Evolution of antibiotic multiresistance in Escherichia coli and Klebsiella pneumoniae isolates from urinary tract infections: A 12-year analysis (2003–2014) | Enfermedades Infecciosas y Microbiología Clínica

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Arana, Margarita Rubio, Juan-Ignacio Alós" "autores" => array:3 [ 0 => array:3 [ "nombre" => "David M." "apellidos" => "Arana" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 1 => array:3 [ "nombre" => "Margarita" "apellidos" => "Rubio" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] ] ] 2 => array:4 [ "nombre" => "Juan-Ignacio" "apellidos" => "Alós" "email" => array:1 [ 0 => "nachoalos@telefonica.net" ] "referencia" => array:3 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:2 [ "etiqueta" => "*" "identificador" => "cor0005" ] ] ] ] "afiliaciones" => array:2 [ 0 => array:3 [ "entidad" => "Servicio de Microbiología, Hospital Universitario de Getafe, Getafe, Madrid, Spain" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Facultad de Ciencias Biomédicas, Universidad Europea de Madrid, Villaviciosa de Odón, Madrid, Spain" "etiqueta" => "b" "identificador" => "aff0010" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Evolución de la multirresistencia a los antibióticos en Escherichia coli y Klebsiella pneumoniae aislados de infecciones del tracto urinario. Un análisis de 12 años (2003-2014)" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0015" "etiqueta" => "Fig. 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 2151 "Ancho" => 1539 "Tamanyo" => 183477 ] ] "descripcion" => array:1 [ "en" => "ESBL contribution to the MDR profile in E. coli (A) and K. pneumoniae (B) from both, community and hospitalized patients." ] ] ] "textoCompleto" => "IntroductionThe increasing rate of antibiotic resistance in uropathogens, especially in Escherichia coli and Klebsiella pneumoniae, as the most common etiologic agents of urinary tract infections (UTI), leads to difficulties in choosing adequate empirical therapy and achieving treatment success.Multiple studies regarding antibiotic susceptibility in uropathogens have been published in medical literature,<a class="elsevierStyleCrossRefs" href="#bib0155">1–4</a> but only a few studies have addressed the multidrug resistance (MDR) behaviour.<a class="elsevierStyleCrossRefs" href="#bib0175">5–7</a> According to a group of international experts from European Centre for Disease Prevention (ECDC) and Centers for Disease Control and Prevention (CDC) a standardized international definition for MDR was created. MDR is defined as acquired non-susceptibility to at least one agent in three or more antimicrobial categories.<a class="elsevierStyleCrossRef" href="#bib0190">8</a>MDR bacteria are more usually associated with nosocomial infections. A significant part of nosocomial infections are diagnosed as UTI (more than 30%) and a considerable part of the antimicrobial agents used in hospitals is dedicated for their treatment.<a class="elsevierStyleCrossRef" href="#bib0195">9</a> However, the vast majority of UTI come from outpatients, the most common being uncomplicated cystitis (infection of bladder) in women. The 2010 guidelines of the Infectious Diseases Society of America and the European Society for Microbiology and Infectious Diseases recommend for empirical treatment of acute uncomplicated cystitis trimethoprim–sulphamethoxazole (if the local resistance is less than 20%), nitrofurantoin, fosfomycin trometamol and pivmecillinam (as first-line therapy). Fluoroquinolones may be used only as alternative therapy and their use must be avoided to treat uncomplicated cystitis whenever possible.<a class="elsevierStyleCrossRef" href="#bib0200">10</a> MDR bacteria at the community level has increased, making the treatment of infections more difficult and requiring, in some cases, intravenous therapy because of the lack of oral options.<a class="elsevierStyleCrossRef" href="#bib0205">11</a>Several factors contribute to the increasing spread of MDR to antimicrobials. The overuse and misuse of antimicrobials inhuman medicine, in veterinary and in agriculture represent, among others, are some of the main factors involved in the selective pressure.In addition, MDR in urine isolates from the community is often associated with the presence of multiple extended-spectrum-β-lactamases (ESBL) genes, as well as aminoglycoside and quinolone resistance genes.<a class="elsevierStyleCrossRef" href="#bib0210">12</a>This study aims to identify MDR in the main enterobacteriaceae implicated as etiologic agents in UTI (E. coli and K. pneumoniae) from both, community and hospitalized patients, and to analyze the evolution over a 12-year period.MethodsStudy population and bacterial isolatesA 12-year (2003–2014) retrospective study was conducted in both hospitalized and non-hospitalized patients suspected of UTI at the Hospital Universitario de Getafe (Madrid). The hospital has 413–600 operational beds and an attended population of 211,000–260,000 inhabitants (depending on the year). During the period of the study, each urine sample was cultured using a 1μL calibrated loop in cysteine lactose electrolytes deficient (CLED) agar and incubated at 37°C for 18–24h. A growth of >104 colony-forming units (CFU) per mL of one type of organism were considered as a positive result. Identification and antibiotic susceptibilities were performed using a microdilution system (WIDER, Franscico Soria Melguizo, SA).Microb Dynamic software (Francisco SoriaMelguizo, SA) was used to analyze the microbiology laboratory database. It provides analysis of antimicrobial susceptibility