Genomic epidemiology and longitudinal sampling of ward wastewater environments and patients reveals complexity of the transmission dynamics of blaKPC-carbapenemase-producing Enterobacterales in a hospital setting
<p><b>Background</b></p> Healthcare-associated wastewater and asymptomatic patient reservoirs colonized by carbapenemase-producing Enterobacterales (CPE) contribute to nosocomial CPE dissemination, but the characteristics and dynamics of this remain unclear. <p><b&g...
| Main Authors: | , , , , , , , , , , , , , , , , |
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| Other Authors: | |
| Format: | Journal article |
| Language: | English |
| Published: |
Oxford University Press
2024
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| _version_ | 1826314460551184384 |
|---|---|
| author | Stoesser, N George, R Aiken, Z Phan, HTT Lipworth, S Quan, TP Mathers, AJ De Maio, N Seale, AC Eyre, DW Vaughan, A Swann, J Peto, TEA Crook, DW Cawthorne, J Dodgson, A Walker, AS |
| author2 | TRACE Investigators’ Group |
| author_facet | TRACE Investigators’ Group Stoesser, N George, R Aiken, Z Phan, HTT Lipworth, S Quan, TP Mathers, AJ De Maio, N Seale, AC Eyre, DW Vaughan, A Swann, J Peto, TEA Crook, DW Cawthorne, J Dodgson, A Walker, AS |
| author_sort | Stoesser, N |
| collection | OXFORD |
| description | <p><b>Background</b></p>
Healthcare-associated wastewater and asymptomatic patient reservoirs colonized by carbapenemase-producing Enterobacterales (CPE) contribute to nosocomial CPE dissemination, but the characteristics and dynamics of this remain unclear.
<p><b>Methods</b></p>
We systematically sampled wastewater sites (<i>n</i> = 4488 samples; 349 sites) and patients (<i>n</i> = 1247) across six wards over 6–12 months to understand bla<sub>KPC</sub>-associated CPE (KPC-E) diversity within these reservoirs and transmission in a healthcare setting. Up to five KPC-E-positive isolates per sample were sequenced (Illumina). Recombination-adjusted phylogenies were used to define genetically related strains; assembly and mapping-based approaches were used to characterize antimicrobial resistance genes, insertion sequences (ISs) and Tn4401 types/target site sequences. The accessory genome was evaluated in some of the largest clusters, and those crossing reservoirs.
<p><b>Results</b></p>
Wastewater site KPC-E-positivity was substantial [101/349 sites (28.9%); 228/5601 (4.1%) patients cultured]. Thirteen KPC-E species and 109 strains were identified using genomics, and 24% of wastewater and 26% of patient KPC-E-positive samples harboured one or more strains. Most diversity was explained by the individual niche, suggesting localized factors are important in selection and spread. Tn4401 + flanking target site sequence diversity was greater in wastewater sites (P < 0.001), which might favour Tn4401-associated transposition/evolution. Shower/bath- and sluice/mop-associated sites were more likely to be KPC-E-positive (adjusted OR = 2.69; 95% CI: 1.44–5.01; P = 0.0019; and adjusted OR = 2.60; 95% CI: 1.04–6.52; P = 0.0410, respectively). Different strains had different bla<sub>KPC<sub> dissemination dynamics.
