Community carriage of ESBL-producing Escherichia coli and Klebsiella pneumoniae: a cross-sectional study of risk factors and comparative genomics of carriage and clinical isolates
ABSTRACT The global prevalence of infections caused by extended-spectrum β-lactamase-producing Enterobacterales (ESBL-E) is increasing, and for Escherichia coli, observations indicate that this is partly driven by community-onset cases. The ESBL-E population structure in the community is scarcely de...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-08-01
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| Series: | mSphere |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msphere.00025-23 |
| _version_ | 1797730328193794048 |
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| author | Niclas Raffelsberger Dorota Julia Buczek Kristian Svendsen Lars Småbrekke Anna Kaarina Pöntinen Iren H. Löhr Lotte Leonore Eivindsdatter Andreassen Gunnar Skov Simonsen Arnfinn Sundsfjord Kirsten Gravningen Ørjan Samuelsen |
| author_facet | Niclas Raffelsberger Dorota Julia Buczek Kristian Svendsen Lars Småbrekke Anna Kaarina Pöntinen Iren H. Löhr Lotte Leonore Eivindsdatter Andreassen Gunnar Skov Simonsen Arnfinn Sundsfjord Kirsten Gravningen Ørjan Samuelsen |
| author_sort | Niclas Raffelsberger |
| collection | DOAJ |
| description | ABSTRACT The global prevalence of infections caused by extended-spectrum β-lactamase-producing Enterobacterales (ESBL-E) is increasing, and for Escherichia coli, observations indicate that this is partly driven by community-onset cases. The ESBL-E population structure in the community is scarcely described, and data on risk factors for carriage are conflicting. Here, we report the prevalence and population structure of fecal ESBL-producing E. coli and Klebsiella pneumoniae (ESBL-Ec/Kp) in a general adult population, examine risk factors, and compare carriage isolates with contemporary clinical isolates. Fecal samples obtained from 4,999 participants (54% women) ≥40 years in the seventh survey of the population-based Tromsø Study, Norway (2015, 2016), were screened for ESBL-Ec/Kp. In addition, we included 118 ESBL-Ec clinical isolates from the Norwegian surveillance program in 2014. All isolates were whole-genome sequenced. Risk factors associated with carriage were analyzed using multivariable logistic regression. ESBL-Ec gastrointestinal carriage prevalence was 3.3% [95% confidence interval (CI) 2.8%–3.9%, no sex difference] and 0.08% (0.02%–0.20%) for ESBL-Kp. For ESBL-Ec, travel to Asia was the only independent risk factor (adjusted odds ratio 3.46, 95% CI 2.18–5.49). E. coli ST131 was most prevalent in both collections. However, the ST131 proportion was significantly lower in carriage (24%) versus clinical isolates (58%, P < 0.001). Carriage isolates were genetically more diverse with a higher proportion of phylogroup A (26%) than clinical isolates (5%, P < 0.001), indicating that ESBL gene acquisition occurs in a variety of E. coli lineages colonizing the gut. STs commonly related to extraintestinal infections were more frequent in clinical isolates also carrying a higher prevalence of antimicrobial resistance, which could indicate clone-associated pathogenicity. IMPORTANCE ESBL-Ec and ESBL-Kp are major pathogens in the global burden of antimicrobial resistance. However, there is a gap in knowledge concerning the bacterial population structure of human ESBL-Ec/Kp carriage isolates in the community. We have examined ESBL-Ec/Kp isolates from a population-based study and compared these to contemporary clinical isolates. The large genetic diversity of carriage isolates indicates frequent ESBL gene acquisition, while those causing invasive infections are more clone dependent and associated with a higher prevalence of antibiotic resistance. The knowledge of factors associated with ESBL carriage helps to identify patients at risk to combat the spread of resistant bacteria within the healthcare system. Particularly, previous travel to Asia stands out as a major risk factor for carriage and should be considered in selecting empirical antibiotic treatment in critically ill patients. |
| first_indexed | 2024-03-12T11:42:42Z |
| format | Article |
| id | doaj.art-92fbb9207ddf431b88472033122999bf |
| institution | Directory Open Access Journal |
| issn | 2379-5042 |
| language | English |
| last_indexed | 2024-03-12T11:42:42Z |
| publishDate | 2023-08-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSphere |
| spelling | doaj.art-92fbb9207ddf431b88472033122999bf2023-08-31T14:26:40ZengAmerican Society for MicrobiologymSphere2379-50422023-08-018410.1128/msphere.00025-23Community carriage of ESBL-producing Escherichia coli and Klebsiella pneumoniae: a cross-sectional study of risk factors and comparative genomics of carriage and clinical isolatesNiclas Raffelsberger0Dorota Julia Buczek1Kristian Svendsen2Lars Småbrekke3Anna Kaarina Pöntinen4Iren H. Löhr5Lotte Leonore Eivindsdatter Andreassen6Gunnar Skov Simonsen7Arnfinn Sundsfjord8Kirsten Gravningen9Ørjan Samuelsen10Department of Microbiology and Infection Control, University Hospital of North Norway , Tromsø, NorwayDepartment of Medical Biology, Faculty of Health Sciences, UiT The Arctic University of Norway , Tromsø, NorwayDepartment of Pharmacy, Faculty of Health Sciences, UiT The Arctic University of Norway , Tromsø, NorwayDepartment of Pharmacy, Faculty of Health Sciences, UiT The Arctic University of Norway , Tromsø, NorwayNorwegian National Advisory Unit on Detection of Antimicrobial Resistance, Department of Microbiology and Infection Control, University