Brief report
Molecular epidemiology of carbapenemase-producing Enterobacteriaceae infection/colonisation in a hospital in Madrid
Epidemiología molecular de las infecciones/colonizaciones por enterobacterias productoras de carbapenemasas en un hospital de Madrid
Patricia Brañas
, Marta Gil, Jennifer Villa, María Ángeles Orellana, Fernando Chaves
Corresponding author
Servicio de Microbiología Clínica, Hospital Universitario 12 de Octubre, Madrid, Spain
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(c) Abundant pigmented chlamydoconidia (10í); insert: magnification of a chlamydoconidium (scale bar: 10<span class="elsevierStyleHsp" style=""></span>α/4m). (d) Globose picnidium (scale bar: 50<span class="elsevierStyleHsp" style=""></span>α/4m), showing three ostiolae (arrows). (e) Polymorphic cells of the picnidium wall (scale bar: 10<span class="elsevierStyleHsp" style=""></span>α/4m). 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Subscript: other species: 4 <span class="elsevierStyleItalic">C. freundii</span> (3 KPC, 1 VIM), 2 <span class="elsevierStyleItalic">E. coli</span> (2 VIM), 2 <span class="elsevierStyleItalic">K. oxytoca</span> (1 OXA-48, 1 KPC), 1 <span class="elsevierStyleItalic">P. mirabilis</span> (OXA-48) and 1 <span class="elsevierStyleItalic">S. marcescens</span> (VIM).</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Multi-resistant bacteria infections are one of the main public health problems and in our centre, the most important infections are caused by carbapenemase-producing Enterobacteriaceae (CPE).<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">1</span></a> In Europe, and specifically in Spain, OXA-48-like carbapenemase is the most frequent strain and is especially relevant in <span class="elsevierStyleItalic">Klebsiella pneumoniae (K. pneumoniae).</span><a class="elsevierStyleCrossRefs" href="#bib0060"><span class="elsevierStyleSup">2,3</span></a> The increase in the number of CPE infections/colonisations has been caused, to a great extent, by the dissemination of epidemic clones, as in the case of <span class="elsevierStyleItalic">K. pneumoniae.</span><a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">4</span></a> An earlier study conducted in our hospital (2009–2014) showed the emergence of carbapenemase producing <span class="elsevierStyleItalic">K. pneumoniae</span>, mainly due to the dissemination of an ST11 clone.<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">5</span></a> Following on from this, the need arose to determine the molecular epidemiology of CPE colonisations/infections in our hospital and to investigate whether some high-risk clones persist.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Material and methods</span><p id="par0010" class="elsevierStylePara elsevierViewall">The study included all CPE isolates from February 2015 to March 2016 at the University Hospital 12 de Octubre (Madrid). Only 1 isolate per patient was included. Identification was carried out using the MALDI-TOF MS system (Microflex, Bruker Daltonics, Bremen, Germany). Antibiotic sensitivity testing was performed using the microdilution method (Neg Combo Panel Type 53 and Neg Urine Combo Panel Type 59, Microscan Walkaway, Soria Melguizo, Madrid, Spain) and the interpretation criteria of the European Committee on Antimicrobial Susceptibility Testing (EUCAST version 5.0, 2015) were applied to determine sensitivity to antibiotics. The modified Hodge test was performed on isolates with suspected carbapenemase and the exact MIC for carbapenems (ertapenem, imipenem and meropenem) and colistin was determined using the E-test (Biomérieux, Durham, NC). Isolates that were positive for carbapenemase using the Hodge test underwent real-time PCR testing using specific primers directed against the <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">OXA-48</span>, <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">VIM</span> and <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">KPC</span><a class="elsevierStyleCrossRefs" href="#bib0080"><span class="elsevierStyleSup">6–8</span></a> genes, which are the most frequent carbapenemase types in Spain. Sequencing was performed using the BigDye 3.1 system (3130 Genetic Analyzer, Applied Biosystems, Austin, TX) in representative samples of each type of carbapenemase to confirm the results obtained by PCR.</p><p id="par0015" class="elsevierStylePara elsevierViewall">All strains of <span class="elsevierStyleItalic">Enterobacter cloacae (E. cloacae)</span> and a representative selection of strains of <span class="elsevierStyleItalic">K. pneumoniae</span> were studied to determine the epidemiological link between isolates from all hospital departments over the study period. Pulsed field gel electrophoresis (PFGE) was performed after digestion with the XbaI enzyme using the CHEF DRIII system (Bio-Rad Laboratories, Hercules, CA). The different band patterns were analysed using the Bionumerics software package v.3.0 (Applied Maths NV, Sint-Martens-Latem, Belgium).