Manuel Recio-Rufián, Teresa López-Viñau, Víctor Gálvez-Soto, Ángela Cano, Rafael Ruiz-Montero, Belén Gutiérrez-Gutiérrez, Irene Gracia-Ahufinger, Germán Peñalva, Juan Antonio Marín-Sanz, Miriam Marín-Sanz, David Segorbe, Juan Jesús Pineda-Capitán, Montserrat Muñoz-Rosa, Cristina Riazzo, Federico Giovagnorio, Elisa Ruiz-Arabi, José David Torres-Peña, Juan José Castón, Isabel Machuca, Inmaculada Salcedo-Leal, Luis Martínez-Martínez, Elena Pérez-Nadales, Julián Torre-Cisneros
{"title":"在COVID-19时代之前和期间，医院和非医院发生的产kpc肺炎克雷伯菌感染的发病率、临床和基因组趋势：一项为期十年的中断时间序列研究","authors":"Manuel Recio-Rufián, Teresa López-Viñau, Víctor Gálvez-Soto, Ángela Cano, Rafael Ruiz-Montero, Belén Gutiérrez-Gutiérrez, Irene Gracia-Ahufinger, Germán Peñalva, Juan Antonio Marín-Sanz, Miriam Marín-Sanz, David Segorbe, Juan Jesús Pineda-Capitán, Montserrat Muñoz-Rosa, Cristina Riazzo, Federico Giovagnorio, Elisa Ruiz-Arabi, José David Torres-Peña, Juan José Castón, Isabel Machuca, Inmaculada Salcedo-Leal, Luis Martínez-Martínez, Elena Pérez-Nadales, Julián Torre-Cisneros","doi":"10.1186/s13756-025-01614-6","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>Infections caused by KPC-producing Klebsiella pneumoniae (KPC-KP) represent a persistent public health challenge. This prospective study examines ten-year trends, clinical features, and genomic epidemiology of hospital-onset (HOI) and non-hospital-onset (non-HOI, including healthcare-associated [HcAI] and community-acquired [CA]) KPC-KP infections following a 2012 outbreak. We evaluated the impacts of a 2014 antimicrobial stewardship program (ASP) and COVID-19-related infection prevention and control (IPC) measures, with emphasis on hospital-to-community dissemination.</p><p><strong>Methods: </strong>We analysed a prospective, longitudinal cohort of patients (2012-2022) in a tertiary referral hospital. Interrupted time series and ARIMA models assessed ASP and IPC impacts on incidence density (ID). Cross-correlation analysis explored temporal associations between HOI and non-HOI trends. Whole-genome sequencing and PERMANOVA evaluated the genomic structure of ST512/KPC-3 isolates. Multivariable regression analysed the association between infection type and clinical outcomes.</p><p><strong>Results: </strong>Among 467 patients, 33.2% had non-HOI (ID 0.53/1,000 admissions/month) and 66.8% HOI (ID 0.30, p = 0.39). Urinary tract infections predominated in non-HOI (52.9%), while bloodstream and respiratory infections were more common in HOI. Incidence density of HOI and non-HOI infections declined significantly following ASP implementation, with a 4-month lag suggesting sequential transmission dynamics. These reductions were maintained during the pandemic. Genomic data confirmed ST512/KPC-3 dominance and hospital-to-community spread, with temporal factors-rather than acquisition type-explaining genetic variation. Adjusted analyses showed similar 30-day mortality and treatment responses across HOI and non-HOI.</p><p><strong>Conclusions: </strong>ASP and COVID-19 IPC measures contributed to maintaining low KPC-KP incidence. Genomic evidence underscores the role of temporal dynamics and clonal expansion in ST512/KPC-3 dissemination. Non-HOI infections are clinically significant and require targeted, system-wide surveillance and control strategies.</p>","PeriodicalId":7950,"journal":{"name":"Antimicrobial Resistance and Infection Control","volume":"14 1","pages":"97"},"PeriodicalIF":4.4000,"publicationDate":"2025-08-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12333191/pdf/","citationCount":"0","resultStr":"{\"title\":\"Incidence, clinical and genomic trends of hospital- and Non-hospital-onset KPC-producing Klebsiella pneumoniae infections before and during the COVID-19 era: a ten-year interrupted time series study.\",\"authors\":\"Manuel Recio-Rufián, Teresa López-Viñau, Víctor Gálvez-Soto, Ángela Cano, Rafael Ruiz-Montero, Belén Gutiérrez-Gutiérrez, Irene Gracia-Ahufinger, Germán Peñalva, Juan Antonio Marín-Sanz, Miriam Marín-Sanz, David Segorbe, Juan Jesús Pineda-Capitán, Montserrat Muñoz-Rosa, Cristina Riazzo, Federico Giovagnorio, Elisa Ruiz-Arabi, José David Torres-Peña, Juan José Castón, Isabel Machuca, Inmaculada Salcedo-Leal, Luis Martínez-Martínez, Elena Pérez-Nadales, Julián Torre-Cisneros\",\"doi\":\"10.1186/s13756-025-01614-6\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><strong>Background: </strong>Infections caused by KPC-producing Klebsiella pneumoniae (KPC-KP) represent a persistent public health challenge. This prospective study examines ten-year trends, clinical features, and genomic epidemiology of hospital-onset (HOI) and non-hospital-onset (non-HOI, including healthcare-associated [HcAI] and community-acquired [CA]) KPC-KP infections following a 2012 outbreak. We evaluated the impacts of a 2014 antimicrobial stewardship program (ASP) and COVID-19-related infection prevention and control (IPC) measures, with emphasis on hospital-to-community dissemination.