A one-year genomic investigation of Escherichia coli epidemiology and nosocomial spread at a large US healthcare network
Abstract Background Extra-intestinal pathogenic Escherichia coli (ExPEC) are a leading cause of bloodstream and urinary tract infections worldwide. Over the last two decades, increased rates of antibiotic resistance in E. coli have been reported, further complicating treatment. Worryingly, specific...
| Main Authors: | , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2022-12-01
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| Series: | Genome Medicine |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s13073-022-01150-7 |
| _version_ | 1797973591720984576 |
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| author | Emma G. Mills Melissa J. Martin Ting L. Luo Ana C. Ong Rosslyn Maybank Brendan W. Corey Casey Harless Lan N. Preston Joshua A. Rosado-Mendez Scott B. Preston Yoon I. Kwak Michael G. Backlund Jason W. Bennett Patrick T. Mc Gann Francois Lebreton |
| author_facet | Emma G. Mills Melissa J. Martin Ting L. Luo Ana C. Ong Rosslyn Maybank Brendan W. Corey Casey Harless Lan N. Preston Joshua A. Rosado-Mendez Scott B. Preston Yoon I. Kwak Michael G. Backlund Jason W. Bennett Patrick T. Mc Gann Francois Lebreton |
| author_sort | Emma G. Mills |
| collection | DOAJ |
| description | Abstract Background Extra-intestinal pathogenic Escherichia coli (ExPEC) are a leading cause of bloodstream and urinary tract infections worldwide. Over the last two decades, increased rates of antibiotic resistance in E. coli have been reported, further complicating treatment. Worryingly, specific lineages expressing extended-spectrum β-lactamases (ESBLs) and fluoroquinolone resistance have proliferated and are now considered a serious threat. Obtaining contemporary information on the epidemiology and prevalence of these circulating lineages is critical for containing their spread globally and within the clinic. Methods Whole-genome sequencing (WGS), phylogenetic analysis, and antibiotic susceptibility testing were performed for a complete set of 2075 E. coli clinical isolates collected from 1776 patients at a large tertiary healthcare network in the USA between October 2019 and September 2020. Results The isolates represented two main phylogenetic groups, B2 and D, with six lineages accounting for 53% of strains: ST-69, ST-73, ST-95, ST-131, ST-127, and ST-1193. Twenty-seven percent of the primary isolates were multidrug resistant (MDR) and 5% carried an ESBL gene. Importantly, 74% of the ESBL-E.coli were co-resistant to fluoroquinolones and mostly belonged to pandemic ST-131 and emerging ST-1193. SNP-based detection of possible outbreaks identified 95 potential transmission clusters totaling 258 isolates (12% of the whole population) from ≥ 2 patients. While the proportion of MDR isolates was enriched in the set of putative transmission isolates compared to sporadic infections (35 vs 27%, p = 0.007), a large fraction (61%) of the predicted outbreaks (including the largest cluster grouping isolates from 12 patients) were caused by the transmission of non-MDR clones. Conclusion By coupling in-depth genomic characterization with a complete sampling of clinical isolates for a full year, this study provides a rare and contemporary survey on the epidemiology and spread of E. coli in a large US healthcare network. While surveillance and infection control efforts often focus on ESBL and MDR lineages, our findings reveal that non-MDR isolates represent a large burden of infections, including those of predicted nosocomial origins. This increased awareness is key for implementing effective WGS-based surveillance as a routine technology for infection control. |
| first_indexed | 2024-04-11T04:06:41Z |
| format | Article |
| id | doaj.art-c6a7e84f8e8342fd913a5627806b0eed |
| institution | Directory Open Access Journal |
| issn | 1756-994X |
| language | English |
| last_indexed | 2024-04-11T04:06:41Z |
| publishDate | 2022-12-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Medicine |
| spelling | doaj.art-c6a7e84f8e8342fd913a5627806b0eed2023-01-01T12:23:59ZengBMCGenome Medicine1756-994X2022-12-0114111310.1186/s13073-022-01150-7A one-year genomic investigation of Escherichia coli epidemiology and nosocomial spread at a large US healthcare networkEmma G. Mills0Melissa J. Martin1Ting L. Luo2Ana C. Ong3Rosslyn Maybank4Brendan W. Corey5Casey Harless6Lan N. Preston7Joshua A. Rosado-Mendez8Scott B. Preston9Yoon I. Kwak10Michael G. Backlund11Jason W. Bennett12Patrick T. Mc Gann13Francois Lebreton14Multidrug-Resistant Organism Repository and Surveillance Network, Walter Reed Army Institute of ResearchMultidrug-Resistant Organism Repository and Surveillance Network, Walter Reed Army Institute of ResearchMultidrug-Resistant Organism Repository and Surveillance Network, Walter Reed Army Institute of ResearchMultidrug-Resistant Organism Repository and Surveillance Network, Walter Reed Army Institute of ResearchMultidrug-Resistant Organism Repository and