</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Results</span><p id="par0020" class="elsevierStylePara elsevierViewall">During the 14 months of the study, a total of 213 CPE isolates were identified, 139 (65.3%) from clinical samples (urine [No.<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>81], exudate/wound pus [No.<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>24], blood [No.<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>13], respiratory [No.<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>11], organic liquid [No.<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>6], catheter [No.<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>3] and biopsy [No.<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>1]) and 74 (34.7%) from surveillance culture samples from multi-resistant bacteria carriers (perianal exudates). The isolates belonged to seven bacterial species: <span class="elsevierStyleItalic">K. pneumoniae</span> (78.9%), <span class="elsevierStyleItalic">E. cloacae</span> (16.4%), <span class="elsevierStyleItalic">Citrobacter freundii</span>–<span class="elsevierStyleItalic">C. freundii</span>–(1.9%), <span class="elsevierStyleItalic">Klebsiella oxytoca</span>–<span class="elsevierStyleItalic">K. oxytoca</span>–(0.9%), <span class="elsevierStyleItalic">Escherichia coli</span>–<span class="elsevierStyleItalic">E. coli</span>–(0.9%), <span class="elsevierStyleItalic">Serratia marcescens</span>–<span class="elsevierStyleItalic">S. marcescens</span>–(0.5%) and <span class="elsevierStyleItalic">Proteus mirabilis</span>–<span class="elsevierStyleItalic">P. mirabilis</span>–(0.5%) (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>, panel A). The percentage of CPE with respect to the total number of isolates, by species, was: <span class="elsevierStyleItalic">K. pneumoniae</span> 4.9% (168/3404), <span class="elsevierStyleItalic">E. cloacae</span> 4.2% (35/841), <span class="elsevierStyleItalic">C. freundii</span> 3.1% (4/127), <span class="elsevierStyleItalic">K. oxytoca</span> 0.4% (2/480), <span class="elsevierStyleItalic">S. marcescens</span> 0.2% (1/472), <span class="elsevierStyleItalic">P. mirabilis</span> 0.1% (1/864) and <span class="elsevierStyleItalic">E. coli</span> 0.02% (2/11<span class="elsevierStyleHsp" style=""></span>298). Nearly all (94.4%) (201/213) of patients infected/colonised by these bacteria were adults, admitted to the following hospital departments: ICU (29.9%), A&E (16.5%), Internal Medicine (12.4%), Surgery (11.3%), Nephrology/Urology (9.8%) and other departments (11.3%); 8.8% were referred from Primary Care. In the case of paediatric patients (5.4%), the largest number of CPEs (9/12) were isolated from patients in the paediatric ICU. The cases occurred at an increasing rate over the entire study period (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>, panel B).</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0025" class="elsevierStylePara elsevierViewall">With regard to the type of carbapenemase detected, 91.1% (153/168) of the <span class="elsevierStyleItalic">K pneumoniae</span> isolates were OXA-48-like producers, 4.8% were VIM producers (8/168), 3.6% were KPC producers (6/168) and 0.6% (1/168) were VIM and KPC co-producers. Regarding <span class="elsevierStyleItalic">E. cloacae</span>, 71.4% were VIM producers (25/35), 14.3% were KPC producers (5/35), 11.4% were OXA-48 producers (4/35) and 2.9% (1/35) were VIM and KPC co-producers (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>, panel A).</p><p id="par0030" class="elsevierStylePara elsevierViewall">Regarding antimicrobial sensitivity testing, meropenem was the most active carbapenem, with an overall resistance of 23% among CPEs (20.8% and 34.3% in <span class="elsevierStyleItalic">K. pneumoniae</span> and <span class="elsevierStyleItalic">E. cloacae</span>, respectively) (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). Analysing carbapenemase by type showed that the KPC-producing strains presented the highest percentage of carbapenem resistance (ertapenem, imipenem and meropenem: 100%, 50% and 50% in <span class="elsevierStyleItalic">K. pneumoniae</span> and 100%, 80% and 80% in <span class="elsevierStyleItalic">E. cloacae</span>, respectively). The percentages of resistance to the remaining antibiotics are shown in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>.</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0035" class="elsevierStylePara elsevierViewall">Seventy four isolates were selected for the molecular typing study, 39<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">K. pneumoniae</span> (36 OXA-48-like, 2 VIM and 1 KPC) and 35 <span class="elsevierStyleItalic">E. cloacae</span> (25 VIM, 5 KPC, 4 OXA-48 and 1 VIM-KPC). In the case of <span class="elsevierStyleItalic">K. pneumoniae</span>, the analysis revealed the presence of 9 clonal types, 5 patterns were found in 89.7% (35/39) of the isolates with a predominant clone (clone A) and 4 showed a unique pattern. Clone A included 18 OXA-48-producing and 2 VIM-producing isolates and was found in patients admitted to 4 departments (ICU, Surgery, Internal Medicine and A&E) and also in primary care patients. The comparison of PFGE patterns with those included in our laboratory database allowed us to identify clone A as the predominant clone in the 2009–2014 period in our hospital as well. This clone had previously been identified as ST11 (JNHB00000000). The PFGE study in <span class="elsevierStyleItalic">E. cloacae</span> revealed the presence of 16 clonal types; 24 isolates corresponded to 5 clonal types and 11 showed a unique pattern.