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Background <p>Infections caused by KPC-producing <i>Klebsiella pneumoniae</i> (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> Methods <p>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> Results <p>Among 467 patients, 33.2% had non-HOI (ID 0.53/1,000 admissions/month) and 66.8% HOI (ID 0.30, <i>p</i> = 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> Conclusions <p>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>

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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

  • 期刊论文

  • 出版模式：

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  • 发表日期：

    2025年8月7日

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  • 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,
  • Cristina Molina,
  • Clara Natera,
  • Álvaro Torre-Giménez,
  • Julián Torre-Giménez,
  • Elisa Vidal,
  • Manuel Causse,
  • Eduardo Marfil,
  • Julia Guzmán-Puche,
  • Tania Blanco,
  • Cristina Elías,
  • María Córdoba,
  • Carmen de la Fuente,
  • Jorge Rodriguez,
  • José López-Miranda,
  • Nicola Lorusso,
  • Laura Pérez-Velasco,
  • Rafael Arévalo-Álvarez,
  • María Camacho-Ruano,
  • Fabiola Gómez-Sevilla

摘要

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.