and resistance test results according to the European Committee for Antimicrobial Susceptibility Testing (EUCAST) 2015 (version 5.0) clinical breakpoints (<a id="intr0005" class="elsevierStyleInterRef" href="http://www.eucast.org/">www.eucast.org</a>). The software was used to determine the prevalence of both MDR E. coli and K. pneumoniae. In order to avoid distortions in the final results, isolates from the same patient with different antibiotic susceptibility patterns were considered as different while isolates showing the same pattern were considered as unique.Statistical analysisA chi square test was applied to compare differences in group proportions in three different periods: 2003–2006, 2007–2010 and 2011–2014. Chi square test for trend was used to determine whether there was a statistically significant linear trend over the period of the study. A p-value <0.05 was considered as statistically significant. All statistical analyses were performed using Epi Info v. 7 (CDC, Atlanta, USA).Antimicrobial susceptibilityWe determined the proportion of isolates resistant to at least the antimicrobials agents that we chose as MDR markers (amoxicillin, gentamicin, ciprofloxacin and trimethoprim–sulphamethoxazole) according to their clinical antimicrobial MIC breakpoints: amoxicillin (MIC >8mg/L), ciprofloxacin (MIC >1mg/L), trimethoprim–sulphamethoxazole (MIC >4/76mg/L) and gentamicin (MIC >4mg/L). Amoxicillin is not considered in K. pneumoniae because of its intrinsic resistance. We also determined the global prevalence of ESBL producing E. coli and K. pneumoniae (MDR and non-MDR) and the proportion of both, MDR E. coli and MDR K. pneumoniae isolates harbouring ESBL. Positive results derived from ESBL producing enterobacteriaceae isolates are routinely introduced in the database when phenotypic studies are developed in the suspected ESBL producers.ResultsIn total, the laboratory counted 39,980 positive urine samples over the 12-year period. 34,564 positive urine samples (3786 from hospitalized patients and 30,778 from non-hospitalized patients) had E. coli as the infecting organism and 5,422 positive urine cultures (774 from hospitalized patients and 4,648 from non-hospitalized patients) had K. pneumoniae as the etiological organism.Prevalence and evolution of MDR profilesThe prevalence of UTI due to MDR E. coli (resistance at least to amoxicillin, ciprofloxacin, gentamicin and trimethoprim–sulphamethoxazole) in hospitalized patients increased from 5.89% [70 out of 1,188 isolates] in the period 2007–2010 to 8.18% [79 out of 966 isolates] in the period 2011–2014 (1.4-fold increase) (p=0.038). Similar results were observed in the same period when outpatient population was analyzed: 3.13% [332 out of 10,615 isolates] versus 4.58% [456 out of 9,947 isolates], respectively (p<0.001). No significant differences were observed between the first and the second periods of the study (2003–2006 and 2007–2010) (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>A).<elsevierMultimedia ident="fig0005"></elsevierMultimedia>However, the prevalence of UTI caused by MDR K. pneumoniae (resistance at least to ciprofloxacin, gentamicin and trimethoprim–sulphamethoxazole) suffered a more drastic change between 2007–2010 and 2011–2014. <a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>B shows a 4-fold increase in hospitalized patients (2.38% [6 out of 252 isolates] in 2007–2010 versus 9.35% [23 out of 246 isolates] in 2011–2014; p<0.001). This change in prevalence was even more pronounced (8-fold increase) when outpatient population was analyzed (0.47% [8 out of 1,689 isolates] in 2007–2010 versus 3.78% [67 out of 1,774 isolates] in 2011–2014; p<0.001) A slight but not significant increase was also observed between the first and second periods (2003–2006 versus 2007–2010) in both hospitalized and non-hospitalized patients (1.45% [4 out of 276 isolates] versus 2.38% [6 out of 252 isolates] and 0.08% [1 out of 1,185 isolates] versus 0.47% [8 out of 1,689 isolates] respectively) (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>B).Therefore, higher percentages of MDR E. coli in hospitalized patients with respect to outpatients (1.8-fold increase in all the time periods) were evident and maintained constant over time (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>A). Similar results were observed in the percentage of MDR K. pneumoniae isolates, but the differences with respect to the non-hospitalized patients were more marked (>1.8-fold increase in all the time periods) (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>B). It is important to note that the increase observed in the prevalence of MDR E. coli isolates is mainly due to the individual resistance to ciprofloxacin and gentamicin regardless of the patient hospitalization, while individual resistance to amoxicillin and trimethoprim–sulphamethoxazole remained stable during the period of the study (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>A).