Department of Animal Health and Food Safety, School of Global Health, Chinese Center for Tropical Diseases Research, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
One Health Center, Shanghai Jiao Tong University-The University of Edinburgh, Shanghai, 200025, China.
Infect Dis Poverty. 2022 Sep 16;11(1):98. doi: 10.1186/s40249-022-01025-4.
Antimicrobial resistance (AMR) is one of the greatest threats to animal and public health. Here, we conducted a dynamic surveillance of Escherichia coli on Chongming Island in Shanghai during 2009-2021 to identify the characteristics and trends of Chongming's AMR pandemic.
Rectal (cloaca) swabs from four poultry and nine swine farms (Chongming Island, 2009-2021) were collected for E. coli strains acquisition. The micro-broth dilution method was used to test antimicrobial susceptibility of E. coli isolates against 10 antimicrobial classes including 15 antimicrobials. Utilizing generalized linear mixed models (GLMMs) and co-occurrence analyses, we further explored the multiple-drug-resistance (MDR) combinations and dynamic patterns of E. coli over 10 years in two food animals.
Total of 863 MDR isolates were found among 945 collected E. coli isolates, 337 from poultry and 608 from swine. Both isolates exhibited high resistant rates (> 70%) to tetracyclines, phenicols, sulfonamides, penicillins, and aminoglycosides (only in swine). The resistant rates of swine isolates to penicillins, aminoglycosides, tetracyclines, phenicols, and polymyxins were significantly higher than those of poultry isolates, whereas resistance to fluoroquinolones was reversed. Resistance to polymyxins decreased similarly in swine (42.4% in 2009 to 0.0% in 2021) and poultry isolates (from 16.5% to 0.0%). However, resistance to other seven antimicrobial classes (excluding carbapenems and penicillins) declined dramatically in swine isolates, particularly fluoroquinolones (from 80.5% to 14.4%), and tendencies of resistance to the seven classes showed markedly divergent patterns in poultry isolates. Using Poisson GLMMs, the AMR carriage since 2016 was significantly lower than that of 2009 (odds ratio < 1), indicating a decline in the risk of MDR emergence. Furthermore, despite the highly diverse MDR profiles, co-occurrence analysis identified two prominent MDR clusters of penicillins-phenicols-fluoroquinolones in poultry and aminoglycosides-tetracyclines-sulfonamides-phenicols in swine.
Our study uncovered vastly distinct AMR patterns and dynamic tendencies of poultry and swine E. coli isolates from Chongming. Meanwhile, Chongming's AMR status has ameliorated, as indicated by the decline in antimicrobials prevalence (particularly in swine), lower likelihood of MDR emergence and low carbapenem-, cephalosporin-, and polymyxin resistance. Importantly, this surveillance results are the vital basis for future policy development in Chongming and Shanghai.
抗菌药物耐药性（AMR）是对动物和公共卫生的最大威胁之一。在这里，我们对 2009-2021 年期间上海崇明岛的大肠杆菌进行了动态监测，以确定崇明岛 AMR 流行的特征和趋势。
从 2009-2021 年崇明岛的四个家禽和九个养猪场（崇明岛）采集直肠（泄殖腔）拭子，以获取大肠杆菌菌株。采用微量肉汤稀释法检测大肠杆菌分离株对包括 15 种抗菌药物在内的 10 种抗菌药物类别的抗菌药物敏感性。利用广义线性混合模型（GLMM）和共现分析，我们进一步研究了两种食用动物中 10 年来大肠杆菌的多重耐药（MDR）组合和动态模式。
在 945 株采集的大肠杆菌分离株中，共发现 863 株多药耐药株，其中 337 株来自家禽，608 株来自猪。两种分离株对四环素类、酚类、磺胺类、青霉素类和氨基糖苷类（仅在猪中）的耐药率均高于 70%。猪分离株对青霉素类、氨基糖苷类、四环素类、酚类和多黏菌素的耐药率明显高于禽分离株，而对氟喹诺酮类的耐药率则相反。猪（2009 年为 42.4%，2021 年为 0.0%）和禽（从 16.5%降至 0.0%）分离株对多黏菌素的耐药性也显著下降。然而，猪分离株中其他七种抗菌药物类别的耐药性（不包括碳青霉烯类和青霉素类）急剧下降，尤其是氟喹诺酮类（从 80.5%降至 14.4%），禽分离株中这七种药物类别的耐药趋势明显不同。使用泊松广义线性混合模型，自 2016 年以来的 AMR 携带率明显低于 2009 年（比值比<1），表明 MDR 出现的风险降低。此外，尽管多药耐药模式高度多样，但共现分析确定了家禽中以青霉素-酚类-氟喹诺酮类为特征的两个主要多药耐药群和猪中以氨基糖苷类-四环素类-磺胺类-酚类为特征的两个主要多药耐药群。
本研究揭示了崇明岛禽、猪大肠杆菌分离株的 AMR 模式和动态趋势存在显著差异。同时，崇明岛的 AMR 状况有所改善，这表明抗菌药物的流行率（特别是在猪中）下降，MDR 出现的可能性降低，碳青霉烯类、头孢菌素类和多黏菌素类的耐药率较低。重要的是，这项监测结果是未来崇明岛和上海市制定政策的重要基础。
