Department of Population Health and Pathobiology, College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina, United States of America.
Department of Agricultural and Human Sciences, College of Agriculture and Life Sciences, North Carolina State University, Raleigh, North Carolina, United States of America.
PLoS One. 2024 Jan 5;19(1):e0294099. doi: 10.1371/journal.pone.0294099. eCollection 2024.
Escherichia coli is commonly used as an indicator for antimicrobial resistance (AMR) in food, animal, environment, and human surveillance systems. Our study aimed to characterize AMR in E. coli isolated from retail meat purchased from grocery stores in North Carolina, USA as part of the National Antimicrobial Resistance Monitoring System (NARMS).
Retail chicken (breast, n = 96; giblets, n = 24), turkey (n = 96), and pork (n = 96) products were purchased monthly from different counties in North Carolina during 2022. Label claims on packages regarding antibiotic use were recorded at collection. E. coli was isolated from meat samples using culture-based methods and isolates were characterized for antimicrobial resistance using whole genome sequencing. Multi-locus sequence typing, phylogroups, and a single nucleotide polymorphism (SNP)-based maximum-likelihood phylogenic tree was generated. Data were analyzed statistically to determine differences between antibiotic use claims and meat type.
Of 312 retail meat samples, 138 (44.2%) were positive for E. coli, with turkey (78/138; 56.5%) demonstrating the highest prevalence. Prevalence was lower in chicken (41/138; 29.7%) and pork (19/138;13.8%). Quality sequence data was available from 84.8% (117/138) of the E. coli isolates, which included 72 (61.5%) from turkey, 27 (23.1%) from chicken breast, and 18 (15.4%) from pork. Genes associated with AMR were detected in 77.8% (91/117) of the isolates and 35.9% (42/117) were defined as multidrug resistant (MDR: being resistant to ≥3 distinct classes of antimicrobials). Commonly observed AMR genes included tetB (35%), tetA (24.8%), aph(3'')-lb (24.8%), and blaTEM-1 (20.5%), the majority of which originated from turkey isolates. Antibiotics use claims had no statistical effect on MDR E. coli isolates from the different meat types (X2 = 2.21, p = 0.33). MDR was observed in isolates from meat products with labels indicating "no claims" (n = 29; 69%), "no antibiotics ever" (n = 9; 21.4%), and "organic" (n = 4; 9.5%). Thirty-four different replicon types were observed. AMR genes were carried on plasmids in 17 E. coli isolates, of which 15 (88.2%) were from turkey and two (11.8%) from chicken. Known sequence types (STs) were described for 81 E. coli isolates, with ST117 (8.5%), ST297 (5.1%), and ST58 (3.4%) being the most prevalent across retail meat types. The most prevalent phylogroups were B1 (29.1%) and A (28.2%). Five clonal patterns were detected among isolates.
E. coli prevalence and the presence of AMR and MDR were highest in turkey retail meat. The lack of an association between MDR E. coli in retail meat and antibiotic use claim, including those with no indication of antimicrobial use, suggests that additional research is required to understand the origin of resistance. The presence of ST117, an emerging human pathogen, warrants further surveillance. The isolates were distinctly diverse suggesting an instability in population dynamics.
大肠杆菌通常被用作食品、动物、环境和人类监测系统中抗微生物药物耐药性（AMR）的指标。我们的研究旨在描述从美国北卡罗来纳州杂货店购买的零售肉类中分离出的大肠杆菌的 AMR，这是国家抗微生物药物耐药性监测系统（NARMS）的一部分。
2022 年期间，从北卡罗来纳州不同县的杂货店每月购买零售鸡肉（鸡胸，n = 96；内脏，n = 24）、火鸡（n = 96）和猪肉（n = 96）产品。在收集时记录包装上关于抗生素使用的标签声明。使用基于培养的方法从肉类样本中分离大肠杆菌，并用全基因组测序对分离株的抗微生物药物耐药性进行特征描述。生成多位点序列分型、 phylogroups 和基于单核苷酸多态性（SNP）的最大似然系统发育树。使用统计方法分析数据，以确定抗生素使用声明和肉类类型之间的差异。
在 312 份零售肉类样本中，138 份（44.2%）为大肠杆菌阳性，火鸡（78/138；56.5%）的阳性率最高。鸡肉（41/138；29.7%）和猪肉（19/138；13.8%）的阳性率较低。84.8%（117/138）的大肠杆菌分离株可获得高质量的序列数据，其中 72 株（61.5%）来自火鸡，27 株（23.1%）来自鸡胸，18 株（15.4%）来自猪肉。在 77.8%（91/117）的分离株中检测到与 AMR 相关的基因，其中 35.9%（42/117）被定义为多药耐药（MDR：对≥3 种不同类别的抗菌药物耐药）。常见的观察到的 AMR 基因包括 tetB（35%）、tetA（24.8%）、aph(3'')-lb（24.8%）和 blaTEM-1（20.5%），其中大多数来自火鸡分离株。抗生素使用声明对来自不同肉类类型的 MDR 大肠杆菌分离株没有统计学影响（X2 = 2.21，p = 0.33）。在标签显示“无声明”（n = 29；69%）、“从未使用过抗生素”（n = 9；21.4%）和“有机”（n = 4；9.5%）的肉产品中观察到 MDR。观察到 34 种不同的复制子类型。在 17 株大肠杆菌分离株中，AMR 基因携带在质粒上，其中 15 株（88.2%）来自火鸡，2 株（11.8%）来自鸡肉。对 81 株大肠杆菌分离株进行了描述已知序列类型（STs），其中 ST117（8.5%）、ST297（5.1%）和 ST58（3.4%）在零售肉类类型中最为普遍。最常见的 phylogroups 是 B1（29.1%）和 A（28.2%）。在分离株中检测到 5 种克隆模式。
火鸡零售肉类中的大肠杆菌阳性率和 AMR 及 MDR 的存在率最高。零售肉类中 MDR 大肠杆菌与抗生素使用声明之间没有关联，包括那些没有表明使用抗菌药物的声明，这表明需要进一步研究以了解耐药性的来源。ST117 的存在，一种新兴的人类病原体，值得进一步监测。分离株明显多样化，表明种群动态不稳定。
