Dynamic association of antimicrobial resistance in urinary isolates of Escherichia coli and Klebsiella pneumoniae between primary care and hospital settings in the Netherlands (2008–2020): a population-based studyResearch in context

Summary: Background: It is unclear whether changes in antimicrobial resistance (AMR) in primary care influence AMR in hospital settings. Therefore, we investigated the dynamic association of AMR between primary care and hospitals. Methods: We studied resistance percentages of Escherichia coli and K...

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Main Authors: Evelyn Pamela Martínez, Annelies Verbon, Annelot F. Schoffelen, Wieke Altorf-van der Kuil, Joost van Rosmalen, James W.T. Cohen Stuart, Damian C. Melles, Karin van Dijk, Ali Alzubaidy, Maarten Scholing, Sacha D. Kuil, Gert J. Blaauw, Wieke Altorf - van der Kuil, Saskia M. Bierman, Sabine C. de Greeff, Sonja R. Groenendijk, Rudy Hertroys, Jos C.M. Monen, Daan W. Notermans, Jan Polman, Wouter J. van den Reek, Caroline Schneeberger-van der Linden, Feline Velthuis, Cornelia C.H. Wielders, Britt J. de Wit, Rony E. Zoetigheid, Wouter van den Bijllaardt, Elise M. Kraan, Michiel B. Haeseker, Júlia M. da Silva, Eefje de Jong, Boulos Maraha, Arjanne J. van Griethuysen, Bastiaan B. Wintermans, Marijke J.C.A. van Trijp, Anouk E. Muller, Man-Chi Wong, Alewijn Ott, Erik Bathoorn, Mariëtte Lokate, Jan Sinnige, Nienke Plantinga, Nicole H.M. Renders, Julia W. Dorigo-Zetsma, Leendert J. Bakker, Wim Ang, Karola Waar, Martha T. van der Beek, Maurine A. Leversteijn-van Hall, Suzan P. van Mens, Erik Schaftenaar, Marrigje H. Nabuurs-Franssen, Ianthe Maat, Patrick D.J. Sturm, Bram M.W. Diederen, Lonneke G.M. Bode, David S.Y. Ong, Michiel van Rijn, Sander Dinant, Martijn den Reijer, Dick W. van Dam, Els I.G.B. de Brauwer, Robbert G. Bentvelsen, Anton G.M. Buiting, Anne L.M. Vlek, Melanie de Graaf, Annet Troelstra, Arjan R. Jansz, Maurits P.A. van Meer, Janneke de Vries, Julian D. Machiels
Format: Article
Language:English
Published: Elsevier 2025-03-01
Series:The Lancet Regional Health. Europe
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Online Access:http://www.sciencedirect.com/science/article/pii/S2666776224003661
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author Evelyn Pamela Martínez
Annelies Verbon
Annelot F. Schoffelen
Wieke Altorf-van der Kuil
Joost van Rosmalen
James W.T. Cohen Stuart
Damian C. Melles
Karin van Dijk
Ali Alzubaidy
Maarten Scholing
Sacha D. Kuil
Gert J. Blaauw
Wieke Altorf - van der Kuil
Saskia M. Bierman
Sabine C. de Greeff
Sonja R. Groenendijk
Rudy Hertroys
Jos C.M. Monen
Daan W. Notermans
Jan Polman
Wouter J. van den Reek
Caroline Schneeberger-van der Linden
Annelot F. Schoffelen
Feline Velthuis
Cornelia C.H. Wielders
Britt J. de Wit
Rony E. Zoetigheid
Wouter van den Bijllaardt
Elise M. Kraan
Michiel B. Haeseker
Júlia M. da Silva
Eefje de Jong
Boulos Maraha
Arjanne J. van Griethuysen
Bastiaan B. Wintermans
Marijke J.C.A. van Trijp
Anouk E. Muller
Man-Chi Wong
Alewijn Ott
Erik Bathoorn
Mariëtte Lokate
Jan Sinnige
Damian C. Melles
Nienke Plantinga
Nicole H.M. Renders
Julia W. Dorigo-Zetsma
Leendert J. Bakker
Wim Ang
Karola Waar
Martha T. van der Beek
Maurine A. Leversteijn-van Hall
Suzan P. van Mens
Erik Schaftenaar
Marrigje H. Nabuurs-Franssen
Ianthe Maat
Patrick D.J. Sturm
Bram M.W. Diederen
Lonneke G.M. Bode
David S.Y. Ong
Michiel van Rijn
Sander Dinant
Martijn den Reijer
Dick W. van Dam
Els I.G.B. de Brauwer
Robbert G. Bentvelsen
Anton G.M. Buiting
