Tracing carriage, acquisition, and transmission of ESBL-producing Escherichia coli over two years in a tertiary care hospital
Abstract Background The impact of community carriage on the influx of extended-spectrum beta-lactamase-producing Enterobacterales (ESBL-E) into hospitals remains understudied. In this prospective 2-year single-centre study, we investigate the community ESBL-E influx and trace the colonisation, nosoc...
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BMC
2024-12-01
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| Series: | Genome Medicine |
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| Online Access: | https://doi.org/10.1186/s13073-024-01424-2 |
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| author | Minh Ngoc Nguyen Beryl Primrose Gladstone Giulia De Angelis Michael Biggel Basil Britto Xavier Christine Lammens Qiang Lin Sandra Van Puyvelde Herman Goossens Samir Kumar-Singh Youri Glupczynski Yehuda Carmeli Evelina Tacconelli Surbhi Malhotra-Kumar the SATURN WP1, 4, 5 study groups |
| author_facet | Minh Ngoc Nguyen Beryl Primrose Gladstone Giulia De Angelis Michael Biggel Basil Britto Xavier Christine Lammens Qiang Lin Sandra Van Puyvelde Herman Goossens Samir Kumar-Singh Youri Glupczynski Yehuda Carmeli Evelina Tacconelli Surbhi Malhotra-Kumar the SATURN WP1, 4, 5 study groups |
| author_sort | Minh Ngoc Nguyen |
| collection | DOAJ |
| description | Abstract Background The impact of community carriage on the influx of extended-spectrum beta-lactamase-producing Enterobacterales (ESBL-E) into hospitals remains understudied. In this prospective 2-year single-centre study, we investigate the community ESBL-E influx and trace the colonisation, nosocomial acquisition, transmission, and infection dynamics of ESBL-producing Escherichia coli (ESBL-Ec) in non-ICU wards at a tertiary care hospital. Methods This study reports primary and post hoc outcomes of the clinical trial NCT01208519 in which hospitalised patients were screened for rectal carriage of ESBL-E. ESBL-Ec isolates from ≈50% of carriers, including all patients who developed infections, were sequenced and genotyped. Endogenous infection was defined as infection by the same strain (< 10 SNPs distance) as colonizing strain. Results Of 3703 screened patients, 456 (12.3%) were ESBL-positive-at-admission (PA-ESBL). Of the 2268 ESBL-negative-at-admission (NA-ESBL) patients with follow-up samples, 240 (10.6%) acquired ESBL-E (HA-ESBL), with an incidence density rate of 7.96 cases/1000 patient-day, notably higher in patients receiving antibiotics (P < 0.001). PA- and HA-ESBL patients developed significantly more ESBL-E infections than ESBL-free patients (P < 0.001). Sequenced ESBL-Ec showed high clonal diversity dominated by the multidrug-resistant and highly virulent ST131 clade, C2/H30-Rx. Among ESBL-Ec infections, 60% (18/30) were endogenous. Direct between-patients transmission clusters (n = 21) involved 23.9% (48/201) of patients and 23.0% (84/366) of ESBL-Ec isolates. Conclusions Our data show a high prevalence of nosocomial acquisition of ESBL-E in a non-ICU setting. The study provides genomic evidence that the endogenous reservoir is the main driver of ESBL-Ec infections underscoring the need for wide implementation of antibiotic stewardship programmes to reduce antibiotic pressure. |
| format | Article |
| id | doaj-art-1d2a47b19111409d99e2793dd38d0e84 |
| institution | OA Journals |
| issn | 1756-994X |
| language | English |
| publishDate | 2024-12-01 |
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| spelling | doaj-art-1d2a47b19111409d99e2793dd38d0e842025-08-20T02:32:03ZengBMCGenome Medicine1756-994X2024-12-0116111510.1186/s13073-024-01424-2Tracing carriage, acquisition, and transmission of ESBL-producing Escherichia coli over two years in a tertiary care hospitalMinh Ngoc Nguyen0Beryl Primrose Gladstone1Giulia De Angelis2Michael Biggel3Basil Britto Xavier4Christine Lammens5Qiang Lin6Sandra Van Puyvelde7Herman Goossens8Samir Kumar-Singh9Youri Glupczynski10Yehuda Carmeli11Evelina Tacconelli12Surbhi Malhotra-Kumar13the SATURN WP1, 4, 5 study groupsLaboratory of Medical Microbiology, Vaccine and Infectious Diseases Institute, University of AntwerpDepartment of Internal Medicine I, Clinical Research Unit - German Centre for Infectious Diseases, Division of Infectious Disease, Tübingen University HospitalInstitute of Microbiology, Fondazione Policlinico Universitario A. Gemelli IRCCS – Università Cattolica del Sacro CuoreInstitute for Food Safety and Hygiene, Vetsuisse Faculty, University of ZurichLaboratory of Medical Microbiology, Vaccine and Infectious Diseases Institute, University of