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
Abstract Background 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. Methods We systematically sampled wastewater s...
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| Veröffentlicht in: | JAC-antimicrobial resistance 2024-09, Vol.6 (5) |
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| creator | Stoesser, N George, R Aiken, Z Phan, H T T Lipworth, S Quan, T P Mathers, A J De Maio, N Seale, A C Eyre, D W Vaughan, A Swann, J Peto, T E A Crook, D W Cawthorne, J Dodgson, A Walker, A S |
| description | Abstract
Background
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.
Methods
We systematically sampled wastewater sites (n = 4488 samples; 349 sites) and patients (n = 1247) across six wards over 6–12 months to understand blaKPC-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.
Results
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 |
| doi_str_mv | 10.1093/jacamr/dlae140 |
| format | Article |
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Background
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.
Methods
We systematically sampled wastewater sites (n = 4488 samples; 349 sites) and patients (n = 1247) across six wards over 6–12 months to understand blaKPC-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.
Results
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 blaKPC dissemination dynamics.
Conclusions
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.</description><identifier>EISSN: 2632-1823</identifier><identifier>DOI: 10.1093/jacamr/dlae140</identifier><language>eng</language><publisher>UK: Oxford University Press</publisher><subject>Original</subject><ispartof>JAC-antimicrobial resistance, 2024-09, Vol.6 (5)</ispartof><rights>The Author(s) 2024. Published by Oxford University Press on behalf of British Society for Antimicrobial Chemotherapy. 2024</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><orcidid>0000-0002-4508-7969</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11369815/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11369815/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,27924,27925,53791,53793</link.rule.ids></links><search><creatorcontrib>Stoesser, N</creatorcontrib><creatorcontrib>George, R</creatorcontrib><creatorcontrib>Aiken, Z</creatorcontrib><creatorcontrib>Phan, H T T</creatorcontrib><creatorcontrib>Lipworth, S</creatorcontrib><creatorcontrib>Quan, T P</creatorcontrib><creatorcontrib>Mathers, A J</creatorcontrib><creatorcontrib>De Maio, N</creatorcontrib><creatorcontrib>Seale, A C</creatorcontrib><creatorcontrib>Eyre, D W</creatorcontrib><creatorcontrib>Vaughan, A</creatorcontrib><creatorcontrib>Swann, J</creatorcontrib><creatorcontrib>Peto, T E A</creatorcontrib><creatorcontrib>Crook, D W</creatorcontrib><creatorcontrib>Cawthorne, J</creatorcontrib><creatorcontrib>Dodgson, A</creatorcontrib><creatorcontrib>Walker, A S</creatorcontrib><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><title>JAC-antimicrobial resistance</title><description>Abstract
Background
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.
Methods
We systematically sampled wastewater sites (n = 4488 samples; 349 sites) and patients (n = 1247) across six wards over 6–12 months to understand blaKPC-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.
Results
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 blaKPC dissemination dynamics.
Conclusions
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.</description><subject>Original</subject><issn>2632-1823</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><recordid>eNpVUUtr3DAQNoFCQpprz7rm4EYj2V77FMqSpqWB9tCezVga7ypYDyTtpvs_-4MqZ0OhlxmGme8xfFX1AfhH4IO8e0aFNt7pBQkaflFdiU6KGnohL6ublJ4556Llm2Yjrqo_j-S8NYpRMJqs8YvfnRg6zRbvdiYftHG4sIQ2LMbtmJ_ZC0ZdSsr0gpkiI3c00TtLLqdXZMBsXodIR8IlMeULmn6bfFrxeU8sR3TJmpSMd0yfHBYLaV1OC377sa0VxgkDObKYqA7R64Na5R9cUfQTqtJwocSMY8j2PgWTV5uUczl7X72biy7dvPXr6tfnh5_bL_XT98ev209PtRfQ5hoGUvMk-1mjxnluBUiEbqOEnNtOc2gQGjkp0QgOk1aD2gjssG90PwzQQi-vq_szbzhMlrQqTxdXY4jGYjyNHs34_8aZ_bjzxxFAdkMPbWG4PTP4Q_iHAz6uOY7nHMe3HOVft-me3Q</recordid><startdate>20240903</startdate><enddate>20240903</enddate><creator>Stoesser, N</creator><creator>George, R</creator><creator>Aiken, Z</creator><creator>Phan, H T T</creator><creator>Lipworth, S</creator><creator>Quan, T P</creator><creator>Mathers, A J</creator><creator>De Maio, N</creator><creator>Seale, A C</creator><creator>Eyre, D W</creator><creator>Vaughan, A</creator><creator>Swann, J</creator><creator>Peto, T E A</creator><creator>Crook, D W</creator><creator>Cawthorne, J</creator><creator>Dodgson, A</creator><creator>Walker, A S</creator><general>Oxford University Press</general><scope>TOX</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-4508-7969</orcidid></search><sort><creationdate>20240903</creationdate><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><author>Stoesser, N ; George, R ; Aiken, Z ; Phan, H T T ; Lipworth, S ; Quan, T P ; Mathers, A J ; De Maio, N ; Seale, A C ; Eyre, D W ; Vaughan, A ; Swann, J ; Peto, T E A ; Crook, D W ; Cawthorne, J ; Dodgson, A ; Walker, A S</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-o215t-19ecfb38fdadaff5213a167c23f56d014a143bc24201bdc9c72a6a84d89915183</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Original</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Stoesser, N</creatorcontrib><creatorcontrib>George, R</creatorcontrib><creatorcontrib>Aiken, Z</creatorcontrib><creatorcontrib>Phan, H T T</creatorcontrib><creatorcontrib>Lipworth, S</creatorcontrib><creatorcontrib>Quan, T P</creatorcontrib><creatorcontrib>Mathers, A J</creatorcontrib><creatorcontrib>De Maio, N</creatorcontrib><creatorcontrib>Seale, A C</creatorcontrib><creatorcontrib>Eyre, D W</creatorcontrib><creatorcontrib>Vaughan, A</creatorcontrib><creatorcontrib>Swann, J</creatorcontrib><creatorcontrib>Peto, T E A</creatorcontrib><creatorcontrib>Crook, D W</creatorcontrib><creatorcontrib>Cawthorne, J</creatorcontrib><creatorcontrib>Dodgson, A</creatorcontrib><creatorcontrib>Walker, A S</creatorcontrib><collection>Open Access: Oxford University Press Open Journals</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>JAC-antimicrobial resistance</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Stoesser, N</au><au>George, R</au><au>Aiken, Z</au><au>Phan, H T T</au><au>Lipworth, S</au><au>Quan, T P</au><au>Mathers, A J</au><au>De Maio, N</au><au>Seale, A C</au><au>Eyre, D W</au><au>Vaughan, A</au><au>Swann, J</au><au>Peto, T E A</au><au>Crook, D W</au><au>Cawthorne, J</au><au>Dodgson, A</au><au>Walker, A S</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>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</atitle><jtitle>JAC-antimicrobial resistance</jtitle><date>2024-09-03</date><risdate>2024</risdate><volume>6</volume><issue>5</issue><eissn>2632-1823</eissn><abstract>Abstract
Background
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.
Methods
We systematically sampled wastewater sites (n = 4488 samples; 349 sites) and patients (n = 1247) across six wards over 6–12 months to understand blaKPC-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.
Results
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 blaKPC dissemination dynamics.
Conclusions
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.</abstract><cop>UK</cop><pub>Oxford University Press</pub><doi>10.1093/jacamr/dlae140</doi><orcidid>https://orcid.org/0000-0002-4508-7969</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Original |
| 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 |
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