Antimicrobial resistance in Escherichia coli and Staphylococcus aureus at human-animal interfaces on Chongming Island, Shanghai: A One Health perspective

Abstract

Antimicrobial resistance (AMR) is a significant concern within the One Health framework due to its ability to spread across multiple interfaces. Phenotypic data remains the primary type for AMR surveillance, but exploring association across multiple interfaces poses certain challenges. In this study, AMR phenotypic data of clinical and food animal E. coli and S. aureus from Chongming Island over the past five years were analyzed to determine key characteristics of AMR and explore its association at the human-animal interface. The clinical E. coli isolates showed significant resistance to penicillins (83.92 %), cephems (63.05 %), fluoroquinolones (62.21 %), and tetracyclines (57.77 %), while S. aureus exhibited high resistance to penicillinase-labile penicillins (90.89 %), macrolides (51.51 %), penicillinase-stable penicillins (43.96 %), and lincosamides (43.55 %). Extended-spectrum β-lactamase (ESBL)-producing E. coli isolates accounted for 53.26 % (1398/2526), while methicillin-resistant Staphylococcus aureus (MRSA) prevalence was 43.81 % (435/993). Notably, there has been an increase in the proportion of E. coli isolates resistant to 8 to 12 antimicrobial classes, and in the proportion of S. aureus isolates resistant to 5 to 9 classes. Certain multi-drug resistance (MDR) phenotypes were first identified in food animal isolates and later emerged in clinical settings. Meanwhile, several MDR phenotypes were shared between the two interfaces, with 44 identified in E. coli and 12 in S. aureus. Further co-occurrence analysis in E. coli and S. aureus identified several co-occurrence phenotypic pairs or clusters, potentially mediated by a single plasmid or multiple plasmids within a bacterium, indicating potential associations at the human-animal interface. To summarize, a heightened prevalence of MDR in clinical E. coli and S. aureus has been observed, with some MDR profiles appearing in food animals before emerging in clinical settings. The co-occurrence of phenotypic pairs or clusters underscores the potential for AMR association and transmission between humans and food animals. Within the One Health framework, integrating genomic data into AMR monitoring is a crucial next step.

Keywords: Clinical isolates; Escherichia coli; Food animals; Multidrug resistance; Staphylococcus aureus.

Fig. 1

Bar charts showing resistance rates of clinical E. coli (A, C) and S. aureus (B, D) isolates to all antimicrobial classes and antimicrobial agents. In antimicrobial susceptibility test (AST) of clinical E.coli, classes of β-Lactam combination agents, cephems, carbapenems, aminoglycosides, tetracyclines, and fluoroquinolones have two or more agents (C). In AST of S. aureus, classe of fluoroquinolones and tetracyclines all have three agents (D). β-Lactam CA β-Lactam combination agents, Folate PA Folate pathway antagomists, SAM Ampicillin/Dsulbactam, CSL Cefoperazone/Sulbactam, TZP Piperacillin/ Tazobactam, AMC Amoxicillin/ Clavulanic acid, CZO Cefazolin, FEP Cefepime, CTX Cefotaxime, CAZ Ceftazidime, CXM Cefuroxime, FOX Cefoxitin, CRO Ceftriaxone, MEM Meropenem, IPM Imipenem, ETP Ertapenem, AMK Amikacin, GEN Gentamicin, TOB Tobramycin, TCY Tetracycline, TGC Tigecycline, LVX Levofloxacin, CIP Ciprofloxacin, MFX Moxifloxacin; PL Penicillins Penicillinase-labicle Penicillins, PS Penicillins Penicillinase-stable Penicillins, TCY Tetracycline, MNO Minocycline, TGC Tigecycline, LVX Levofloxacin, CIP Ciprofloxacin, MFX Moxifloxacin.

Fig. 2

Trends of the resistance rates of E. coli (A) and S. aureus (B) isolates to various antimicrobial classes from 2018 to 2022. Only complete data from these 5 years will be displayed. The trends of resistance rates were fitted by linear models in R. The gray shadow represents the 95 % confidence interval. β-Lactam CA β-Lactam combination agents; Folate PA Folate pathway antagonists; PL Penicillins Penicillinase-labile Penicillins; PS Penicillins Penicillinase-stable Penicillins.

Fig. 3

The prevalence and trends of clinical ESBL-positive E. coli and MRSA from 2018 to 2022. (A) the prevalence of ESBL-positive E. coli; (B) the prevalence trends of ESBL-positive E. coli from 2018 to 2022. The trends of resistance rates were fitted by linear models in R. The gray shadow represents the 95 % confidence interval; (C) the prevalence of MRSA; (D) the prevalence trends of ESBL-E. coli from 2018 to 2022. The trends of resistance rates were fitted by linear models in R. The gray shadow represents the 95 % confidence interval.

Fig. 4

The status and trends of MDR E. coli (A-C) and S. aureus (D—F) isolates from 2018 to 2022. (A, D) Number of isolates in each antimicrobial class; (B, E) The percentage of isolates in each antimicrobial class annually; (C, F) The proportion trends of MDR isolates. The trends of resistance rates were fitted by linear models in R. The gray shadow represents the 95 % confidence interval.

Fig. 5

The status of AMR profiles in E. coli and S. aureus at the clinical interfaces. The quantity of E. coli (A) and S. aureus (C) AMR profiles categorized by antibiogram length; the quantity of E. coli (B) and S. aureus (D) AMR profiles categorized by years and antibiogram length.

Fig. 6

The association of E. coli (A, C, E) and S. aureus (B, D, F) between the clinical and food animal interfaces. A-B The shared profiles between the two interfaces of E. coli (A) and S. aureus (B). Pen Penicillins, βLac β-Lactam combination agents, Cep Cephems, Ami Aminoglycosides, Tet Tetracyclines, Flu Fluoroquinolones, Fpa Folate pathway antagonists, Fos Fosfomycins, Mon Monobactams, Phe PheniPols, Nit Nitrofuran, PLPen Penicillinase-labile Penicillins, PSPen Penicillinase-stable Penicillins, Gly Glycopeptides, Mac Macrolides,Lin Lincosamides,Ans Ansamycins, Oxa Oxazolidinines. C—D The correlation of resistance rate of every antimicrobial class between the clinical E. coli, S. aureus, and that of food animals. The sign (a) indicates the classes used in food animals. βLactam CA β-Lactam combination agents; Folate PA Folate pathway antagonists; PL Penicillins Penicillinase-labile Penicillins; PS Penicillins Penicillinase-stable Penicillins. E-F Co-occurrence analysis of antimicrobial class in clinical E. coli and S. aureus. The numbers within the boxes reflect values for the correction coefficient (r). The legends beneath the two heat maps indicate whether the link between resistant phenotypes is positive (closer to 1; darker blue) or negative (less than 1; lighter blue) (closer to −1, dark red). *P < 0.05, **P < 0.01. βLactam CA β-Lactam combination agents; Folate PA Folate pathway antagonists; PL Penicillins Penicillinase-labile Penicillins; PS Penicillins Penicillinase-stable Penicillins. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)