Genomic characterization of third-generation cephalosporin-resistant Escherichia coli strains isolated from diseased dogs and cats: Report from Japanese Veterinary Antimicrobial Resistance Monitoring

IF 2.4 2区农林科学 Q3 MICROBIOLOGY Veterinary microbiology Pub Date : 2024-08-24 DOI:10.1016/j.vetmic.2024.110220

Yukari Hiraoka (Furuya), Hitoshi Abo, Mari Matsuda, Saki Harada, Mio Kumakawa, Takahiro Shirakawa, Manao Ozawa, Michiko Kawanishi, Hideto Sekiguchi, Yoko Shimazaki

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Abstract

This study investigates the genomic characteristics of canine and feline cefotaxime (CTX, a third-generation cephalosporin)-resistant Escherichia coli using the JVARM, Japanese Veterinary Antimicrobial Resistance Monitoring System, a nationwide monitoring.

In this study, whole-genome sequencing (WGS) was performed on 51 canine and 45 feline CTX-resistant E. coli isolates, with certain isolates subjected to pulsed-field gel electrophoresis with S1 nuclease for plasmid–chromosome separation.

The most common bla_CTX-M genes were bla_CTX-M-27 (dogs: 11/51 [21.6 %]; cat: 10/45 [22.2 %]), followed by bla_CTX-M-14 (dogs: 10/51 [19.6 %]; cats: 10/45 [22.2 %]), and bla_CTX-M-15 (dogs: 9/51 [17.6 %]; cats: 5/45 [11.1 %]). Besides β-lactamase genes, all isolates harbored mdf(A), a multidrug efflux pump, with resistance genes for aminoglycosides, sulfonamides, trimethoprims, macrolides and tetracyclines. None of the isolates had carbapenemase genes, such as bla_OXA-48, bla_NDM, and bla_IMP, whereas most of the isolates showed double mutations in gyrA and parC, which affected quinolone resistance. For the isolates separately analyzed for plasmid and chromosomal DNA via WGS, the majority of CTX-M genes were present on the plasmids. Some plasmids also harbored the same combination of resistance genes and plasmid replicon type, although they differed from isolates derived from different areas of Japan. The predominant plasmids were bla_CTX-M-_27, aadA5, aph(6)-Id, aph(3”)-Ib, sul1, sul2, tet(A), dfrA17, and mph(A) on IncF. The predominant combination of ST131, O25:H4, and B2 isolates comprised the largest cluster in the minimum spanning tree and the ST131 E. coli harboring bla_CTX-M-27 from human in Japan was closely related to these isolates.

The results indicated that CTX-resistant canine and feline E. coli harbored multiple plasmids carrying the same combination of resistance genes and emphasizes the need to prevent the spread.

Data Availability

All raw short-read sequence data have been deposited in the DNA Data Bank of Japan. (DRR Run No, DRR335726–335821).

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从患病猫狗中分离出的对第三代头孢菌素耐药的大肠埃希菌菌株的基因组特征：日本兽医抗菌药耐药性监测报告

本研究利用日本兽医抗菌药耐药性监测系统（JVARM）对犬和猫耐头孢他啶（CTX，第三代头孢菌素）大肠杆菌的基因组特征进行了调查。最常见的 blaCTX-M 基因是 blaCTX-M-27（犬：11/51 [21.最常见的 blaCTX-M 基因是 blaCTX-M-27（狗：11/51 [21.6%]；猫：10/45 [22.2%]），其次是 blaCTX-M-14（狗：10/51 [19.6%]；猫：10/45 [22.2%]）和 blaCTX-M-15（狗：9/51 [17.6%]；猫：5/45 [11.1%]）。除了β-内酰胺酶基因外，所有分离株都携带有多种药物外排泵 mdf(A)，以及对氨基糖苷类、磺胺类、三甲双胍类、大环内酯类和四环素类的耐药基因。这些分离物都没有碳青霉烯酶基因，如 blaOXA-48、blaNDM 和 blaIMP，而大多数分离物的 gyrA 和 parC 出现了双重突变，从而影响了对喹诺酮类药物的耐药性。通过 WGS 分别分析质粒和染色体 DNA 的分离物发现，大多数 CTX-M 基因存在于质粒上。尽管来自日本不同地区的分离物的抗性基因和质粒复制子类型不同，但有些质粒也含有相同的抗性基因组合和质粒复制子类型。主要的质粒是 blaCTX-M-27、adA5、aph（6）-Id、aph（3"）-Ib、sul1、sul2、tet（A）、dfrA17 和 IncF 上的 mph（A）。结果表明，耐CTX犬大肠杆菌和耐CTX猫大肠杆菌携带多个质粒，这些质粒携带相同的耐药基因组合，强调了防止传播的必要性。数据提供所有原始短读序列数据已存入日本DNA数据库。(DRR Run No, DRR335726-335821）。

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来源期刊

Veterinary microbiology 农林科学-兽医学

CiteScore

5.90

自引率

6.10%

发文量

221

审稿时长

52 days

期刊介绍： Veterinary Microbiology is concerned with microbial (bacterial, fungal, viral) diseases of domesticated vertebrate animals (livestock, companion animals, fur-bearing animals, game, poultry, fish) that supply food, other useful products or companionship. In addition, Microbial diseases of wild animals living in captivity, or as members of the feral fauna will also be considered if the infections are of interest because of their interrelation with humans (zoonoses) and/or domestic animals. Studies of antimicrobial resistance are also included, provided that the results represent a substantial advance in knowledge. Authors are strongly encouraged to read - prior to submission - the Editorials (''Scope or cope'' and ''Scope or cope II'') published previously in the journal. The Editors reserve the right to suggest submission to another journal for those papers which they feel would be more appropriate for consideration by that journal. Original research papers of high quality and novelty on aspects of control, host response, molecular biology, pathogenesis, prevention, and treatment of microbial diseases of animals are published. Papers dealing primarily with immunology, epidemiology, molecular biology and antiviral or microbial agents will only be considered if they demonstrate a clear impact on a disease. Papers focusing solely on diagnostic techniques (such as another PCR protocol or ELISA) will not be published - focus should be on a microorganism and not on a particular technique. Papers only reporting microbial sequences, transcriptomics data, or proteomics data will not be considered unless the results represent a substantial advance in knowledge. Drug trial papers will be considered if they have general application or significance. Papers on the identification of microorganisms will also be considered, but detailed taxonomic studies do not fall within the scope of the journal. Case reports will not be published, unless they have general application or contain novel aspects. Papers of geographically limited interest, which repeat what had been established elsewhere will not be considered. The readership of the journal is global.