<elsevierMultimedia ident="fig0010"></elsevierMultimedia>By contrast, the increase in prevalence of MDR K. pneumoniae isolates is due to the individual resistance to ciprofloxacin, gentamicin and trimethoprim–sulphamethoxazole (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>B).ESBL contribution to the MDR profileThe global prevalence of UTI due to ESBL producing E. coli in hospitalized patients increased from 8.1% in the period 2003–2006 to 10.3% in the period 2011–2014 (1.27 fold-increase) while this increase in prevalence was more marked when non-hospitalized patients were analyzed (2.7% in 2003–2006 versus 5.7% in 2011–2014; 2 fold-increase).However, the rise in global prevalence of UTI due to ESBL producing K. pneumoniae in both, hospitalized and outpatients was more pronounced (6.1% in 2003–2006 versus 15% in 2011–2014; 2.4 fold-increase and 1.1% in 2003–2006 versus 5.5% in 2011–2014; 5 fold-increase, respectively). <a class="elsevierStyleCrossRefs" href="#tbl0005">Table 1</a> show an analysis for linear trend in ESBL-producing E. coli and ESBL-producing K. pneumoniae in hospitalized patients (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1A</a>) and non-hospitalized patients (<a class="elsevierStyleCrossRef" href="#tbl0010">Table 1B</a>) over the period of the study.<elsevierMultimedia ident="tbl0005"></elsevierMultimedia><elsevierMultimedia ident="tbl0010"></elsevierMultimedia>In order to determine the contribution of ESBL in the MDR phenotype of both K. pneumoniae and E. coli, Microb Dynamic software was used to analyze the percentage of MDR isolates harbouring an ESBL.The results show that the prevalence of UTI due to ESBL producing MDR E. coli in hospitalized patients increased from 0.86% in the period 2003–2006 to 3.11% in the period 2011–2014 (3.6 fold-increase) while this increase in prevalence was more marked, as above, when non-hospitalized patients were analyzed (0.18% in 2003–2006 versus 1.08% in 2011–2014; 6 fold-increase).By contrast, the prevalence of UTI due to ESBL producing MDR K. pneumoniae in hospitalized patients increased from 1.09% in the period 2003–2006 to 7.72% in the period 2011–2014 (7.6 fold-increase) while this increase in prevalence was more marked when non-hospitalized patients were analyzed (0.08% in 2003–2006 versus 2.82% in 2011–2014; 35.2 fold-increase). In hospitalized patients, 14 out of 70 (20%) MDR E. coli isolates were MDR ESBL-producing E. coli in 2007–2010. This percentage increased to 38% (30 out of 79) in 2011–2014 (p=0.016). However, the increase observed in non-hospitalized patients between the same periods was not as marked (18.2% in 2007–2010 to 23.6% in 2011–2014) (p=0.085) (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>A). The contribution of ESBL to the MDR K. pneumoniae isolated in hospitalized patients was 66.8% (4 out of 6) in 2007–2010; this percentage rose to 82.6% (19 out of 23) in 2011–2014 (p=0.77). The increase observed in non-hospitalized patients between the same periods was 51% (4 out of 8) in 2007–2010 to 74.6% (50 out of 67) in 2011–2014 (p=0.143) (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>B). The results indicate that the contribution of ESBL to the MDR behaviour was more pronounced in K. pneumoniae isolates. <a class="elsevierStyleCrossRefs" href="#tbl0015">Table 2</a> shows an analysis for linear trend in MDR E. coli and K. pneumoniae in hospitalized patients (<a class="elsevierStyleCrossRef" href="#tbl0015">Table 2A</a>) and MDR E. coli and K. pneumoniae in non-hospitalized patients (<a class="elsevierStyleCrossRef" href="#tbl0020">Table 2B</a>) over the period of the study.<elsevierMultimedia ident="fig0015"></elsevierMultimedia><elsevierMultimedia ident="tbl0015"></elsevierMultimedia><elsevierMultimedia ident="tbl0020"></elsevierMultimedia>Susceptibility to other antibiotics in MDR isolatesIn order to study the role of alternative antibiotic treatments in the MDR isolates, susceptibility to fosfomycin, meropenem and amoxicillin/clavulanate was analyzed. All the MDR E. coli isolates (from both, inpatients and outpatients) were sensitive to fosfomycin during the first 8 years (first and second periods). The proportion of susceptible isolates diminished during the last period (82% from inpatients and 86% from outpatients).In the same way, all the isolates studied were susceptible to meropenem (except one isolate of MDR K. pneumoniae from a hospitalized patient harbouring a carbapenemase OXA-48 in 2013).Susceptibility to amoxicillin/clavulanate decreased along the period of the study in both, MDR E. coli and MDR K. pneumoniae. Susceptibility to amoxicillin/clavulanate in MDR E. coli isolates from hospitalized patients decreased from 84.5% in the period 2003–2006 to 46.8% in the period 2011–2014 (1.8-fold decreased). Comparable results were obtained in the same period when outpatient population was analyzed: 86.6% versus 51.7% respectively. Susceptibility to amoxicillin/clavulanate in MDR K. pneumoniae suffered a more drastic change between 2003–2006 and 2011–2014. All the MDR K. pneumoniae isolates from hospitalized patients were resistant to amoxicillin/clavulanate in 2011–2014 respect to the first period (49.6% were susceptible). Susceptibility to amoxicillin/clavulanate in MDR K. pneumoniae isolates from outpatients decreased from 100% in the period 2003–2006 to 16.4% in the period 2011–2014 (6-fold decrease).DiscussionThe increase of bacterial resistance to antibiotics is a cause of global concern. Infections caused by multiresistant microorganisms frequently fail to respond to a suitable empirical therapy and often times, do not achieve treatment success.<a class="elsevierStyleCrossRef" href="#bib0215">13</a>Few studies have reported on the MDR patterns expressed by Gram negative uropathogens in both, hospitalized and non-hospitalized patients, and the evolution over time of such patterns.<a class="elsevierStyleCrossRefs" href="#bib0185">7,14–16</a> Some studies performed at community level have showed a high percentage (about 38%) of MDR in E. coli, the most prevalent bacteria involved in the community-acquired UTI<a class="elsevierStyleCrossRef" href="#bib0235">17</a> while, on the other hand, MDR-Klebsiella species are considered as one of the most common bacteria involved in nosocomial and urinary tract infections.