Hospital of North Norway , Tromsø, NorwayDepartment of Medical Microbiology, Stavanger University Hospital , Stavanger, NorwayDepartment of Microbiology and Infection Control, University Hospital of North Norway , Tromsø, NorwayDepartment of Microbiology and Infection Control, University Hospital of North Norway , Tromsø, NorwayDepartment of Medical Biology, Faculty of Health Sciences, UiT The Arctic University of Norway , Tromsø, NorwayDepartment of Microbiology and Infection Control, University Hospital of North Norway , Tromsø, NorwayDepartment of Pharmacy, Faculty of Health Sciences, UiT The Arctic University of Norway , Tromsø, NorwayABSTRACT The global prevalence of infections caused by extended-spectrum β-lactamase-producing Enterobacterales (ESBL-E) is increasing, and for Escherichia coli, observations indicate that this is partly driven by community-onset cases. The ESBL-E population structure in the community is scarcely described, and data on risk factors for carriage are conflicting. Here, we report the prevalence and population structure of fecal ESBL-producing E. coli and Klebsiella pneumoniae (ESBL-Ec/Kp) in a general adult population, examine risk factors, and compare carriage isolates with contemporary clinical isolates. Fecal samples obtained from 4,999 participants (54% women) ≥40 years in the seventh survey of the population-based Tromsø Study, Norway (2015, 2016), were screened for ESBL-Ec/Kp. In addition, we included 118 ESBL-Ec clinical isolates from the Norwegian surveillance program in 2014. All isolates were whole-genome sequenced. Risk factors associated with carriage were analyzed using multivariable logistic regression. ESBL-Ec gastrointestinal carriage prevalence was 3.3% [95% confidence interval (CI) 2.8%–3.9%, no sex difference] and 0.08% (0.02%–0.20%) for ESBL-Kp. For ESBL-Ec, travel to Asia was the only independent risk factor (adjusted odds ratio 3.46, 95% CI 2.18–5.49). E. coli ST131 was most prevalent in both collections. However, the ST131 proportion was significantly lower in carriage (24%) versus clinical isolates (58%, P < 0.001). Carriage isolates were genetically more diverse with a higher proportion of phylogroup A (26%) than clinical isolates (5%, P < 0.001), indicating that ESBL gene acquisition occurs in a variety of E. coli lineages colonizing the gut. STs commonly related to extraintestinal infections were more frequent in clinical isolates also carrying a higher prevalence of antimicrobial resistance, which could indicate clone-associated pathogenicity. IMPORTANCE ESBL-Ec and ESBL-Kp are major pathogens in the global burden of antimicrobial resistance. However, there is a gap in knowledge concerning the bacterial population structure of human ESBL-Ec/Kp carriage isolates in the community. We have examined ESBL-Ec/Kp isolates from a population-based study and compared these to contemporary clinical isolates. The large genetic diversity of carriage isolates indicates frequent ESBL gene acquisition, while those causing invasive infections are more clone dependent and associated with a higher prevalence of antibiotic resistance. The knowledge of factors associated with ESBL carriage helps to identify patients at risk to combat the spread of resistant bacteria within the healthcare system. Particularly, previous travel to Asia stands out as a major risk factor for carriage and should be considered in selecting empirical antibiotic treatment in critically ill patients.https://journals.asm.org/doi/10.1128/msphere.00025-23Escherichia coliKlebsiella pneumoniaeextended-spectrum β-lactamaseantimicrobial resistancecarriagerisk factors |
| spellingShingle | Niclas Raffelsberger Dorota Julia Buczek Kristian Svendsen Lars Småbrekke Anna Kaarina Pöntinen Iren H. Löhr Lotte Leonore Eivindsdatter Andreassen Gunnar Skov Simonsen Arnfinn Sundsfjord Kirsten Gravningen Ørjan Samuelsen Community carriage of ESBL-producing Escherichia coli and Klebsiella pneumoniae: a cross-sectional study of risk factors and comparative genomics of carriage and clinical isolates mSphere Escherichia coli Klebsiella pneumoniae extended-spectrum β-lactamase antimicrobial resistance carriage risk factors |
| title | Community carriage of ESBL-producing Escherichia coli and Klebsiella pneumoniae: a cross-sectional study of risk factors and comparative genomics of carriage and clinical isolates |
| title_full | Community carriage of ESBL-producing Escherichia coli and Klebsiella pneumoniae: a cross-sectional study of risk factors and comparative genomics of carriage and clinical isolates |
| title_fullStr | Community carriage of ESBL-producing Escherichia coli and Klebsiella pneumoniae: a cross-sectional study of risk factors and comparative genomics of carriage and clinical isolates |
| title_full_unstemmed | Community carriage of ESBL-producing Escherichia coli and Klebsiella pneumoniae: a cross-sectional study of risk factors and comparative genomics of carriage and clinical isolates |
| title_short | Community carriage of ESBL-producing Escherichia coli and Klebsiella pneumoniae: a cross-sectional study of risk factors and comparative genomics of carriage and clinical isolates |
| title_sort | community carriage of esbl producing escherichia coli and klebsiella pneumoniae a cross sectional study of risk factors and comparative genomics of carriage and clinical isolates |
| topic | Escherichia coli Klebsiella pneumoniae extended-spectrum β-lactamase antimicrobial resistance carriage risk factors |
| url | https://journals.asm.org/doi/10.1128/msphere.00025-23 |
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