</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Discussion</span><p id="par0040" class="elsevierStylePara elsevierViewall">Resistance to beta-lactam antibiotics in Enterobacteriaceae has increased dramatically in recent years, mainly due to the increase in carbapenemase-producing strains.<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">9</span></a> Our results show that up to 7 different species of Enterobacteriaceae are producers of these enzymes, most notably OXA-48 <span class="elsevierStyleItalic">K. peumoniae</span>. A multicentre study conducted in 2013 reported up to 9 species of CPE, the most common being OXA-48-producing <span class="elsevierStyleItalic">K. pneumoniae</span>.<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">2</span></a></p><p id="par0045" class="elsevierStylePara elsevierViewall">The molecular epidemiology study shows different patterns of CPE dissemination in our hospital. On the one hand, the emergence and spread of <span class="elsevierStyleItalic">K. pneumoniae</span> occurs as a result of a few, predominantly OXA-48-producing clones. The appearance of high epidemic risk clones, such as carbapenemase-producing <span class="elsevierStyleItalic">K. pneumoniae</span> ST11, aggravates the problem, since this clone is widely distributed in Spain and in other European countries and can contain different types of carbapenemase in addition to multiple resistance to other antimicrobial groups.<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">4</span></a> In our hospital, it was first identified in 2011 in a VIM-1-producing strain. From then on, it extended to all clinical departments but as of 2012, most of the isolates were OXA-48 producers.<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">5</span></a> Our results confirm the persistence of this clone and its wide distribution throughout the hospital. Despite considerable efforts to control the spread of this type of infection, it is now endemic to our institution. In contrast, <span class="elsevierStyleItalic">E. cloacae</span> showed a very different pattern, since 16 clonal types with no predominant pattern were identified. In addition, most isolates (71.4%) were VIM producers, suggesting that the genes encoding this type of carbapenemase may be transmitted horizontally between strains of this species.</p><p id="par0050" class="elsevierStylePara elsevierViewall">It is important to be familiar with the drug resistance pattern in order to optimise empirical antimicrobial therapy in these patients. Our study shows that meropenem is the most active <span class="elsevierStyleItalic">in vitro</span> carbapenem in all isolated species and for all types of carbapenemase. It also reveals the high rates of resistance to aminoglycosides, fluoroquinolones and cotrimoxazole and especially to colistin (25%) and tigecycline (34.6%), two antibiotics used almost exclusively as rescue treatment for infection by these bacteria. A study conducted in 83 Spanish hospitals in 2013 found that among the CPE strains characterised, 4.5% were resistant to colistin and 29% to tigecycline.<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">2</span></a> It is striking to note the growing colistin resistance in <span class="elsevierStyleItalic">K. pneumoniae</span> observed in our hospital, which has increased from 2.1% in 2011–2014<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">5</span></a> to 27.4% in 2015–2016. This is a sign of the increased resistance to this antibiotic in this species.</p><p id="par0055" class="elsevierStylePara elsevierViewall">Our results also provide useful information regarding the possible use of new antibiotics, such as ceftazidime–avibactam in the treatment of CPE infections. This combination may play an important role in the treatment of some of these bacteria, since it is potentially active against OXA-48- and KPC-producing strains,<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">10</span></a> although <span class="elsevierStyleItalic">in vitro</span> sensitivity to this new antimicrobial must be confirmed in each case.