently, a mobile tigecycline resistance gene tet(X4) has been identified in Escherichia coli, Klebsiella pneumoniae, and Acinetobacter baumannii that causes high resistance to tigecycline and other tetracyclines. In this study, the prevalence of tet(X4) in E. coli isolates from duck and goose farms in Southeast China was identified and characterized.MethodsFeces, soil, sewage, and dust samples were collected from duck and goose farms along with the southeast coast provinces of China. Antimicrobial susceptibility testing and polymerase chain reaction screening were performed to investigate the phenotype and genotype of tigecycline resistance. Conjugation, S1 pulsed-field gel electrophoresis (PFGE), and whole-genome sequencing were used to determine the transferability, genetic location, and the genomic characteristics of tet(X4).ResultsIn total, 1,716 samples were collected, and 16 isolates (0.9%) recovered from Guangdong, Shandong, and Jiangsu were positive for tet(X4) gene with tigecycline minimum inhibitory concentrations ≥16 mg/L. Notably, among these tet(X4)-positive E. coil isolates, seven of them were from the environment samples (soil and sewage). PFGE and multilocus sequence typing demonstrated that ST3997 was the most prevalent sequence type (eight isolates, 50%) in Jiangsu province. By conjugation assays, 11 isolates were able to transfer tet(X4) plasmid to E. coli C600 recipient, and these plasmids belonged to IncHI1 and IncX1 detected by sequence analysis. tet(X4) was found adjacent to an insertion sequence ISCR2 downstream and a catD gene upstream for all isolates. In addition, multiple-drug resistance to tigecycline, chlortetracycline, ampicillin, florfenicol, ciprofloxacin, gentamicin, trimethoprim/sulfamethoxazole, and fosfomycin was profiled in most of the tet(X4)-positive isolates.ConclusionThe identification of tet(X4) harboring E. coli strains in duck farms and their surrounding environment enlarges our knowledge of the variety and prevalence of tigecycline resistance. The prevalence of tet(X4) raises concern for the use of tetracyclines in animal farming, and the tet(X4) gene should be listed as primary gene for resistance surveillance.

Highlights

Carbapenems, colistin, and tigecycline are considered as the last-resort antibiotics against severe human infections caused by multidrug-resistant (MDR) bacteria
We investigated the prevalence of tet(X4) in duck and goose farms belonging to different breeding patterns in Southeast China
One to three well-formed tigecycline non-susceptible colonies were randomly selected for polymerase chain reaction (PCR) screening of tet(X), and the tet(X4) subtypes were further confirmed by full-length amplification and Sanger sequencing, as previously described (Sun et al, 2019a)

Summary

Introduction

Carbapenems, colistin, and tigecycline are considered as the last-resort antibiotics against severe human infections caused by multidrug-resistant (MDR) bacteria. The discovery of a series of carbapenems resistance genes, such as blaOXA, blaNDM, blaVIM, and blaKPC, as well as the mobile colistin resistance mcr gene, has compromised the effectiveness of carbapenems and colistin in clinics (Gangcuangco et al, 2016; Lunha et al, 2016; Wang et al, 2017; Gaibani et al, 2020) Under such circumstances, tigecycline was considered as the last chance for treatment of extensively drug-resistant pathogens. Tigecycline, a glycylcycline tetracycline, has demonstrated antibacterial activity across a broad spectrum of Gram-positive, Gram-negative, anaerobic, and atypical bacteria (Peterson, 2008) It was approved for complicated skin and intra-abdominal infections by both the Food and Drug Administration (FDA) in the United States and the European Medicines Agency (European medicines agency, 2013). Tigecycline exhibits antimicrobial susceptibility against broadspectrum pathogens including the CRE and even colistinmeropenem–coresistant Escherichia coli (Yu et al, 2019)

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