Novel Class 1 Integron Structures in High-Risk Metallo-β-Lactamase-Producing Pseudomonas aeruginosa ST235 and ST654 From Companion Animals

IF 2.3 2区农林科学 Q3 INFECTIOUS DISEASES

Zoonoses and Public Health Pub Date : 2025-05-04 DOI:10.1111/zph.13224

Chavin Leelapsawas, Rungtip Chuanchuen, Parinya Sroithongkham, Vincent Perreten, Pattrarat Chanchaithong

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引用次数: 0

Abstract

Introduction

Carbapenemase-producing Pseudomonas aeruginosa (CP-Pa) has emerged as a significant clinical and public health concern due to its ability to limit treatment options with last-resort antimicrobials. This study aims to characterise novel class 1 integron (Int1) structures containing bla_VIM-2 and bla_IMP-1 in high-risk CP-Pa sequence type (ST) 235 and ST654 strains from dogs and cats and illustrate the genetic relatedness between CP-Pa strains from animal and human origins.

Methods and Results

Of the four CP-Pa strains, whole-genome sequencing and analysis revealed that three strains belonged to ST235/O11/exoU+/exoS-, with two strains harbouring bla_VIM-2, and one strain harbouring bla_IMP-1. The remaining strain was characterised as ST654/O4/exoU-/exoS+ and harboured bla_VIM-2. Core-genome single nucleotide polymorphism-based phylogeny illustrated genetic relationships between animal and human high-risk CP-Pa ST235/O11 and ST654/O4 strains within the same STs. Three novel Int1 gene cassette arrays were identified in the canine and feline CP-Pa strains in this study. The novel ~6.2-kb bla_VIM-2-containing Int1[Pae-CUVET21-397] and Int1[Pae-CUVET23-830] (intI1-aadB-bla_VIM-2-aadB-cmlA6-qacE∆1-folP) formed a complex Int1 located in an integrative and conjugative element of two feline CP-Pa ST235 strains. The canine CP-Pa ST235 strain CUVET20-956 contained a novel ~5.8-kb bla_IMP-1-containing Int1[Pae-CUVET20-956] (intI1-bla_IMP-1-aacA4-aacA4-IS1595-qacE∆1-sul1). The CP-Pa ST654 strain CUVET18-860 contained In1206 encoding bla_VIM-2 and a novel ~5.9-kb Int1[Pae-CUVET18-860] (∆intI1-bla_VEB-1-aadB-qnrVC1-aacA4-bla_OXA-10-aadA1-dfrA14) encoding multidrug resistance (MDR). Additionally, In51-containing Tn6162 inserted in genomic island 1 was identified in all CP-Pa ST235 strains.

Conclusions

The novel Int1s encoding metallo-β-lactamases and MDR in canine and feline CP-Pa play a crucial role in the development of resistance to multiple antimicrobials and last-resort carbapenems in P. aeruginosa ST235 and ST654 strains of veterinary and public health importance, posing possible zoonotic and anthroponotic transmission of the high-risk CP-Pa clones between companion animals and humans.

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来自伴侣动物的产金属β-内酰胺酶高风险铜绿假单胞菌ST235和ST654的新型1类整合子结构

产生碳青霉烯酶的铜绿假单胞菌（CP-Pa）已经成为一个重要的临床和公共卫生问题，因为它能够限制最后的抗微生物药物治疗选择。本研究旨在分析狗和猫的高风险CP-Pa序列型（ST） 235和ST654株中含有blaVIM-2和blaIMP-1的新型1类整合子（Int1）结构，并阐明动物和人类来源的CP-Pa株之间的遗传相关性。方法与结果：对4株CP-Pa进行全基因组测序和分析，发现3株属于ST235/O11/exoU+/exoS-， 2株为blaVIM-2, 1株为blaIMP-1。剩余菌株的特征为ST654/O4/exoU-/exoS+，携带blaVIM-2。基于核心基因组单核苷酸多态性的系统发育揭示了同一STs内动物和人类高风险CP-Pa ST235/O11和ST654/O4菌株之间的遗传关系。本研究在犬和猫CP-Pa株中鉴定出三个新的Int1基因盒阵列。新发现的含有Int1[Pae-CUVET21-397]和Int1[Pae-CUVET23-830] （intI1-aadB-blaVIM-2-aadB-cmlA6-qacE∆1-folP）的约6.2 kb blavim -2复合物Int1位于两种猫CP-Pa ST235菌株的整合共轭元件中。犬CP-Pa ST235菌株CUVET20-956含有一种新的~5.8 kb的含有blaimp -1的Int1[Pae-CUVET20-956] （intI1-blaIMP-1-aacA4-aacA4-IS1595-qacE∆1-sul1）。CP-Pa ST654菌株CUVET18-860含有编码blaVIM-2的In1206和编码多药耐药（MDR）的新inti1 [Pae-CUVET18-860]（∆intI1-blaVEB-1-aadB-qnrVC1-aacA4-blaOXA-10-aadA1-dfrA14）。此外，在所有CP-Pa ST235菌株中均鉴定到插入基因组岛1的含in51的Tn6162。结论：新型Int1s编码金属β-内酰胺酶和犬猫CP-Pa的耐多药在铜绿假单胞菌ST235和ST654菌株对多种抗菌素和最后的碳青霉烯类药物产生耐药性的过程中发挥了关键作用，对兽医和公共卫生具有重要意义，可能导致高风险CP-Pa克隆在伴侣动物和人类之间的人畜共患和人传。

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来源期刊

Zoonoses and Public Health 医学-传染病学

CiteScore

5.30

自引率

4.20%

发文量

115

审稿时长

6-12 weeks

期刊介绍： Zoonoses and Public Health brings together veterinary and human health researchers and policy-makers by providing a venue for publishing integrated and global approaches to zoonoses and public health. The Editors will consider papers that focus on timely collaborative and multi-disciplinary research in zoonoses and public health. This journal provides rapid publication of original papers, reviews, and potential discussion papers embracing this collaborative spirit. Papers should advance the scientific knowledge of the sources, transmission, prevention and control of zoonoses and be authored by scientists with expertise in areas such as microbiology, virology, parasitology and epidemiology. Articles that incorporate recent data into new methods, applications, or approaches (e.g. statistical modeling) which enhance public health are strongly encouraged.