<a class="elsevierStyleCrossRef" href="#bib0240">18</a>The goal of this work was to analyze the evolution of multidrug resistance in both, outpatients and inpatients, to antibiotics commonly used in the treatment of urinary tract infection over a 12-year period. As expected, MDR phenotypes were more usually associated with hospitalization, but the results show that MDR bacteria at the community level are increasing almost at the same rate as in hospitalized patients.The multiresistance could be associated with the high prescription of these antibiotics groups at community level in Spain.<a class="elsevierStyleCrossRefs" href="#bib0245">19,20</a>Quinolone resistance is frequently associated with ESBL-production, and according to the literature, CTX-M represent the most common ESBL produced among bacteria implicated in community-acquired UTI worldwide.<a class="elsevierStyleCrossRef" href="#bib0255">21</a> In our study, a high percentage of strains producing ESBL were detected in MDR isolates from both inpatients and outpatients. The prevalence of infection due to MDR ESBL-producing K. pneumoniae in non-hospitalized patients increased significantly during the last 8 years. On the other hand, exposure to penicillins and/or trimethoprim–sulfamethoxazole has been considered a risk factor for ESBL-producing E. coli isolation.<a class="elsevierStyleCrossRef" href="#bib0260">22</a> All of these results are in accordance with the results obtained in our study suggesting that resistance to quinolones and trimethoprim–sulphamethoxazole are associated with ESBL production. By contrast, this phenomenon was less marked in hospitalized patients.It is important to take into account that alternative therapies such as fosfomycin represent a promising treatment option against MDR urinary isolates. Fosfomycin resistance is usually rare in areas with limited use but it is increasing in countries with higher usage.<a class="elsevierStyleCrossRef" href="#bib0265">23</a> Our results show that all the MDR E. coli isolates were sensitive to fosfomycin during the first 8 years, but resistant isolates have emerged during the last years. By contrast all the MDR isolates were susceptible to carbapenems due to the absence of carbapenemases.The emergence and spread of different clones have to be taken into account in order to explain the increase in MDR bacteria. Numerous articles have reported that the well-known high-risk E. coli ST131 and K. pneumoniae ST258 clones have been responsible for the sudden increase in multidrug resistance.<a class="elsevierStyleCrossRefs" href="#bib0270">24–27</a> ST131 is responsible of UTI, frequently fluoroquinolone resistant and can be linked with the production of CTX-M-15,<a class="elsevierStyleCrossRef" href="#bib0290">28</a> while ST258 is also known to cause UTI, respiratory tract infections, and blood stream infections and is associated with carbapenemase production, most often KPC-2 and KPC-3.<a class="elsevierStyleCrossRef" href="#bib0295">29</a> Unfortunately, we do not have information about molecular characterization of the strains isolated in our study.It is also important to take into consideration that mobile elements (plasmids, transposons, integrons, etc.) play an important role in the transfer of other resistance genes and thus allowing a co-selection phenomenon (see for a review<a class="elsevierStyleCrossRef" href="#bib0300">30</a>).The present study has some limitations; it was conducted in an area (Getafe), which represents a small portion of the total population of Spain and, in this case, the results cannot be extrapolated to other settings because specific epidemiology of different areas have to be taken into consideration. Further studies would be necessary to address the problem at national and global level. Despite the above limitations, some strengths are also remarkable and include data of a large sample size of urinary strains isolated over a 12 year period that demonstrates that MDR is an increasing phenomenon of particular importance over the last few years.FundingNo specific funding has been received.Conflict of interestNone to declare." "textoCompletoSecciones" => array:1 [ "secciones" => array:11 [ 0 => array:3 [ "identificador" => "xres1012334" "titulo" => "Abstract" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Introduction" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Methods" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Results" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Conclusions" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec971498" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres1012333" "titulo" => "Resumen" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0025" "titulo" => "Introducción" ] 1 => array:2 [ "identificador" => "abst0030" "titulo" => "Métodos" ] 2 => array:2 [ "identificador" => "abst0035" "titulo" => "Resultados" ] 3 => array:2 [ "identificador" => "abst0040" "titulo" => "Conclusiones" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec971497" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:3 [ "identificador" => "sec0010" "titulo" => "Methods" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Study population and bacterial isolates" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "Statistical analysis" ] 2 => array:2 [ "identificador" => "sec0025" "titulo" => "Antimicrobial susceptibility" ] ] ] 6 => array:3 [ "identificador" => "sec0030" "titulo" => "Results" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0035" "titulo" => "Prevalence