</p><p id="par0060" class="elsevierStylePara elsevierViewall">This study has certain limitations. First, the microdilution panels used to perform the CPE antibiogram contained only imipenem and ertapenem, the latter at concentrations higher than those recommended for suspected carbapenemase production, so some CPEs might not have been identified. In addition, only OXA-48, VIM and KPC PCR were performed, as these are the most common carbapenemases in Spain. Finally, the <span class="elsevierStyleItalic">K. pneumoniae</span> PFGE study did not include all the isolates, only a representative sample, so it is likely that not all circulating clones in our hospital were detected.</p><p id="par0065" class="elsevierStylePara elsevierViewall">Despite this, the study raises awareness of the serious problem of multi-resistant microorganisms. CPE infections have spread beyond the limits of our departments and the hospital itself to different types of patients and clinical settings. While we await the development of new antibiotics, it is important to review and intensify control measures and to update policies designed to encourage prudent use of antibiotics in hospitals and other care settings.</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Conflicts of interest</span><p id="par0070" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:10 [ 0 => array:3 [ "identificador" => "xres986146" "titulo" => "Abstract" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Introduction" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Material and methods" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Results" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Conclusions" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec953777" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres986147" "titulo" => "Resumen" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0025" "titulo" => "Introducción" ] 1 => array:2 [ "identificador" => "abst0030" "titulo" => "Material y métodos" ] 2 => array:2 [ "identificador" => "abst0035" "titulo" => "Resultados" ] 3 => array:2 [ "identificador" => "abst0040" "titulo" => "Conclusiones" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec953778" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:2 [ "identificador" => "sec0010" "titulo" => "Material and methods" ] 6 => array:2 [ "identificador" => "sec0015" "titulo" => "Results" ] 7 => array:2 [ "identificador" => "sec0020" "titulo" => "Discussion" ] 8 => array:2 [ "identificador" => "sec0025" "titulo" => "Conflicts of interest" ] 9 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2016-08-09" "fechaAceptado" => "2016-10-05" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec953777" "palabras" => array:5 [ 0 => "Enterobacteria" 1 => "Carbapenemases" 2 => "<span class="elsevierStyleItalic">Klebsiella pneumoniae</span>" 3 => "OXA-48" 4 => "Molecular epidemiology" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec953778" "palabras" => array:5 [ 0 => "Enterobacterias" 1 => "Carbapenemasas" 2 => "<span class="elsevierStyleItalic">Klebsiella pneumoniae</span>" 3 => "OXA-48" 4 => "Epidemiología molecular" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:3 [ "titulo" => "Abstract" "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Introduction</span><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">A description is presented on the molecular epidemiology of carbapenemase-producing enterobacteriaceae infection in a tertiary hospital.</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Material and methods</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">A study was made on all the carbapenemase-producing enterobacteriaceae isolations obtained between February 2015 and March 2016 in the Hospital Universitario 12 de Octubre (Madrid). Phenotypic and molecular methods were used.</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">A total of 7 bacterial species were identified, with the majority being <span class="elsevierStyleItalic">Klebsiella pneumoniae (K. pneumoniae)</span> (78.9%) and <span class="elsevierStyleItalic">Enterobacter cloacae (E. cloacae)</span> (16.4%). The resistance of <span class="elsevierStyleItalic">K. pneumoniae</span> and <span class="elsevierStyleItalic">E. cloacae</span> for carbapenems was 88.7 and 88.6% for ertapenem, 21.4 and 54.3% for imipenem, and 20.8 and 34.3% for meropenem, respectively. The most frequent carbapenemase type was OXA-48 (91.1%) and VIM (71.4%) in <span class="elsevierStyleItalic">E. cloacae</span>. A total of 9 <span class="elsevierStyleItalic">K. pneumoniae</span> clonal types were identified, including a majority pertaining to the sequence type ST11. In <span class="elsevierStyleItalic">E. cloacae</span>, 16 clonal types were identified.</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Conclusions</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">The current increase in carbapenemase-producing enterobacteriaceae is mainly due to the spread of OXA-48-producing <span class="elsevierStyleItalic">K. pneumoniae</span>.</p></span>" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Introduction" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Material and methods" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Results" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Conclusions" ] ] ] "es" => array:3 [ "titulo" => "Resumen" "resumen" => "<span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Introducción</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Se describe la epidemiología molecular de las enterobacterias productoras de carbapenemasas en un hospital terciario.