Knysz Przemysław, Szkucik Krzysztof, Gondek Michał
Department of Food Hygiene of Animal Origin, Faculty of Veterinary Medicine, University of Life Sciences in Lublin, Akademicka 12, Lublin, 20-033, Poland.
BMC Vet Res. 2025 Jun 4;21(1):400. doi: 10.1186/s12917-025-04849-y.
Numerous studies indicate that multidrug-resistant Enterococcus bacteria are widely present on the carcasses of various food-producing animal species as well as in facilities used for their production. However, in the global literature, there is no information available regarding the prevalence, species composition or antibiotic resistance of enterococci contaminating rabbit carcasses. Therefore, the aim of this study was to determine the prevalence of Enterococcus bacteria on the surface of carcasses of rabbits slaughtered in an EU-approved abattoir with particular emphasis on two species, i.e., Enterococcus faecalis (E. faecalis) and Enterococcus faecium (E. faecium). In addition, the phenotypic and genotypic resistance to antibiotics of rabbit-origin E. faecalis isolates and the relatedness of multi-drug resistance strains has been evaluated.
The study revealed that 425 out of 496 examined rabbit carcasses were contaminated with Enterococcus spp., with a prevalence of 85.69% (95% CI: 82.60-88.77%). E. faecalis was confirmed on the surface of 237 carcasses, which constituted 55.8% of the Enterococcus-positive swabs and 47.8% of all carcasses examined. E. faecium was not detected on the surface of any of the rabbit carcasses tested. Phenotypically, 97.5% of isolates were classified as resistant to tetracycline, 92.4% to erythromycin, 65% to kanamycin, 54% to streptomycin, 40.4% to ciprofloxacin, 30% to enrofloxacin, and 0.4% to penicillin and ampicillin. Moreover, 66.40% of E. faecalis isolates showed multidrug resistance to at least three classes of antibiotics. The presence of genes determining the resistance to tetracycline (tetM and tetL), erythromycin (ermB), aminoglycosides (aac(6')-Ie-aph(2")-Ia), and streptomycin (ant(6)-Ia), was consistent with the phenotypic resistance pattern observed in E. faecalis isolates. Using ADSRRS fingerprinting analysis, four main clusters were visualized, with almost every branch containing multi-drug resistant isolates from rabbits bred on farms in different locations.
The high prevalence of enterococci on rabbit carcass surfaces indicates poor hygiene during the production process at rabbit abattoirs. Compared to E. faecium, E. faecalis appears better adapted to persist on the surface of rabbit carcasses and/or meat cuts in the slaughterhouse environment. This may be attributed to its stronger biofilm-forming ability, as E. faecalis was the only species detected in all Enterococcus-positive samples tested. Rabbit carcasses are also an important vector of multidrug-resistant E. faecalis. The high genetic similarity of multidrug-resistant E. faecalis isolates from rabbit carcasses raised on different farms suggests a common source of these bacteria or cross-contamination at slaughter. Our results supported E. faecalis as an indicator bacterium for antibiotic resistance under Commission Implementing Decision (EU) 2020/1729 and highlighted the need to extend monitoring to rabbit meat production at the national level.
大量研究表明，耐多药肠球菌广泛存在于各种食用动物的胴体以及其生产设施中。然而，在全球文献中，尚无关于污染兔胴体的肠球菌的流行情况、种类组成或抗生素耐药性的信息。因此，本研究的目的是确定在欧盟批准的屠宰场宰杀的兔胴体表面肠球菌的流行情况，特别关注粪肠球菌（E. faecalis）和屎肠球菌（E. faecium）这两个菌种。此外，还评估了源自兔的粪肠球菌分离株的表型和基因型抗生素耐药性以及多重耐药菌株的相关性。
研究表明，在496份检测的兔胴体中，有425份被肠球菌污染，流行率为85.69%（95%置信区间：82.60 - 88.77%）。在237份胴体表面确认有粪肠球菌，占肠球菌阳性拭子的55.8%，占所有检测胴体的47.8%。在所检测的任何兔胴体表面均未检测到屎肠球菌。表型上，97.5%的分离株被归类为对四环素耐药，92.4%对红霉素耐药，65%对卡那霉素耐药，54%对链霉素耐药，40.4%对环丙沙星耐药，30%对恩诺沙星耐药，0.4%对青霉素和氨苄西林耐药。此外，66.40%的粪肠球菌分离株对至少三类抗生素表现出多重耐药。决定对四环素（tetM和tetL）、红霉素（ermB）、氨基糖苷类（aac(6')-Ie-aph(2")-Ia）和链霉素（ant(6)-Ia）耐药的基因的存在与在粪肠球菌分离株中观察到的表型耐药模式一致。使用ADSRRS指纹分析，观察到四个主要聚类，几乎每个分支都包含来自不同地点农场饲养的兔的多重耐药分离株。
兔胴体表面肠球菌的高流行率表明兔屠宰场生产过程中的卫生状况不佳。与屎肠球菌相比，粪肠球菌似乎更能适应在屠宰场环境中在兔胴体和/或肉块表面持续存在。这可能归因于其更强的生物膜形成能力，因为粪肠球菌是所有检测的肠球菌阳性样本中唯一检测到的菌种。兔胴体也是耐多药粪肠球菌的重要载体。来自不同农场饲养的兔胴体的耐多药粪肠球菌分离株的高遗传相似性表明这些细菌有共同来源或在屠宰时发生交叉污染。我们的结果支持粪肠球菌作为欧盟委员会实施决定（EU）2020/1729下抗生素耐药性的指示菌，并强调有必要在国家层面将监测扩展到兔肉生产。