AntwerpLaboratory of Medical Microbiology, Vaccine and Infectious Diseases Institute, University of AntwerpLaboratory of Medical Microbiology, Vaccine and Infectious Diseases Institute, University of AntwerpLaboratory of Medical Microbiology, Vaccine and Infectious Diseases Institute, University of AntwerpLaboratory of Medical Microbiology, Vaccine and Infectious Diseases Institute, University of AntwerpLaboratory of Medical Microbiology, Vaccine and Infectious Diseases Institute, University of AntwerpLaboratory of Medical Microbiology, Vaccine and Infectious Diseases Institute, University of AntwerpDivision of Epidemiology and Preventive Medicine, Tel Aviv Sourasky Medical CentreDepartment of Internal Medicine I, Clinical Research Unit - German Centre for Infectious Diseases, Division of Infectious Disease, Tübingen University HospitalLaboratory of Medical Microbiology, Vaccine and Infectious Diseases Institute, University of AntwerpAbstract Background The impact of community carriage on the influx of extended-spectrum beta-lactamase-producing Enterobacterales (ESBL-E) into hospitals remains understudied. In this prospective 2-year single-centre study, we investigate the community ESBL-E influx and trace the colonisation, nosocomial acquisition, transmission, and infection dynamics of ESBL-producing Escherichia coli (ESBL-Ec) in non-ICU wards at a tertiary care hospital. Methods This study reports primary and post hoc outcomes of the clinical trial NCT01208519 in which hospitalised patients were screened for rectal carriage of ESBL-E. ESBL-Ec isolates from ≈50% of carriers, including all patients who developed infections, were sequenced and genotyped. Endogenous infection was defined as infection by the same strain (< 10 SNPs distance) as colonizing strain. Results Of 3703 screened patients, 456 (12.3%) were ESBL-positive-at-admission (PA-ESBL). Of the 2268 ESBL-negative-at-admission (NA-ESBL) patients with follow-up samples, 240 (10.6%) acquired ESBL-E (HA-ESBL), with an incidence density rate of 7.96 cases/1000 patient-day, notably higher in patients receiving antibiotics (P < 0.001). PA- and HA-ESBL patients developed significantly more ESBL-E infections than ESBL-free patients (P < 0.001). Sequenced ESBL-Ec showed high clonal diversity dominated by the multidrug-resistant and highly virulent ST131 clade, C2/H30-Rx. Among ESBL-Ec infections, 60% (18/30) were endogenous. Direct between-patients transmission clusters (n = 21) involved 23.9% (48/201) of patients and 23.0% (84/366) of ESBL-Ec isolates. Conclusions Our data show a high prevalence of nosocomial acquisition of ESBL-E in a non-ICU setting. The study provides genomic evidence that the endogenous reservoir is the main driver of ESBL-Ec infections underscoring the need for wide implementation of antibiotic stewardship programmes to reduce antibiotic pressure.https://doi.org/10.1186/s13073-024-01424-2ESBL-Escherichia coliNosocomial acquisitionAntibiotic selective pressureCommunity settingHospital settingST131 |
| spellingShingle | Minh Ngoc Nguyen Beryl Primrose Gladstone Giulia De Angelis Michael Biggel Basil Britto Xavier Christine Lammens Qiang Lin Sandra Van Puyvelde Herman Goossens Samir Kumar-Singh Youri Glupczynski Yehuda Carmeli Evelina Tacconelli Surbhi Malhotra-Kumar the SATURN WP1, 4, 5 study groups Tracing carriage, acquisition, and transmission of ESBL-producing Escherichia coli over two years in a tertiary care hospital Genome Medicine ESBL-Escherichia coli Nosocomial acquisition Antibiotic selective pressure Community setting Hospital setting ST131 |
| title | Tracing carriage, acquisition, and transmission of ESBL-producing Escherichia coli over two years in a tertiary care hospital |
| title_full | Tracing carriage, acquisition, and transmission of ESBL-producing Escherichia coli over two years in a tertiary care hospital |
| title_fullStr | Tracing carriage, acquisition, and transmission of ESBL-producing Escherichia coli over two years in a tertiary care hospital |
| title_full_unstemmed | Tracing carriage, acquisition, and transmission of ESBL-producing Escherichia coli over two years in a tertiary care hospital |
| title_short | Tracing carriage, acquisition, and transmission of ESBL-producing Escherichia coli over two years in a tertiary care hospital |
| title_sort | tracing carriage acquisition and transmission of esbl producing escherichia coli over two years in a tertiary care hospital |
| topic | ESBL-Escherichia coli Nosocomial acquisition Antibiotic selective pressure Community setting Hospital setting ST131 |
| url | https://doi.org/10.1186/s13073-024-01424-2 |
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