N Stoesser, R George, Z Aiken, H T T Phan, S Lipworth, T P Quan, A J Mathers, N De Maio, A C Seale, D W Eyre, A Vaughan, J Swann, T E A Peto, D W Crook, J Cawthorne, A Dodgson, A S Walker
{"title":"通过对病房废水环境和患者进行基因组流行病学和纵向采样，揭示了医院环境中产蓝 KPC-碳青霉烯酶肠杆菌传播动态的复杂性。","authors":"N Stoesser, R George, Z Aiken, H T T Phan, S Lipworth, T P Quan, A J Mathers, N De Maio, A C Seale, D W Eyre, A Vaughan, J Swann, T E A Peto, D W Crook, J Cawthorne, A Dodgson, A S Walker","doi":"10.1093/jacamr/dlae140","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>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><p><strong>Methods: </strong>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 Tn<i>4401</i> types/target site sequences. The accessory genome was evaluated in some of the largest clusters, and those crossing reservoirs.</p><p><strong>Results: </strong>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. Tn<i>4401</i> + flanking target site sequence diversity was greater in wastewater sites (<i>P</i> < 0.001), which might favour Tn<i>4401</i>-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; <i>P</i> = 0.0019; and adjusted OR = 2.60; 95% CI: 1.04-6.52; <i>P</i> = 0.0410, respectively). Different strains had different bla<sub>KPC</sub> dissemination dynamics.</p><p><strong>Conclusions: </strong>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.</p>","PeriodicalId":14594,"journal":{"name":"JAC-Antimicrobial Resistance","volume":"6 5","pages":"dlae140"},"PeriodicalIF":3.7000,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11369815/pdf/","citationCount":"0","resultStr":"{\"title\":\"Genomic epidemiology and longitudinal sampling of ward wastewater environments and patients reveals complexity of the transmission dynamics of <i>bla</i> <sub>KPC</sub>-carbapenemase-producing Enterobacterales in a hospital setting.\",\"authors\":\"N Stoesser, R George, Z Aiken, H T T Phan, S Lipworth, T P Quan, A J Mathers, N De Maio, A C Seale, D W Eyre, A Vaughan, J Swann, T E A Peto, D W Crook, J Cawthorne, A Dodgson, A S Walker\",\"doi\":\"10.1093/jacamr/dlae140\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><strong>Background: </strong>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><p><strong>Methods: </strong>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 Tn<i>4401</i> types/target site sequences. The accessory genome was evaluated in some of the largest clusters, and those crossing reservoirs.</p><p><strong>Results: </strong>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. Tn<i>4401</i> + flanking target site sequence diversity was greater in wastewater sites (<i>P</i> < 0.001), which might favour Tn<i>4401</i>-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; <i>P</i> = 0.0019; and adjusted OR = 2.60; 95% CI: 1.04-6.52; <i>P</i> = 0.0410, respectively). Different strains had different bla<sub>KPC</sub> dissemination dynamics.</p><p><strong>Conclusions: </strong>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.</p>\",\"PeriodicalId\":14594,\"journal\":{\"name\":\"JAC-Antimicrobial Resistance\",\"volume\":\"6 5\",\"pages\":\"dlae140\"},\"PeriodicalIF\":3.7000,\"publicationDate\":\"2024-09-03\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11369815/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"JAC-Antimicrobial Resistance\",\"FirstCategoryId\":\"1085\",\"ListUrlMain\":\"https://doi.org/10.1093/jacamr/dlae140\",\"RegionNum\":0,\"RegionCategory\":null,\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2024/10/1 0:00:00\",\"PubModel\":\"eCollection\",\"JCR\":\"Q2\",\"JCRName\":\"INFECTIOUS DISEASES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"JAC-Antimicrobial Resistance","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1093/jacamr/dlae140","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/10/1 0:00:00","PubModel":"eCollection","JCR":"Q2","JCRName":"INFECTIOUS DISEASES","Score":null,"Total":0}
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.
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.
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