</p><p><strong>Methods: </strong>We analysed a prospective, longitudinal cohort of patients (2012-2022) in a tertiary referral hospital. Interrupted time series and ARIMA models assessed ASP and IPC impacts on incidence density (ID). Cross-correlation analysis explored temporal associations between HOI and non-HOI trends. Whole-genome sequencing and PERMANOVA evaluated the genomic structure of ST512/KPC-3 isolates. Multivariable regression analysed the association between infection type and clinical outcomes.</p><p><strong>Results: </strong>Among 467 patients, 33.2% had non-HOI (ID 0.53/1,000 admissions/month) and 66.8% HOI (ID 0.30, p = 0.39). Urinary tract infections predominated in non-HOI (52.9%), while bloodstream and respiratory infections were more common in HOI. Incidence density of HOI and non-HOI infections declined significantly following ASP implementation, with a 4-month lag suggesting sequential transmission dynamics. These reductions were maintained during the pandemic. Genomic data confirmed ST512/KPC-3 dominance and hospital-to-community spread, with temporal factors-rather than acquisition type-explaining genetic variation. Adjusted analyses showed similar 30-day mortality and treatment responses across HOI and non-HOI.</p><p><strong>Conclusions: </strong>ASP and COVID-19 IPC measures contributed to maintaining low KPC-KP incidence. Genomic evidence underscores the role of temporal dynamics and clonal expansion in ST512/KPC-3 dissemination. Non-HOI infections are clinically significant and require targeted, system-wide surveillance and control strategies.</p>\",\"PeriodicalId\":7950,\"journal\":{\"name\":\"Antimicrobial Resistance and Infection Control\",\"volume\":\"14 1\",\"pages\":\"97\"},\"PeriodicalIF\":4.4000,\"publicationDate\":\"2025-08-07\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12333191/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Antimicrobial Resistance and Infection Control\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.1186/s13756-025-01614-6\",\"RegionNum\":2,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"INFECTIOUS DISEASES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Antimicrobial Resistance and Infection Control","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1186/s13756-025-01614-6","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"INFECTIOUS DISEASES","Score":null,"Total":0}
Incidence, clinical and genomic trends of hospital- and Non-hospital-onset KPC-producing Klebsiella pneumoniae infections before and during the COVID-19 era: a ten-year interrupted time series study.
Background: Infections caused by KPC-producing Klebsiella pneumoniae (KPC-KP) represent a persistent public health challenge. This prospective study examines ten-year trends, clinical features, and genomic epidemiology of hospital-onset (HOI) and non-hospital-onset (non-HOI, including healthcare-associated [HcAI] and community-acquired [CA]) KPC-KP infections following a 2012 outbreak. We evaluated the impacts of a 2014 antimicrobial stewardship program (ASP) and COVID-19-related infection prevention and control (IPC) measures, with emphasis on hospital-to-community dissemination.
Methods: We analysed a prospective, longitudinal cohort of patients (2012-2022) in a tertiary referral hospital. Interrupted time series and ARIMA models assessed ASP and IPC impacts on incidence density (ID). Cross-correlation analysis explored temporal associations between HOI and non-HOI trends. Whole-genome sequencing and PERMANOVA evaluated the genomic structure of ST512/KPC-3 isolates. Multivariable regression analysed the association between infection type and clinical outcomes.
Results: Among 467 patients, 33.2% had non-HOI (ID 0.53/1,000 admissions/month) and 66.8% HOI (ID 0.30, p = 0.39). Urinary tract infections predominated in non-HOI (52.9%), while bloodstream and respiratory infections were more common in HOI. Incidence density of HOI and non-HOI infections declined significantly following ASP implementation, with a 4-month lag suggesting sequential transmission dynamics. These reductions were maintained during the pandemic. Genomic data confirmed ST512/KPC-3 dominance and hospital-to-community spread, with temporal factors-rather than acquisition type-explaining genetic variation. Adjusted analyses showed similar 30-day mortality and treatment responses across HOI and non-HOI.
Conclusions: ASP and COVID-19 IPC measures contributed to maintaining low KPC-KP incidence. Genomic evidence underscores the role of temporal dynamics and clonal expansion in ST512/KPC-3 dissemination. Non-HOI infections are clinically significant and require targeted, system-wide surveillance and control strategies.
期刊介绍：
Antimicrobial Resistance and Infection Control is a global forum for all those working on the prevention, diagnostic and treatment of health-care associated infections and antimicrobial resistance development in all health-care settings. The journal covers a broad spectrum of preeminent practices and best available data to the top interventional and translational research, and innovative developments in the field of infection control.
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