Dissemination of carbapenemase-producing Enterobacterales through wastewater and gulls at a wastewater treatment plant in Sweden

Hanna Woksepp; Klara Karlsson; Stefan Börjesson; Oskar Karlsson Lindsjö; Robert Söderlund; Jonas Bonnedahl

doi:10.1016/j.scitotenv.2023.163997

Dissemination of carbapenemase-producing Enterobacterales through wastewater and gulls at a wastewater treatment plant in Sweden

Sci Total Environ. 2023 Aug 15:886:163997. doi: 10.1016/j.scitotenv.2023.163997. Epub 2023 May 9.

Authors

Hanna Woksepp¹, Klara Karlsson², Stefan Börjesson³, Oskar Karlsson Lindsjö⁴, Robert Söderlund⁵, Jonas Bonnedahl⁶

Affiliations

¹ Department of Research, Region Kalmar County, Kalmar 391 85, Sweden; Department of Chemistry and Biomedical Sciences, Linnaeus University, Kalmar 392 31, Sweden. Electronic address: hanna.woksepp@regionkalmar.se.
² Faculty of Medicine and Health Sciences, Linköping University, Linköping 581 83, Sweden.
³ Department of Microbiology, Public Health Agency of Sweden, Solna 171 82, Sweden; Department of Laboratory Medicine, Karolinska Institute, Stockholm 171 77, Sweden; School of Health Sciences, Örebro University, Örebro 701 82, Sweden.
⁴ Department of Microbiology, Public Health Agency of Sweden, 17182 Solna, Sweden.
⁵ Department of Microbiology, Swedish National Veterinary Institute, Uppsala 751 89, Sweden.
⁶ Department of Biomedical and Clinical Sciences, Linköping University, Linköping 581 83, Sweden; Department of Infectious Diseases, Region Kalmar County, Kalmar 391 85, Sweden.

PMID: 37164093
DOI: 10.1016/j.scitotenv.2023.163997

Abstract

Here we report the detection of carbapenemase-producing Enterobacterales (CPE) isolated from Swedish wastewater and gull faeces. CPE have not been detected in samples from animals in Sweden preceding this report. Sampling of wastewater treatment plant (WWTP) inlet and outlet, sedimentation basins, surface seawater from key aquatic bird habitats and freshly deposited gull faeces was done on six separate occasions during May to September 2021. Following broth enrichment, selective screening of putative CPE was performed on mSuperCarba™ (CHROMagar). Species identification was done with MALDI-TOF. Antimicrobial susceptibility testing was performed according to EUCAST. In total, seventeen CPE were verified by genome sequencing carrying bla_GES-5, bla_IMI-3, bla_OXA-181 or bla_OXA-244. The bla_GES-5 was carried on IncP plasmids in four different species; Escherichia coli ST10 isolated from WWTP outlet, Raoultella ornithinolytica isolated from WWTP inlet, outlet and sedimentation basins as well as gull faeces collected at the WWTP and Klebsiella spp. isolates from WWTP inlet and outlet. The genetic environment surrounding bla_GES-5 was similar in two Citrobacter freundii causing human infections. The bla_IMI-3 was carried on IncFII(Yp) plasmids in four Enterobacter ludwigii, isolated from WWTP outlet and gull faeces collected at a recreational city park 2 km from the WWTP. The bla_OXA-181 was located on a COLKP3 plasmid found in an E. coli, while bla_OXA-244 was chromosomally located in an E. coli ST10, both isolated from WWTP inlet. Phylogenetic analysis of R. ornithinolytica and E. ludwigii isolates indicate that the gulls carried strains related to those identified in the WWTP samples. The results thus add to the increasing evidence of WWTPs as anthropogenic reservoirs for mobile genetic elements with antibiotic-resistance functionality. Such environments could profoundly impact the dissemination and spread of such genetic elements via for example aquatic birds, thereby warranting further study and surveillance.

Keywords: Antibiotic resistant bacteria; Aquatic birds; Carbapenemases; Environmental hotspots; Mobile genetic elements; Wastewater.

MeSH terms

Animals
Anti-Bacterial Agents / pharmacology
Bacterial Proteins / genetics
Charadriiformes* / genetics
Escherichia coli / genetics
Humans
Microbial Sensitivity Tests
Phylogeny
Plasmids
Sweden
Wastewater
Water Purification*
beta-Lactamases / genetics

Substances

carbapenemase
Wastewater
Bacterial Proteins
beta-Lactamases
Anti-Bacterial Agents