Colonization with resistant bacteria in hospital employees: an epidemiological surveillance and typing study

Abstract

The objective of this study was to determine the prevalence, molecular epidemiology, and risk factors for gut colonization with extended-spectrum β-lactamase-producing Enterobacterales (ESBL-E), carbapenemase-producing Enterobacterales (CPE), and vancomycin-resistant enterococci (VRE) in healthcare workers (HCWs). In September/October 2022, we performed a cross-sectional study among HCW from 14 institutions in Northeastern Switzerland. HCWs reported risk factors for antimicrobial resistance (covering the last 12-24 months) and provided rectal swabs. Swabs were screened for ESBL-E, CPE, and VRE; whole-genome sequencing (WGS) was performed to assess the genetic relatedness. Logistic regression was used to identify occupational and non-occupational risk factors. Among approximately 22,500 employees, 1,209 participated (median age 46 years, 82% female). Prevalences of ESBL-E (n = 65) and CPE (n = 1) were 5.4% [95% confidence interval (CI) 4.2-6.8] and 0.1% (95% CI 0.0-0.5), respectively; no VREs were detected. In the multivariable analysis, non-European ethnicity [adjusted odds ratio (aOR) 7.0, 95% CI 1.4-27.3], travel to high-risk countries (aOR 4.9, 95% CI 2.5-9.3), systemic antibiotics (aOR 2.1, 95% CI 1.1-3.7), antibiotic eye drops (aOR 4.7, 95% CI 1.7-11.9), and monthly sushi consumption (aOR 2.4, 95% CI 1.4-4.3) were positively associated with ESBL-E colonization, whereas alcohol consumption (aOR 0.5 per glass/week, 95% CI 0.3-0.9) was negatively associated with ESBL-E colonization. Occupational factors showed no association. Among ESBL-Escherichia coli, ST131 (15 of 61, 25%) and bla_CTX-M-15 (37/61; 61%) were most common; one isolate co-harbored bla_OXA-244. WGS data did not show relevant clustering. Occupational exposure is not associated with ESBL-E colonization in HCW. Given the potential public health and antibiotic stewardship implications, the role of sushi consumption and antibiotic eye drops as risk factors should be further elucidated.

Keywords: ESBL; antibiotic resistance; colonization; epidemiology; healthcare workers; occupation; prevalence; risk factors; sushi.

Fig 1

Results of multivariable logistic regression of factors independently associated with extended-spectrum β-lactamase-producing-Enterobacterales (ESBL-E) colonization shown as forest plot, including adjusted odds ratios (ORs) and corresponding 95% confidence intervals (red, factors with significant positive association).

Fig 2

cgMLST analysis of extended-spectrum β-lactamase-producing Escherichia coli (n = 61), according to sequence type Warwick (a) and according to institution (b).

Fig 3

Maximum-likelihood phylogenetic tree of 259 Swiss E. coli ST131 isolates. In addition to 15 isolates from this study, 244 isolates from three other collections were included (annotated in the outer ring). ST131 clades A, B, C1, and C2 are labeled. Bold branch lines indicate international sublineages mentioned in the main text. The tree is based on 4,585 variable sites identified in a 3.6-Mb core genome alignment and was visualized using iTOL (17). UTI, urinary tract infection; BSI, bloodstream infection.