</p></span> <span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Material y métodos</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Se incluyeron todos los aislamientos de enterobacterias productoras de carbapenemasas obtenidos entre febrero de 2015 y marzo de 2016 en el Hospital Universitario 12 de Octubre (Madrid). Se utilizaron métodos fenotípicos y moleculares.</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Se identificaron 7 especies bacterianas, predominando <span class="elsevierStyleItalic">Klebsiella pneumoniae (K. pneumoniae)</span> (78,9%) y <span class="elsevierStyleItalic">Enterobacter cloacae</span> (<span class="elsevierStyleItalic">E. cloacae)</span> (16,4%). La resistencia en <span class="elsevierStyleItalic">K. pneumoniae</span> y <span class="elsevierStyleItalic">E. cloacae</span> para carbapenemes fue del 88,7 y 88,6% para ertapenem, 21,4 y 54,3% para imipenem, y 20,8 y 34,3% para meropenem. El tipo de carbapenemasa más frecuente en <span class="elsevierStyleItalic">K pneumoniae</span> fue OXA-48 (91,1%) y en <span class="elsevierStyleItalic">E. cloacae</span> VIM (71,4%). Se identificaron 9 tipos clonales de <span class="elsevierStyleItalic">K. pneumoniae</span>, incluyendo uno mayoritario perteneciente al tipo de secuencia ST11, y 16 de <span class="elsevierStyleItalic">E. cloacae</span>.</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusiones</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">El incremento actual de enterobacterias productoras de carbapenemasas se debe en gran medida a la diseminación de <span class="elsevierStyleItalic">K. pneumoniae</span> productora de OXA-48.</p></span>" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0025" "titulo" => "Introducción" ] 1 => array:2 [ "identificador" => "abst0030" "titulo" => "Material y métodos" ] 2 => array:2 [ "identificador" => "abst0035" "titulo" => "Resultados" ] 3 => array:2 [ "identificador" => "abst0040" "titulo" => "Conclusiones" ] ] ] ] "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "<p class="elsevierStyleNotepara" id="npar0010">Please cite this article as: Brañas P, Gil M, Villa J, Orellana MÁ, Chaves F. Epidemiología molecular de las infecciones/colonizaciones por enterobacterias productoras de carbapenemasas en un hospital de Madrid. Enferm Infecc Microbiol Clin. 2018;36:100–103.</p>" ] ] "multimedia" => array:2 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 2415 "Ancho" => 2143 "Tamanyo" => 273634 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Types of CPE and distribution over the study period. Subscript: other species: 4 <span class="elsevierStyleItalic">C. freundii</span> (3 KPC, 1 VIM), 2 <span class="elsevierStyleItalic">E. coli</span> (2 VIM), 2 <span class="elsevierStyleItalic">K. oxytoca</span> (1 OXA-48, 1 KPC), 1 <span class="elsevierStyleItalic">P. mirabilis</span> (OXA-48) and 1 <span class="elsevierStyleItalic">S. marcescens</span> (VIM).</p>" ] ] 1 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at1" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:2 [ "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Antibiotic (%) \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">All (No.<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>213)<a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a> \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">K. pneumoniae</span> (No.<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>168) \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">E. cloacae</span> (No.<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>35) \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Ertapenem \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">86.8 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">88.7 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">88.6 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Imipenem \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">28.1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">21.4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">54.3 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Meropenem \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">23.0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">20.8 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">34.3 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Gentamicin \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">55.0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">56.0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">54.0 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Tobramycin \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">81.0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">82.0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">80.0 