and evolution of MDR profiles" ] 1 => array:2 [ "identificador" => "sec0040" "titulo" => "ESBL contribution to the MDR profile" ] 2 => array:2 [ "identificador" => "sec0045" "titulo" => "Susceptibility to other antibiotics in MDR isolates" ] ] ] 7 => array:2 [ "identificador" => "sec0050" "titulo" => "Discussion" ] 8 => array:2 [ "identificador" => "sec0055" "titulo" => "Funding" ] 9 => array:2 [ "identificador" => "sec0060" "titulo" => "Conflict of interest" ] 10 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2015-10-30" "fechaAceptado" => "2016-02-20" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec971498" "palabras" => array:4 [ 0 => "Multidrug resistance" 1 => "Uropathogens" 2 => "Escherichia coli" 3 => "Klebsiella pneumoniae" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec971497" "palabras" => array:4 [ 0 => "Multirresistencia a antibióticos" 1 => "Uropatógenos" 2 => "Escherichia coli" 3 => "Klebsiella pneumoniae" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:3 [ "titulo" => "Abstract" "resumen" => "IntroductionThe aim of this study was to identify multi-drug resistance (MDR) in the main enterobacteriaceae implicated in urinary tract infections (Escherichia coli and Klebsiella pneumoniae) from both, community and hospitalized patients and to analyze the evolution over a 12-year period. MethodsMicrob Dynamic software was used to analyze the microbiology laboratory database and a chi square test was applied to compare differences in group proportions and to determine the linear trend over 12 years in three different periods: 2003–2006, 2007–2010, 2011–2014. We chose amoxicillin, gentamicin, ciprofloxacin and trimethoprim–sulphamethoxazole as MDR markers. ResultsA total of 39,980 positive urine samples were analyzed, 34,564 (3786 from hospitalized patients and 30,778 from non-hospitalized patients) E. coli isolates, and 5,422 (774 from hospitalized patients and 4,648 from non-hospitalized patients) K. pneumoniae isolates. The prevalence of UTI due to MDR E. coli and MDR K. pneumoniae significantly increased in the period studied, both in hospitalized and outpatients. A higher percentage of MDR E. coli (5.89% in 2007–2010 versus 8.18% in 2011–2014) and MDR K. pneumoniae (2.38% in 2007–2010 versus 9.35% in 2011–2014) was evident and maintained constant over time in hospitalized patients in comparison to non-hospitalized ones. Infection due to MDR ESBL-producing E. coli and K. pneumoniae increased significantly during the last 8 years in both, hospitalized (20% versus 38% and 66.8% versus 82.6%, respectively) and non-hospitalized patients (18.2% versus 23.6% and 51% versus 74.6%, respectively). ConclusionsThis study includes data of a large sample size of urinary strains isolated over a 12 year period and demonstrates that MDR is an increasing phenomenon of particular importance in the main UTI-causing species." "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Introduction" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Methods" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Results" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Conclusions" ] ] ] "es" => array:3 [ "titulo" => "Resumen" "resumen" => "IntroducciónEl objetivo principal de este estudio fue identificar multirresistencia a antibióticos (multi-drug resistance [MDR]) en las principales enterobacterias implicadas en infecciones del tracto urinario (ITU) (Escherichia coli y Klebsiella pneumoniae) procedentes de pacientes hospitalizados y ambulatorios, y analizar su evolución durante un periodo de 12años. MétodosSe eligieron como marcadores de MDR amoxicilina, gentamicina, ciprofloxacino y trimetoprim-sulfametoxazol. Se realizó un tratamiento estadístico por chi cuadrado de los resultados obtenidos de nuestra base de datos y se analizó la tendencia lineal de la MDR en 3 periodos de 4 años: 2003-2006, 2007-2010 y 2011-2014. ResultadosSe analizaron un total de 39.980 muestras de orina con cultivo positivo para E.coli (3.786 de pacientes hospitalizados y 30.778 de pacientes ambulatorios) y 5.422 con cultivo positivo para K.pneumoniae (774 de pacientes hospitalizados y 4.648 de pacientes ambulatorios). La prevalencia de ITU debida a MDR E.coli y MDR K.pneumoniae aumentó significativamente en el periodo estudiado, tanto en pacientes hospitalizados como en pacientes ambulatorios, observándose un mayor porcentaje de MDR E.coli (5,89% en 2007-2010 versus 8,18% en 2011-2014) y MDR K.pneumoniae (2,38% in 2007-2010 versus 9,35% en 2011-2014) en pacientes hospitalizados. La infección debida a MDR E.coli y K.pneumoniae productoras de β-lactamasas de espectro extendido (BLEA) aumentó también de forma significativa durante los últimos 8años, tanto en pacientes hospitalizados (20% versus 38% y 66,8% versus 82,6%, respectivamente) como en los no hospitalizados (18,2% versus 23,6% y 51% versus 74,6%, respectivamente). ConclusionesEn este estudio se demuestra que la MDR es un fenómeno en aumento de particular importancia en las principales enterobacterias implicadas en ITU." "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0025" "titulo" => "Introducción" ] 1 => array:2 [ "identificador" => "abst0030" "titulo" => "Métodos" ] 2 => array:2 [ "identificador" => "abst0035" "titulo" => "Resultados" ] 3 => array:2 [ "identificador" => "abst0040" "titulo" => "Conclusiones" ] ] ] ] "multimedia" => array:7 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1828 "Ancho" => 1722 "Tamanyo" => 204214 ] ] "descripcion" => array:1 [ "en" => "Prevalence and evolution of MDR E. coli (A) and K. pneumoniae (B) urinary isolates from both, community and hospitalized patients." ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Fig. 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 1682 "Ancho" => 2792 "Tamanyo" => 331098 ] ] "descripcion" => array:1 [ "en" => "Prevalence and evolution of E. coli (A) and K. pneumoniae (B) urinary isolates from both, community and hospitalized patients, in individual resistance to amoxicillin, ciprofloxacin, gentamicin and trimethoprim–sulphamethoxazole." ] ] 2 => array:7 [ "identificador" => "fig0015" "etiqueta" => "Fig. 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 2151 "Ancho" => 1539 "Tamanyo" => 183477 ] ] "descripcion" => array:1 [ "en" => "ESBL contribution to the MDR profile in E. coli (A) and K. pneumoniae (B) from both, community and hospitalized patients." ] ] 3 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1A" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at1" "detalle" => "Table 1" "rol" => "short" ] ] "tabla" => array:1 [ "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">Hospitalized patients \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">2003–2006 \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">2007–2010 \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">2011–2014 \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">χ2 for trend (p) \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">ESBL-producing E. coli \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">8.15% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">12.21% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">10.35% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">4.88 (0.027) \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">ESBL-producing K. pneumoniae \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">6.16% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">7.54% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">15.04% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">11.19 (<0.001) \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1714380.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Percentage of global ESBL-producing E. coli (A) and K. pneumoniae (B) urinary isolates from both, hospitalized patients and outpatients over the periods of the study (2003–2006, 2007–2010, and 2011–2013), and chi square test for trend. A p-value<0.05 was considered as statistically significant." ] ] 4 => array:6 [ "identificador" => "tbl0010" "etiqueta" => "Table 1B" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:1 [ "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">Outpatients \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">2003–2006 \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">2007–2010 \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">2011–2014 \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">χ2 for trend (p) \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">ESBL-producing E. coli \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2.75% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">5.29% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">5.69% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">100.03 (<0.001) \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">ESBL-producing K. pneumoniae \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.18% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.60% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">5.52% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">51.86 (<0.001) \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1714383.png" ] ] ] ] ] 5 => array:8 [ "identificador" => "tbl0015" "etiqueta" => "Table 2A" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at2" "detalle" => "Table 2" "rol" => "short" ] ] "tabla" => array:1 [ "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">Hospitalized patients \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">2003–2006 \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">2007–2010 \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">2011–2014 \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">χ2 for trend (p) \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">MDR E. coli \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">5.58% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">5.89% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">8.18% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">5.99 (<0.014) \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">MDR K. pneumoniae \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.45% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2.38% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">9.35% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">18.38 (<0.001) \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">MDR ESBL-producing E. coli \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.86% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.18% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3.11% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">17.65 (<0.001) \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">MDR ESBL-producing K. pneumoniae \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.09% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.59% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">7.72% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">16.10 (<0.001) \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1714382.