Phenotypic and molecular characterization of IMP-producing Enterobacterales in Spain: Predominance of IMP-8 in Klebsiella pneumoniae and IMP-22 in Enterobacter roggenkampii

ObjectivesLittle is known about IMP-producing Enterobacterales (IMP-Ent) in Europe. We analyzed at genomic and phenotypic level IMP-Ent isolates circulating in Spain in a 9-year period.Materials and methodsIMP-Ent isolates submitted to our reference laboratory were included. Antibiotic susceptibilit...

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Main Authors: Javier E. Cañada-García, Natalin Grippo, Eva Ramírez de Arellano, Verónica Bautista, Noelia Lara, Ana María Navarro, Teresa Cabezas, Nora Mariela Martínez-Ramírez, Silvia García-Cobos, Jorge Calvo, Emilia Cercenado, Belén Aracil, María Pérez-Vázquez, Jesús Oteo-Iglesias, the Spanish IMP Study Group
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-09-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.1000787/full
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author Javier E. Cañada-García
Natalin Grippo
Natalin Grippo
Eva Ramírez de Arellano
Verónica Bautista
Noelia Lara
Ana María Navarro
Teresa Cabezas
Nora Mariela Martínez-Ramírez
Silvia García-Cobos
Jorge Calvo
Jorge Calvo
Emilia Cercenado
Emilia Cercenado
Belén Aracil
Belén Aracil
María Pérez-Vázquez
María Pérez-Vázquez
Jesús Oteo-Iglesias
Jesús Oteo-Iglesias
the Spanish IMP Study Group
author_facet Javier E. Cañada-García
Natalin Grippo
Natalin Grippo
Eva Ramírez de Arellano
Verónica Bautista
Noelia Lara
Ana María Navarro
Teresa Cabezas
Nora Mariela Martínez-Ramírez
Silvia García-Cobos
Jorge Calvo
Jorge Calvo
Emilia Cercenado
Emilia Cercenado
Belén Aracil
Belén Aracil
María Pérez-Vázquez
María Pérez-Vázquez
Jesús Oteo-Iglesias
Jesús Oteo-Iglesias
the Spanish IMP Study Group
author_sort Javier E. Cañada-García
collection DOAJ
description ObjectivesLittle is known about IMP-producing Enterobacterales (IMP-Ent) in Europe. We analyzed at genomic and phenotypic level IMP-Ent isolates circulating in Spain in a 9-year period.Materials and methodsIMP-Ent isolates submitted to our reference laboratory were included. Antibiotic susceptibility was performed using microdilution method (EUCAST), and IMP-carbapenemase activity was measured with carbapenemase inhibitors, the β-CARBA method, the modified Hodge test (MHT), and the modified carbapenemase inhibition method (mCIM). All isolates collected were sequenced for high-resolution single-nucleotide polymorphism (SNP) typing, core genome multilocus sequence typing (cgMLST), and resistome analysis.ResultsFifty IMP-Ent isolates, collected from 19 hospitals in 13 Spanish provinces, were detected: Klebsiella pneumoniae (IMP-Kpn) (24; 48%), Enterobacter roggenkampii (13; 26%), Enterobacter hormaechei (8, 16%), Klebsiella oxytoca (two; 4%), Enterobacter asburiae (one, 2%), Serratia marcescens (one; 2%) and Escherichia coli (one; 2%). All isolates were positive by the MHT and β-CARBA tests; 48 (96%) were mCIM positive; 12 (24%) and 26 (52%) displayed positive inhibition with dipicolinic (meropenem) and EDTA (ertapenem), respectively. Five IMP-carbapenemase types were identified: IMP-8 (22; 44%), IMP-22 (17; 34%), IMP-13 (7; 14%), IMP-28 (two; 4%), and IMP-15 (two; 4%), predominating IMP-8 in K. pneumoniae and IMP-22 in E. roggenkampii. IMP-28 was exclusively identified in K. oxytoca and IMP-15 in E. hormaechei. Predominant STs were ST405 (29.2%), ST15 (25%) and ST464 (20.8%) in IMP-Kpn; ST96 (100%) in E. roggenkampii and ST182 (62.5%) in E. hormachei. Colistin and amikacin were the most active non-carbapenem antibiotics against IMP-Ent.ConclusionIMP-Ent isolates remain infrequent in Spain, although in recent years have been circulating causing nosocomial outbreaks, being IMP-8-producing K. pneumoniae and IMP-22-producing E. roggenkampii the most frequently detected in this study. Inhibition with EDTA or dipicolinic acid presented false negative results in some IMP-producing strains. Active microbiological and molecular surveillance is essential for a better comprehension and control of IMP-Ent dissemination.