Anne L.M. Vlek
Melanie de Graaf
Annet Troelstra
Arjan R. Jansz
Maurits P.A. van Meer
Janneke de Vries
Julian D. Machiels
author_facet Evelyn Pamela Martínez
Annelies Verbon
Annelot F. Schoffelen
Wieke Altorf-van der Kuil
Joost van Rosmalen
James W.T. Cohen Stuart
Damian C. Melles
Karin van Dijk
Ali Alzubaidy
Maarten Scholing
Sacha D. Kuil
Gert J. Blaauw
Wieke Altorf - van der Kuil
Saskia M. Bierman
Sabine C. de Greeff
Sonja R. Groenendijk
Rudy Hertroys
Jos C.M. Monen
Daan W. Notermans
Jan Polman
Wouter J. van den Reek
Caroline Schneeberger-van der Linden
Annelot F. Schoffelen
Feline Velthuis
Cornelia C.H. Wielders
Britt J. de Wit
Rony E. Zoetigheid
Wouter van den Bijllaardt
Elise M. Kraan
Michiel B. Haeseker
Júlia M. da Silva
Eefje de Jong
Boulos Maraha
Arjanne J. van Griethuysen
Bastiaan B. Wintermans
Marijke J.C.A. van Trijp
Anouk E. Muller
Man-Chi Wong
Alewijn Ott
Erik Bathoorn
Mariëtte Lokate
Jan Sinnige
Damian C. Melles
Nienke Plantinga
Nicole H.M. Renders
Julia W. Dorigo-Zetsma
Leendert J. Bakker
Wim Ang
Karola Waar
Martha T. van der Beek
Maurine A. Leversteijn-van Hall
Suzan P. van Mens
Erik Schaftenaar
Marrigje H. Nabuurs-Franssen
Ianthe Maat
Patrick D.J. Sturm
Bram M.W. Diederen
Lonneke G.M. Bode
David S.Y. Ong
Michiel van Rijn
Sander Dinant
Martijn den Reijer
Dick W. van Dam
Els I.G.B. de Brauwer
Robbert G. Bentvelsen
Anton G.M. Buiting
Anne L.M. Vlek
Melanie de Graaf
Annet Troelstra
Arjan R. Jansz
Maurits P.A. van Meer
Janneke de Vries
Julian D. Machiels
author_sort Evelyn Pamela Martínez
collection DOAJ
description Summary: Background: It is unclear whether changes in antimicrobial resistance (AMR) in primary care influence AMR in hospital settings. Therefore, we investigated the dynamic association of AMR between primary care and hospitals. Methods: We studied resistance percentages of Escherichia coli and Klebsiella pneumoniae isolates to co-amoxiclav, ciprofloxacin, fosfomycin, nitrofurantoin and trimethoprim submitted by primary care, hospital outpatient and hospital inpatient settings to the Dutch National AMR surveillance network (ISIS-AR) from 2008 to 2020. For each bacterium–antibiotic combination, we first conducted multivariable logistic regressions to calculate AMR odds ratios (ORs) by month and healthcare setting, adjusted for patient-related factors and a time term. Second, multiple time series analysis was done using vector autoregressive models including the (log) ORs for each bacterium–antibiotic combination. Models were interpreted by impulse response functions and Granger-causality tests. Findings: The main AMR association was unidirectional from primary care to hospital settings with Granger-causality p-values between <0.0001 and 0.029. Depending on the bacterium–antibiotic combination, a 1% increase of AMR in E. coli and K. pneumoniae in primary care leads to an increase of AMR in hospital settings ranging from 0.10% to 0.40%. For ciprofloxacin resistance in K. pneumoniae, we found significant bidirectional associations between all healthcare settings with Granger-causality p-values between <0.0001 and 0.0075. Interpretation: For the majority of bacterium–antibiotic combinations, the main AMR association was from primary care to hospital settings. These results underscore the importance of antibiotic stewardship at the community level. Funding: ISIS-AR is supported by the Ministry of Health, Welfare and Sport of the Netherlands and the first author by the Central University of Ecuador to follow a PhD program in Erasmus MC.