Surveillance Network, Walter Reed Army Institute of ResearchMultidrug-Resistant Organism Repository and Surveillance Network, Walter Reed Army Institute of ResearchMultidrug-Resistant Organism Repository and Surveillance Network, Walter Reed Army Institute of ResearchMultidrug-Resistant Organism Repository and Surveillance Network, Walter Reed Army Institute of ResearchMultidrug-Resistant Organism Repository and Surveillance Network, Walter Reed Army Institute of ResearchDepartment of Pathology, Walter Reed National Military Medical CenterMultidrug-Resistant Organism Repository and Surveillance Network, Walter Reed Army Institute of ResearchDepartment of Pathology, Walter Reed National Military Medical CenterMultidrug-Resistant Organism Repository and Surveillance Network, Walter Reed Army Institute of ResearchMultidrug-Resistant Organism Repository and Surveillance Network, Walter Reed Army Institute of ResearchMultidrug-Resistant Organism Repository and Surveillance Network, Walter Reed Army Institute of ResearchAbstract Background Extra-intestinal pathogenic Escherichia coli (ExPEC) are a leading cause of bloodstream and urinary tract infections worldwide. Over the last two decades, increased rates of antibiotic resistance in E. coli have been reported, further complicating treatment. Worryingly, specific lineages expressing extended-spectrum β-lactamases (ESBLs) and fluoroquinolone resistance have proliferated and are now considered a serious threat. Obtaining contemporary information on the epidemiology and prevalence of these circulating lineages is critical for containing their spread globally and within the clinic. Methods Whole-genome sequencing (WGS), phylogenetic analysis, and antibiotic susceptibility testing were performed for a complete set of 2075 E. coli clinical isolates collected from 1776 patients at a large tertiary healthcare network in the USA between October 2019 and September 2020. Results The isolates represented two main phylogenetic groups, B2 and D, with six lineages accounting for 53% of strains: ST-69, ST-73, ST-95, ST-131, ST-127, and ST-1193. Twenty-seven percent of the primary isolates were multidrug resistant (MDR) and 5% carried an ESBL gene. Importantly, 74% of the ESBL-E.coli were co-resistant to fluoroquinolones and mostly belonged to pandemic ST-131 and emerging ST-1193. SNP-based detection of possible outbreaks identified 95 potential transmission clusters totaling 258 isolates (12% of the whole population) from ≥ 2 patients. While the proportion of MDR isolates was enriched in the set of putative transmission isolates compared to sporadic infections (35 vs 27%, p = 0.007), a large fraction (61%) of the predicted outbreaks (including the largest cluster grouping isolates from 12 patients) were caused by the transmission of non-MDR clones. Conclusion By coupling in-depth genomic characterization with a complete sampling of clinical isolates for a full year, this study provides a rare and contemporary survey on the epidemiology and spread of E. coli in a large US healthcare network. While surveillance and infection control efforts often focus on ESBL and MDR lineages, our findings reveal that non-MDR isolates represent a large burden of infections, including those of predicted nosocomial origins. This increased awareness is key for implementing effective WGS-based surveillance as a routine technology for infection control.https://doi.org/10.1186/s13073-022-01150-7Escherichia coliGenomic epidemiologyST-131Antibiotic resistanceNosocomial |
| spellingShingle | Emma G. Mills Melissa J. Martin Ting L. Luo Ana C. Ong Rosslyn Maybank Brendan W. Corey Casey Harless Lan N. Preston Joshua A. Rosado-Mendez Scott B. Preston Yoon I. Kwak Michael G. Backlund Jason W. Bennett Patrick T. Mc Gann Francois Lebreton A one-year genomic investigation of Escherichia coli epidemiology and nosocomial spread at a large US healthcare network Genome Medicine Escherichia coli Genomic epidemiology ST-131 Antibiotic resistance Nosocomial |
| title | A one-year genomic investigation of Escherichia coli epidemiology and nosocomial spread at a large US healthcare network |
| title_full | A one-year genomic investigation of Escherichia coli epidemiology and nosocomial spread at a large US healthcare network |
| title_fullStr | A one-year genomic investigation of Escherichia coli epidemiology and nosocomial spread at a large US healthcare network |
| title_full_unstemmed | A one-year genomic investigation of Escherichia coli epidemiology and nosocomial spread at a large US healthcare network |
| title_short | A one-year genomic investigation of Escherichia coli epidemiology and nosocomial spread at a large US healthcare network |
| title_sort | one year genomic investigation of escherichia coli epidemiology and nosocomial spread at a large us healthcare network |
| topic | Escherichia coli Genomic epidemiology ST-131 Antibiotic resistance Nosocomial |
| url | https://doi.org/10.1186/s13073-022-01150-7 |
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