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Percentage of MDR E. coli (A) and K. pneumoniae (B) urinary isolates from both, hospitalized patients and outpatients over the periods of the study (2003–2006, 2007–2010, and 2011–2013), and chi square test for trend. A p-value<0.05 was considered as statistically significant." ] ] 6 => array:6 [ "identificador" => "tbl0020" "etiqueta" => "Table 2B" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "tabla" => array:1 [ "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">Outpatients \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">2003–2006 \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">2007–2010 \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">2011–2014 \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">χ2 for trend (p) \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">MDR E. coli \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3.21% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3.13% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">4.58% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">26.74 (<0.001) \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">MDR K. pneumoniae \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.08% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.47% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3.78% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">67.27 (<0.001) \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">MDR ESBL-producing E. coli \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.18% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.57% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">1.08% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">67.07 (<0.001) \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">MDR ESBL-producing K. pneumoniae \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.17% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">0.24% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2.82% \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">47.54 (<0.001) \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1714381.png" ] ] ] ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:30 [ 0 => array:3 [ "identificador" => "bib0155" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Antibiotic susceptibility of common pediatric uropathogens in the United States" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:5 [ 0 => "P.D. 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Original article

Evolution of antibiotic multiresistance in Escherichia coli and Klebsiella pneumoniae isolates from urinary tract infections: A 12-year analysis (2003–2014)

Evolución de la multirresistencia a los antibióticos en Escherichia coli y Klebsiella pneumoniae aislados de infecciones del tracto urinario. Un análisis de 12 años (2003-2014)

David M. Aranaa, Margarita Rubiob, Juan-Ignacio Alósa,b,

Corresponding author

nachoalos@telefonica.net

Corresponding author.

a Servicio de Microbiología, Hospital Universitario de Getafe, Getafe, Madrid, Spain

b Facultad de Ciencias Biomédicas, Universidad Europea de Madrid, Villaviciosa de Odón, Madrid, Spain

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        "titulo" => "Evoluci&#243;n de la multirresistencia a los antibi&#243;ticos en <span class="elsevierStyleItalic">Escherichia coli</span> y <span class="elsevierStyleItalic">Klebsiella pneumoniae</span> aislados de infecciones del tracto urinario&#46; Un an&#225;lisis de 12 a&#241;os &#40;2003-2014&#41;"
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          "en" => "<p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">ESBL contribution to the MDR profile in <span class="elsevierStyleItalic">E&#46; coli</span> &#40;A&#41; and <span class="elsevierStyleItalic">K&#46; pneumoniae</span> &#40;B&#41; from both&#44; community and hospitalized patients&#46;</p>"
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">The increasing rate of antibiotic resistance in uropathogens&#44; especially in <span class="elsevierStyleItalic">Escherichia coli</span> and <span class="elsevierStyleItalic">Klebsiella pneumoniae</span>&#44; as the most common etiologic agents of urinary tract infections &#40;UTI&#41;&#44; leads to difficulties in choosing adequate empirical therapy and achieving treatment success&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">Multiple studies regarding antibiotic susceptibility in uropathogens have been published in medical literature&#44;<a class="elsevierStyleCrossRefs" href="#bib0155"><span class="elsevierStyleSup">1&#8211;4</span></a> but only a few studies have addressed the multidrug resistance &#40;MDR&#41; behaviour&#46;<a class="elsevierStyleCrossRefs" href="#bib0175"><span class="elsevierStyleSup">5&#8211;7</span></a> According to a group of international experts from European Centre for Disease Prevention &#40;ECDC&#41; and Centers for Disease Control and Prevention &#40;CDC&#41; a standardized international definition for MDR was created&#46; MDR is defined as acquired non-susceptibility to at least one agent in three or more antimicrobial categories&#46;<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">8</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">MDR bacteria are more usually associated with nosocomial infections&#46; A significant part of nosocomial infections are diagnosed as UTI &#40;more than 30&#37;&#41; and a considerable part of the antimicrobial agents used in hospitals is dedicated for their treatment&#46;<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">9</span></a> However&#44; the vast majority of UTI come from outpatients&#44; the most common being uncomplicated cystitis &#40;infection of