Department of Veterinary Preventive Medicine, The Ohio State University, Columbus, Ohio, USA.
Appl Environ Microbiol. 2023 May 31;89(5):e0025723. doi: 10.1128/aem.00257-23. Epub 2023 Apr 17.
Environmental surfaces can serve as reservoirs for pathogens and antimicrobial-resistant (AMR) bacteria in healthcare settings. Although active surveillance programs are used in veterinary and human healthcare, unconventional settings like zoological facilities are often overlooked, even though antimicrobials are used to maintain the health of their animal collections. Here, we used electrostatic cloths to conduct active environmental surveillance over a 2-year period at two zoological institutions to determine contamination prevalence of human-only and mixed animal-human touch environments with AMR bacteria. We recovered isolates that expressed quinolone resistance, an AmpC-like phenotype, and an extended-spectrum β-lactamase phenotype from 144 (39%), 141 (38.2%), and 72 (19.5%) of the environmental samples, respectively. The zoological institutions, areas and exhibits within the zoological facility, and sampling surface type affected the odds of recovering AMR bacteria from the environment. Three carbapenemase-producing Enterobacter cloacae complex ST171 isolates recovered from one zoological facility harbored an IncH12 plasmid with a Tn-KPC-4 transposon conferring multidrug resistance. One isolate maintained three tandem repeats of a Tn-KPC-4 element on an IncHI2 plasmid, although this isolate was susceptible to the four carbapenem drugs tested. These three isolates and their IncH12 plasmids shared significant genomic similarity with two E. cloacae complex isolates recovered from canine patients at a regional veterinary hospital during year 2 of this study. Our results indicated that surface environments at zoological institutions can serve as reservoirs for AMR bacteria and their genes and have implications for animal and public health. Environmental surfaces can be a source of antimicrobial-resistant (AMR) bacteria that pose a risk to human and animal health. Zoological institutions are unique environments where exotic animals, staff, and visitors intermingle and antimicrobials are used to maintain animal health. However, zoological environments are often overlooked as reservoirs of AMR bacteria. Here, we show that zoological environments can serve as reservoirs of fluoroquinolone-resistant and extended-spectrum cephalosporin-resistant bacteria. In addition, we isolated three carbapenemase-producing Enterobacter cloacae complex strains carrying , including one with a unique, tandem triplicate of the Tn-KPC-4 element. Comparative whole genomics of these isolates with two E. cloacae complex isolates from patients at a regional veterinary hospital highlighted the possibility of local KPC-4 spread between animal environments. Our results suggest that environments at zoological institutions serve as reservoirs for AMR bacteria and pose a hypothetical One Health risk to the public, staff, and the wild animal populations in captivity.
环境表面可以作为病原体和抗菌药物耐药(AMR)细菌在医疗保健环境中的储库。尽管兽医和人类医疗保健中使用了主动监测计划,但像动物园设施这样的非常规环境往往被忽视,尽管抗生素被用于维持其动物收藏的健康。在这里,我们使用静电布在两年内对两个动物园机构进行了主动环境监测,以确定 AMR 细菌在人与动物混合触摸环境和仅人类触摸环境中的污染流行情况。我们从 144 个(39%)、141 个(38.2%)和 72 个(19.5%)环境样本中分别回收了表达喹诺酮耐药性、AmpC 样表型和扩展谱β-内酰胺酶表型的 分离株。动物园机构、动物园设施内的区域和展览以及采样表面类型影响从环境中回收 AMR 细菌的可能性。从一个动物园设施中回收的三株产碳青霉烯酶阴沟肠杆菌复合 ST171 分离株携带一个 IncH12 质粒,其中包含一个 Tn-KPC-4 转座子,赋予多药耐药性。一个分离株在一个 IncHI2 质粒上维持三个串联的 Tn-KPC-4 元件,尽管该分离株对测试的四种碳青霉烯类药物敏感。这三个分离株及其 IncH12 质粒与本研究第二年在一家地区兽医医院从犬科患者中回收的两个阴沟肠杆菌复合菌株具有显著的基因组相似性。我们的结果表明,动物园机构的表面环境可以作为 AMR 细菌及其基因的储库,这对动物和公共卫生具有重要意义。 环境表面可能是对人类和动物健康构成威胁的抗菌药物耐药(AMR)细菌的来源。动物园机构是一个独特的环境,其中异国情调的动物、工作人员和访客相互混合,并且使用抗生素来维持动物的健康。然而,动物园环境往往被忽视为 AMR 细菌的储库。在这里,我们表明,动物园环境可以作为氟喹诺酮类和扩展谱头孢菌素类耐药细菌的储库。此外,我们分离了三株产碳青霉烯酶阴沟肠杆菌复合菌株,其中包括一株携带独特的 Tn-KPC-4 元件串联三重复的菌株。对这些分离株与来自地区兽医医院患者的两株阴沟肠杆菌复合菌株的全基因组比较突出了动物环境之间局部 KPC-4 传播的可能性。我们的研究结果表明,动物园机构的环境充当 AMR 细菌的储库,并对公众、工作人员和圈养野生动物种群构成假设的 One Health 风险。