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spelling doaj-art-f07191146b2649a69e6a92fb20a3771c2025-01-04T04:57:14ZengElsevierThe Lancet Regional Health. Europe2666-77622025-03-0150101197Dynamic association of antimicrobial resistance in urinary isolates of Escherichia coli and Klebsiella pneumoniae between primary care and hospital settings in the Netherlands (2008–2020): a population-based studyResearch in contextEvelyn Pamela Martínez0Annelies Verbon1Annelot F. Schoffelen2Wieke Altorf-van der Kuil3Joost van Rosmalen4James W.T. Cohen StuartDamian C. MellesKarin van DijkAli AlzubaidyMaarten ScholingSacha D. KuilGert J. BlaauwWieke Altorf - van der KuilSaskia M. BiermanSabine C. de GreeffSonja R. GroenendijkRudy HertroysJos C.M. MonenDaan W. NotermansJan PolmanWouter J. van den ReekCaroline Schneeberger-van der LindenAnnelot F. SchoffelenFeline VelthuisCornelia C.H. WieldersBritt J. de WitRony E. ZoetigheidWouter van den BijllaardtElise M. KraanMichiel B. HaesekerJúlia M. da SilvaEefje de JongBoulos MarahaArjanne J. van GriethuysenBastiaan B. WintermansMarijke J.C.A. van TrijpAnouk E. MullerMan-Chi WongAlewijn OttErik BathoornMariëtte LokateJan SinnigeDamian C. MellesNienke PlantingaNicole H.M. RendersJulia W. Dorigo-ZetsmaLeendert J. BakkerWim AngKarola WaarMartha T. van der BeekMaurine A. Leversteijn-van HallSuzan P. van MensErik SchaftenaarMarrigje H. Nabuurs-FranssenIanthe MaatPatrick D.J. SturmBram M.W. DiederenLonneke G.M. BodeDavid S.Y. OngMichiel van RijnSander DinantMartijn den ReijerDick W. van DamEls I.G.B. de BrauwerRobbert G. BentvelsenAnton G.M. BuitingAnne L.M. VlekMelanie de GraafAnnet TroelstraArjan R. JanszMaurits P.A. van MeerJanneke de VriesJulian D. MachielsFacultad de Medicina Veterinaria y Zootecnia, Universidad Central del Ecuador, Quito, Ecuador; Department of Medical Microbiology and Infectious Diseases, Erasmus MC, University Medical Centre, Rotterdam, the Netherlands; Corresponding author. Facultad de Medicina Veterinaria y Zootecnia, Universidad Central del Ecuador, Quito, Ecuador.Department of Medical Microbiology and Infectious Diseases, Erasmus MC, University Medical Centre, Rotterdam, the Netherlands; Department of Infectious Diseases, Division of Internal Medicine and Dermatology, University Medical Center Utrecht, Utrecht University, the NetherlandsCentre for Infectious Diseases, Epidemiology and Surveillance, Dutch National Institute for Public Health and the Environment (RIVM), Bilthoven, the NetherlandsCentre for Infectious Diseases, Epidemiology and Surveillance, Dutch National Institute for Public Health and the Environment (RIVM), Bilthoven, the NetherlandsDepartment of Biostatistics, Erasmus MC, University Medical Centre, Rotterdam, the Netherlands; Department of Epidemiology, Erasmus MC, University Medical Centre, Rotterdam, the Netherlands; Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht University, Utrecht, the NetherlandsSummary: Background: It is unclear whether changes in antimicrobial resistance (AMR) in primary care influence AMR in hospital settings. Therefore, we investigated the dynamic association of AMR between primary care and hospitals. Methods: We studied resistance percentages of Escherichia coli and Klebsiella pneumoniae isolates to co-amoxiclav, ciprofloxacin, fosfomycin, nitrofurantoin and trimethoprim submitted by primary care, hospital outpatient and hospital inpatient settings to the Dutch National AMR surveillance network (ISIS-AR) from 2008 to 2020. For each bacterium–antibiotic combination, we first conducted multivariable logistic regressions to calculate AMR odds ratios (ORs) by month and healthcare setting, adjusted for patient-related factors and a time term. Second, multiple time series analysis was done using vector autoregressive models including the (log) ORs for each bacterium–antibiotic combination. Models were interpreted by impulse response functions and Granger-causality tests. Findings: The main AMR association was unidirectional from primary care to hospital settings with Granger-causality p-values between <0.0001 and 0.029. Depending on the bacterium–antibiotic combination, a 1% increase of AMR in E. coli and K. pneumoniae in primary care leads to an increase of AMR in hospital settings ranging from 0.10% to 0.40%. For ciprofloxacin resistance in K. pneumoniae, we found significant bidirectional associations between all healthcare settings with Granger-causality p-values between <0.0001 and 0.0075. Interpretation: For the majority of bacterium–antibiotic combinations, the main AMR association was from primary care to hospital settings. These results underscore the importance of antibiotic stewardship at the community level. Funding: ISIS-AR is supported by the Ministry of Health, Welfare and Sport of the Netherlands and the first author by the Central University of Ecuador to follow a PhD program in Erasmus MC.http://www.sciencedirect.com/science/article/pii/S2666776224003661Antimicrobial resistanceGeneral practitionersHealth care settingsGranger causalityMultiple time series
spellingShingle Evelyn Pamela Martínez
Annelies Verbon
Annelot F. Schoffelen
Wieke Altorf-van der Kuil