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Amikacin \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">15.2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">15.9 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">9.1 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Fluoroquinolones \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">88.0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">91.0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">80.0 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Co-trimoxazole \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">71.3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">71.4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">69.0 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Tigecycline \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">34.6 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">41.1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">9.1 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top">Colistin \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">25.0 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">27.4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">20.0 \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1673963.png" ] ] ] "notaPie" => array:1 [ 0 => array:3 [ "identificador" => "tblfn0005" "etiqueta" => "a" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Including <span class="elsevierStyleItalic">C. freundii</span> (No.<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>4), <span class="elsevierStyleItalic">E. coli</span> (No.<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>2), <span class="elsevierStyleItalic">K. oxytoca</span> (No.<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>2), <span class="elsevierStyleItalic">P. mirabilis</span> (No.<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>1) and <span class="elsevierStyleItalic">S. marcescens</span> (No.<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>1).</p>" ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">Pattern of CPE antibiotic resistance.</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0015" "bibliografiaReferencia" => array:10 [ 0 => array:3 [ "identificador" => "bib0055" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Combating the spread of carbapenemases in Enterobacteriaceae: a battle that infection prevention should not lose" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "P. 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| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 November | 1 | 1 | 2 |
| 2024 October | 10 | 5 | 15 |
| 2024 September | 26 | 6 | 32 |
| 2024 August | 21 | 10 | 31 |
| 2024 July | 15 | 6 | 21 |
| 2024 June | 17 | 4 | 21 |
| 2024 May | 26 | 9 | 35 |
| 2024 April | 23 | 4 | 27 |
| 2024 March | 12 | 10 | 22 |
| 2024 February | 12 | 5 | 17 |
| 2024 January | 9 | 2 | 11 |
| 2023 December | 12 | 3 | 15 |
| 2023 November | 10 | 2 | 12 |
| 2023 October | 15 | 2 | 17 |
| 2023 September | 11 | 1 | 12 |
| 2023 August | 13 | 6 | 19 |
| 2023 July | 7 | 3 | 10 |
| 2023 June | 26 | 3 | 29 |
| 2023 May | 43 | 4 | 47 |
| 2023 April | 20 | 1 | 21 |
| 2023 March | 22 | 1 | 23 |
| 2023 February | 24 | 4 | 28 |
| 2023 January | 15 | 5 | 20 |
| 2022 December | 24 | 4 | 28 |
| 2022 November | 26 | 9 | 35 |
| 2022 October | 39 | 16 | 55 |
| 2022 September | 32 | 7 | 39 |
| 2022 August | 36 | 7 | 43 |
| 2022 July | 26 | 9 | 35 |
| 2022 June | 24 | 4 | 28 |
| 2022 May | 18 | 6 | 24 |
| 2022 April | 22 | 8 | 30 |
| 2022 March | 19 | 9 | 28 |
| 2022 February | 22 | 9 | 31 |
| 2022 January | 27 | 13 | 40 |
| 2021 December | 23 | 9 | 32 |
| 2021 November | 24 | 8 | 32 |
| 2021 October | 20 | 7 | 27 |
| 2021 September | 16 | 10 | 26 |
| 2021 August | 67 | 6 | 73 |
| 2021 July | 29 | 11 | 40 |
| 2021 June | 29 | 7 | 36 |
| 2021 May | 19 | 13 | 32 |
| 2021 April | 45 | 11 | 56 |
| 2021 March | 17 | 7 | 24 |
| 2021 February | 13 | 7 | 20 |
| 2021 January | 16 | 12 | 28 |
| 2020 December | 21 | 9 | 30 |
| 2020 November | 33 | 9 | 42 |
| 2020 October | 25 | 10 | 35 |
| 2020 September | 28 | 10 | 38 |
| 2020 August | 38 | 9 | 47 |
| 2020 July | 17 | 10 | 27 |
| 2020 June | 14 | 8 | 22 |
| 2020 May | 30 | 15 | 45 |
| 2020 April | 19 | 6 | 25 |
| 2020 March | 20 | 3 | 23 |
| 2020 February | 37 | 15 | 52 |
| 2020 January | 41 | 5 | 46 |
| 2019 December | 37 | 12 | 49 |
| 2019 November | 26 | 11 | 37 |
| 2019 October | 27 | 6 | 33 |
| 2019 September | 28 | 2 | 30 |
| 2019 August | 25 | 4 | 29 |
| 2019 July | 27 | 5 | 32 |
| 2019 June | 34 | 20 | 54 |
| 2019 May | 62 | 22 | 84 |
| 2019 April | 11 | 10 | 21 |
| 2019 March | 6 | 2 | 8 |
| 2019 February | 13 | 2 | 15 |
| 2019 January | 10 | 3 | 13 |
| 2018 December | 17 | 1 | 18 |
| 2018 November | 10 | 2 | 12 |
| 2018 October | 7 | 3 | 10 |
| 2018 September | 9 | 0 | 9 |
| 2018 August | 4 | 0 | 4 |
| 2018 May | 2 | 0 | 2 |
| 2018 March | 2 | 0 | 2 |
| 2018 February | 20 | 0 | 20 |
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