<p><b>Conclusions</b></p>
We identified substantial and diverse KPC-E colonization of wastewater sites and patients in this hospital setting. Reservoir and niche-specific factors (e.g. microbial interactions, selection pressures), and different strains and mobile genetic elements likely affect transmission dynamics. This should be considered in surveillance and control strategies. |
| first_indexed | 2024-09-25T04:34:23Z |
| format | Journal article |
| id | oxford-uuid:01192d00-dd7b-46ea-b236-823e883b8147 |
| institution | University of Oxford |
| language | English |
| last_indexed | 2024-09-25T04:34:23Z |
| publishDate | 2024 |
| publisher | Oxford University Press |
| record_format | dspace |
| spelling | oxford-uuid:01192d00-dd7b-46ea-b236-823e883b81472024-09-13T20:03:43ZGenomic epidemiology and longitudinal sampling of ward wastewater environments and patients reveals complexity of the transmission dynamics of blaKPC-carbapenemase-producing Enterobacterales in a hospital settingJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:01192d00-dd7b-46ea-b236-823e883b8147EnglishSymplectic ElementsOxford University Press2024Stoesser, NGeorge, RAiken, ZPhan, HTTLipworth, SQuan, TPMathers, AJDe Maio, NSeale, ACEyre, DWVaughan, ASwann, JPeto, TEACrook, DWCawthorne, JDodgson, AWalker, ASTRACE Investigators’ Group<p><b>Background</b></p> Healthcare-associated wastewater and asymptomatic patient reservoirs colonized by carbapenemase-producing Enterobacterales (CPE) contribute to nosocomial CPE dissemination, but the characteristics and dynamics of this remain unclear. <p><b>Methods</b></p> We systematically sampled wastewater sites (<i>n</i> = 4488 samples; 349 sites) and patients (<i>n</i> = 1247) across six wards over 6–12 months to understand bla<sub>KPC</sub>-associated CPE (KPC-E) diversity within these reservoirs and transmission in a healthcare setting. Up to five KPC-E-positive isolates per sample were sequenced (Illumina). Recombination-adjusted phylogenies were used to define genetically related strains; assembly and mapping-based approaches were used to characterize antimicrobial resistance genes, insertion sequences (ISs) and Tn4401 types/target site sequences. The accessory genome was evaluated in some of the largest clusters, and those crossing reservoirs. <p><b>Results</b></p> Wastewater site KPC-E-positivity was substantial [101/349 sites (28.9%); 228/5601 (4.1%) patients cultured]. Thirteen KPC-E species and 109 strains were identified using genomics, and 24% of wastewater and 26% of patient KPC-E-positive samples harboured one or more strains. Most diversity was explained by the individual niche, suggesting localized factors are important in selection and spread. Tn4401 + flanking target site sequence diversity was greater in wastewater sites (P < 0.001), which might favour Tn4401-associated transposition/evolution. Shower/bath- and sluice/mop-associated sites were more likely to be KPC-E-positive (adjusted OR = 2.69; 95% CI: 1.44–5.01; P = 0.0019; and adjusted OR = 2.60; 95% CI: 1.04–6.52; P = 0.0410, respectively). Different strains had different bla<sub>KPC<sub> dissemination dynamics. <p><b>Conclusions</b></p> We identified substantial and diverse KPC-E colonization of wastewater sites and patients in this hospital setting. Reservoir and niche-specific factors (e.g. microbial interactions, selection pressures), and different strains and mobile genetic elements likely affect transmission dynamics. This should be considered in surveillance and control strategies. |
| spellingShingle | Stoesser, N George, R Aiken, Z Phan, HTT Lipworth, S Quan, TP Mathers, AJ De Maio, N Seale, AC Eyre, DW Vaughan, A Swann, J Peto, TEA Crook, DW Cawthorne, J Dodgson, A Walker, AS Genomic epidemiology and longitudinal sampling of ward wastewater environments and patients reveals complexity of the transmission dynamics of blaKPC-carbapenemase-producing Enterobacterales in a hospital setting |
| title | Genomic epidemiology and longitudinal sampling of ward wastewater environments and patients reveals complexity of the transmission dynamics of blaKPC-carbapenemase-producing Enterobacterales in a hospital setting |
| title_full | Genomic epidemiology and longitudinal sampling of ward wastewater environments and patients reveals complexity of the transmission dynamics of blaKPC-carbapenemase-producing Enterobacterales in a hospital setting |
| title_fullStr | Genomic epidemiology and longitudinal sampling of ward wastewater environments and patients reveals complexity of the transmission dynamics of blaKPC-carbapenemase-producing Enterobacterales in a hospital setting |
| title_full_unstemmed | Genomic epidemiology and longitudinal sampling of ward wastewater environments and patients reveals complexity of the transmission dynamics of blaKPC-carbapenemase-producing Enterobacterales in a hospital setting |
| title_short | Genomic epidemiology and longitudinal sampling of ward wastewater environments and patients reveals complexity of the transmission dynamics of blaKPC-carbapenemase-producing Enterobacterales in a hospital setting |
| title_sort | genomic epidemiology and longitudinal sampling of ward wastewater environments and patients reveals complexity of the transmission dynamics of blakpc carbapenemase producing enterobacterales in a hospital setting |
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