Joost van Rosmalen
James W.T. Cohen Stuart
Damian C. Melles
Karin van Dijk
Ali Alzubaidy
Maarten Scholing
Sacha D. Kuil
Gert J. Blaauw
Wieke Altorf - van der Kuil
Saskia M. Bierman
Sabine C. de Greeff
Sonja R. Groenendijk
Rudy Hertroys
Jos C.M. Monen
Daan W. Notermans
Jan Polman
Wouter J. van den Reek
Caroline Schneeberger-van der Linden
Annelot F. Schoffelen
Feline Velthuis
Cornelia C.H. Wielders
Britt J. de Wit
Rony E. Zoetigheid
Wouter van den Bijllaardt
Elise M. Kraan
Michiel B. Haeseker
Júlia M. da Silva
Eefje de Jong
Boulos Maraha
Arjanne J. van Griethuysen
Bastiaan B. Wintermans
Marijke J.C.A. van Trijp
Anouk E. Muller
Man-Chi Wong
Alewijn Ott
Erik Bathoorn
Mariëtte Lokate
Jan Sinnige
Damian C. Melles
Nienke Plantinga
Nicole H.M. Renders
Julia W. Dorigo-Zetsma
Leendert J. Bakker
Wim Ang
Karola Waar
Martha T. van der Beek
Maurine A. Leversteijn-van Hall
Suzan P. van Mens
Erik Schaftenaar
Marrigje H. Nabuurs-Franssen
Ianthe Maat
Patrick D.J. Sturm
Bram M.W. Diederen
Lonneke G.M. Bode
David S.Y. Ong
Michiel van Rijn
Sander Dinant
Martijn den Reijer
Dick W. van Dam
Els I.G.B. de Brauwer
Robbert G. Bentvelsen
Anton G.M. Buiting
Anne L.M. Vlek
Melanie de Graaf
Annet Troelstra
Arjan R. Jansz
Maurits P.A. van Meer
Janneke de Vries
Julian D. Machiels
Dynamic association of antimicrobial resistance in urinary isolates of Escherichia coli and Klebsiella pneumoniae between primary care and hospital settings in the Netherlands (2008–2020): a population-based studyResearch in context
The Lancet Regional Health. Europe
Antimicrobial resistance
General practitioners
Health care settings
Granger causality
Multiple time series
title Dynamic association of antimicrobial resistance in urinary isolates of Escherichia coli and Klebsiella pneumoniae between primary care and hospital settings in the Netherlands (2008–2020): a population-based studyResearch in context
title_full Dynamic association of antimicrobial resistance in urinary isolates of Escherichia coli and Klebsiella pneumoniae between primary care and hospital settings in the Netherlands (2008–2020): a population-based studyResearch in context
title_fullStr Dynamic association of antimicrobial resistance in urinary isolates of Escherichia coli and Klebsiella pneumoniae between primary care and hospital settings in the Netherlands (2008–2020): a population-based studyResearch in context
title_full_unstemmed Dynamic association of antimicrobial resistance in urinary isolates of Escherichia coli and Klebsiella pneumoniae between primary care and hospital settings in the Netherlands (2008–2020): a population-based studyResearch in context
title_short Dynamic association of antimicrobial resistance in urinary isolates of Escherichia coli and Klebsiella pneumoniae between primary care and hospital settings in the Netherlands (2008–2020): a population-based studyResearch in context
title_sort dynamic association of antimicrobial resistance in urinary isolates of escherichia coli and klebsiella pneumoniae between primary care and hospital settings in the netherlands 2008 2020 a population based studyresearch in context
topic Antimicrobial resistance
General practitioners
Health care settings
Granger causality
Multiple time series
url http://www.sciencedirect.com/science/article/pii/S2666776224003661
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AT suzanpvanmens dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext
AT erikschaftenaar dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext
AT marrigjehnabuursfranssen dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext
AT ianthemaat dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext
AT patrickdjsturm dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext
AT brammwdiederen dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext
AT lonnekegmbode dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext
AT davidsyong dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext
AT michielvanrijn dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext
AT sanderdinant dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext
AT martijndenreijer dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext
AT dickwvandam dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext
AT elsigbdebrauwer dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext
AT robbertgbentvelsen dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext
AT antongmbuiting dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext
AT annelmvlek dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext
AT melaniedegraaf dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext
AT annettroelstra dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext
AT arjanrjansz dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext
AT mauritspavanmeer dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext
AT jannekedevries dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext
AT juliandmachiels dynamicassociationofantimicrobialresistanceinurinaryisolatesofescherichiacoliandklebsiellapneumoniaebetweenprimarycareandhospitalsettingsinthenetherlands20082020apopulationbasedstudyresearchincontext