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spelling doaj.art-3ea51fc53d5e498b8cf071edccc7fa452023-11-23T16:53:19ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-09-011310.3389/fmicb.2022.10007871000787Phenotypic and molecular characterization of IMP-producing Enterobacterales in Spain: Predominance of IMP-8 in Klebsiella pneumoniae and IMP-22 in Enterobacter roggenkampiiJavier E. Cañada-García0Natalin Grippo1Natalin Grippo2Eva Ramírez de Arellano3Verónica Bautista4Noelia Lara5Ana María Navarro6Teresa Cabezas7Nora Mariela Martínez-Ramírez8Silvia García-Cobos9Jorge Calvo10Jorge Calvo11Emilia Cercenado12Emilia Cercenado13Belén Aracil14Belén Aracil15María Pérez-Vázquez16María Pérez-Vázquez17Jesús Oteo-Iglesias18Jesús Oteo-Iglesias19the Spanish IMP Study GroupLaboratorio de Referencia e Investigación en Resistencia a Antibióticos e Infecciones Relacionadas con la Asistencia Sanitaria, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Madrid, SpainLaboratorio de Referencia e Investigación en Resistencia a Antibióticos e Infecciones Relacionadas con la Asistencia Sanitaria, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Madrid, SpainCentro de Educación Médica e Investigaciones Clínicas “Norberto Quirno”, Buenos Aires, ArgentinaLaboratorio de Referencia e Investigación en Resistencia a Antibióticos e Infecciones Relacionadas con la Asistencia Sanitaria, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Madrid, SpainLaboratorio de Referencia e Investigación en Resistencia a Antibióticos e Infecciones Relacionadas con la Asistencia Sanitaria, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Madrid, SpainLaboratorio de Referencia e Investigación en Resistencia a Antibióticos e Infecciones Relacionadas con la Asistencia Sanitaria, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Madrid, SpainLaboratorio de Referencia e Investigación en Resistencia a Antibióticos e Infecciones Relacionadas con la Asistencia Sanitaria, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Madrid, SpainServicio de Microbiología, Hospital de Poniente, Almería, SpainServicio de Microbiología, Hospital Universitario de Guadalajara, Guadalajara, SpainLaboratorio de Referencia e Investigación en Resistencia a Antibióticos e Infecciones Relacionadas con la Asistencia Sanitaria, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Madrid, SpainCIBER de Enfermedades Infecciosas (CIBERINFEC), Spanish Network for Research in Infectious Diseases (REIPI), Instituto de Salud Carlos III, Madrid, SpainServicio de Microbiología, Hospital Universitario Marqués de Valdecilla, Santander, SpainServicio de Microbiología, Hospital Universitario Gregorio Marañón, Madrid, SpainCIBER de Enfermedades Respiratorias (CIBERES), Instituto de Salud Carlos III, Madrid, SpainLaboratorio de Referencia e Investigación en Resistencia a Antibióticos e Infecciones Relacionadas con la Asistencia Sanitaria, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Madrid, SpainCIBER de Enfermedades Infecciosas (CIBERINFEC), Spanish Network for Research in Infectious Diseases (REIPI), Instituto de Salud Carlos III, Madrid, SpainLaboratorio de Referencia e Investigación en Resistencia a Antibióticos e Infecciones Relacionadas con la Asistencia Sanitaria, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Madrid, SpainCIBER de Enfermedades Infecciosas (CIBERINFEC), Spanish Network for Research in Infectious Diseases (REIPI), Instituto de Salud Carlos III, Madrid, SpainLaboratorio de Referencia e Investigación en Resistencia a Antibióticos e Infecciones Relacionadas con la Asistencia Sanitaria, Centro Nacional de Microbiología, Instituto de Salud Carlos III, Madrid, SpainCIBER de Enfermedades Infecciosas (CIBERINFEC), Spanish Network for Research in Infectious Diseases (REIPI), Instituto de Salud Carlos III, Madrid, SpainObjectivesLittle is known about IMP-producing Enterobacterales (IMP-Ent) in Europe. We analyzed at genomic and phenotypic level IMP-Ent isolates circulating in Spain in a 9-year period.Materials and methodsIMP-Ent isolates submitted to our reference laboratory were included. Antibiotic susceptibility was performed using microdilution method (EUCAST), and IMP-carbapenemase activity was measured with carbapenemase inhibitors, the β-CARBA method, the modified Hodge test (MHT), and the modified carbapenemase inhibition method (mCIM). All isolates collected were sequenced for high-resolution single-nucleotide polymorphism (SNP) typing, core genome multilocus sequence typing (cgMLST), and resistome analysis.ResultsFifty IMP-Ent isolates, collected from 19 hospitals in 13 Spanish provinces, were detected: Klebsiella pneumoniae (IMP-Kpn) (24; 48%), Enterobacter roggenkampii (13; 26%), Enterobacter hormaechei (8, 16%), Klebsiella oxytoca (two; 4%), Enterobacter asburiae (one, 2%), Serratia marcescens (one; 2%) and Escherichia coli (one; 2%). All isolates were positive by the MHT and β-CARBA tests; 48 (96%) were mCIM positive; 12 (24%) and 26 (52%) displayed positive inhibition with dipicolinic (meropenem) and EDTA (ertapenem), respectively. Five IMP-carbapenemase types were identified: IMP-8 (22; 44%), IMP-22 (17; 34%), IMP-13 (7; 14%), IMP-28 (two; 4%), and IMP-15 (two; 4%), predominating IMP-8 in K. pneumoniae and IMP-22 in E. roggenkampii. IMP-28 was exclusively identified in K. oxytoca and IMP-15 in E. hormaechei. Predominant STs were ST405 (29.2%), ST15 (25%) and ST464 (20.8%) in IMP-Kpn; ST96 (100%) in E. roggenkampii and ST182 (62.5%) in E. hormachei. Colistin and amikacin were the most active non-carbapenem antibiotics against IMP-Ent.ConclusionIMP-Ent isolates remain infrequent in Spain, although in recent years have been circulating causing nosocomial outbreaks, being IMP-8-producing K. pneumoniae and IMP-22-producing E. roggenkampii the most frequently detected in this study. Inhibition with EDTA or dipicolinic acid presented false negative results in some IMP-producing strains. Active microbiological and molecular surveillance is essential for a better comprehension and control of IMP-Ent dissemination.https://www.frontiersin.org/articles/10.3389/fmicb.2022.1000787/fullantimicrobial resistant bacteriacarbapenem resistancewhole genome sequencingsurveillanceIMP carbapenemaseEnterobacterales
spellingShingle Javier E. Cañada-García
Natalin Grippo
Natalin Grippo
Eva Ramírez de Arellano
Verónica Bautista
Noelia Lara
Ana María Navarro
Teresa Cabezas
Nora Mariela Martínez-Ramírez
Silvia García-Cobos
Jorge Calvo
Jorge Calvo
Emilia Cercenado
Emilia Cercenado
Belén Aracil
Belén Aracil
María Pérez-Vázquez
María Pérez-Vázquez
Jesús Oteo-Iglesias
Jesús Oteo-Iglesias
the Spanish IMP Study Group
Phenotypic and molecular characterization of IMP-producing Enterobacterales in Spain: Predominance of IMP-8 in Klebsiella pneumoniae and IMP-22 in Enterobacter roggenkampii
Frontiers in Microbiology
antimicrobial resistant bacteria
carbapenem resistance
whole genome sequencing
surveillance
IMP carbapenemase
Enterobacterales
title Phenotypic and molecular characterization of IMP-producing Enterobacterales in Spain: Predominance of IMP-8 in Klebsiella pneumoniae and IMP-22 in Enterobacter roggenkampii
title_full Phenotypic and molecular characterization of IMP-producing Enterobacterales in Spain: Predominance of IMP-8 in Klebsiella pneumoniae and IMP-22 in Enterobacter roggenkampii
title_fullStr Phenotypic and molecular characterization of IMP-producing Enterobacterales in Spain: Predominance of IMP-8 in Klebsiella pneumoniae and IMP-22 in Enterobacter roggenkampii
title_full_unstemmed Phenotypic and molecular characterization of IMP-producing Enterobacterales in Spain: Predominance of IMP-8 in Klebsiella pneumoniae and IMP-22 in Enterobacter roggenkampii
title_short Phenotypic and molecular characterization of IMP-producing Enterobacterales in Spain: Predominance of IMP-8 in Klebsiella pneumoniae and IMP-22 in Enterobacter roggenkampii
title_sort phenotypic and molecular characterization of imp producing enterobacterales in spain predominance of imp 8 in klebsiella pneumoniae and imp 22 in enterobacter roggenkampii
topic antimicrobial resistant bacteria
carbapenem resistance
whole genome sequencing
surveillance
IMP carbapenemase
Enterobacterales
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.1000787/full
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