bladder&#41; in women&#46; The 2010 guidelines of the Infectious Diseases Society of America and the European Society for Microbiology and Infectious Diseases recommend for empirical treatment of acute uncomplicated cystitis trimethoprim&#8211;sulphamethoxazole &#40;if the local resistance is less than 20&#37;&#41;&#44; nitrofurantoin&#44; fosfomycin trometamol and pivmecillinam &#40;as first-line therapy&#41;&#46; Fluoroquinolones may be used only as alternative therapy and their use must be avoided to treat uncomplicated cystitis whenever possible&#46;<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">10</span></a> MDR bacteria at the community level has increased&#44; making the treatment of infections more difficult and requiring&#44; in some cases&#44; intravenous therapy because of the lack of oral options&#46;<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">11</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">Several factors contribute to the increasing spread of MDR to antimicrobials&#46; The overuse and misuse of antimicrobials inhuman medicine&#44; in veterinary and in agriculture represent&#44; among others&#44; are some of the main factors involved in the selective pressure&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">In addition&#44; MDR in urine isolates from the community is often associated with the presence of multiple extended-spectrum-&#946;-lactamases &#40;ESBL&#41; genes&#44; as well as aminoglycoside and quinolone resistance genes&#46;<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">12</span></a></p><p id="par0030" class="elsevierStylePara elsevierViewall">This study aims to identify MDR in the main enterobacteriaceae implicated as etiologic agents in UTI &#40;<span class="elsevierStyleItalic">E&#46; coli</span> and <span class="elsevierStyleItalic">K&#46; pneumoniae</span>&#41; from both&#44; community and hospitalized patients&#44; and to analyze the evolution over a 12-year period&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Methods</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Study population and bacterial isolates</span><p id="par0035" class="elsevierStylePara elsevierViewall">A 12-year &#40;2003&#8211;2014&#41; retrospective study was conducted in both hospitalized and non-hospitalized patients suspected of UTI at the Hospital Universitario de Getafe &#40;Madrid&#41;&#46; The hospital has 413&#8211;600 operational beds and an attended population of 211&#44;000&#8211;260&#44;000 inhabitants &#40;depending on the year&#41;&#46; During the period of the study&#44; each urine sample was cultured using a 1<span class="elsevierStyleHsp" style=""></span>&#956;L calibrated loop in cysteine lactose electrolytes deficient &#40;CLED&#41; agar and incubated at 37<span class="elsevierStyleHsp" style=""></span>&#176;C for 18&#8211;24<span class="elsevierStyleHsp" style=""></span>h&#46; A growth of &#62;10<span class="elsevierStyleSup">4</span> colony-forming units &#40;CFU&#41; per mL of one type of organism were considered as a positive result&#46; Identification and antibiotic susceptibilities were performed using a microdilution system &#40;WIDER&#44; Franscico Soria Melguizo&#44; SA&#41;&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">Microb Dynamic software &#40;Francisco SoriaMelguizo&#44; SA&#41; was used to analyze the microbiology laboratory database&#46; It provides analysis of antimicrobial susceptibility and resistance test results according to the European Committee for Antimicrobial Susceptibility Testing &#40;EUCAST&#41; 2015 &#40;version 5&#46;0&#41; clinical breakpoints &#40;<a id="intr0005" class="elsevierStyleInterRef" href="http://www.eucast.org/">www&#46;eucast&#46;org</a>&#41;&#46; The software was used to determine the prevalence of both MDR <span class="elsevierStyleItalic">E&#46; coli</span> and <span class="elsevierStyleItalic">K&#46; pneumoniae</span>&#46; In order to avoid distortions in the final results&#44; isolates from the same patient with different antibiotic susceptibility patterns were considered as different while isolates showing the same pattern were considered as unique&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Statistical analysis</span><p id="par0045" class="elsevierStylePara elsevierViewall">A chi square test was applied to compare differences in group proportions in three different periods&#58; 2003&#8211;2006&#44; 2007&#8211;2010 and 2011&#8211;2014&#46; Chi square test for trend was used to determine whether there was a statistically significant linear trend over the period of the study&#46; A <span class="elsevierStyleItalic">p</span>-value &#60;0&#46;05 was considered as statistically significant&#46; All statistical analyses were performed using Epi Info v&#46; 7 &#40;CDC&#44; Atlanta&#44; USA&#41;&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Antimicrobial susceptibility</span><p id="par0050" class="elsevierStylePara elsevierViewall">We determined the proportion of isolates resistant to at least the antimicrobials agents that we chose as MDR markers &#40;amoxicillin&#44; gentamicin&#44; ciprofloxacin and trimethoprim&#8211;sulphamethoxazole&#41; according to their clinical antimicrobial MIC breakpoints&#58; amoxicillin &#40;MIC &#62;8<span class="elsevierStyleHsp" style=""></span>mg&#47;L&#41;&#44; ciprofloxacin &#40;MIC &#62;1<span class="elsevierStyleHsp" style=""></span>mg&#47;L&#41;&#44; trimethoprim&#8211;sulphamethoxazole &#40;MIC &#62;4&#47;76<span class="elsevierStyleHsp" style=""></span>mg&#47;L&#41; and gentamicin &#40;MIC &#62;4<span class="elsevierStyleHsp" style=""></span>mg&#47;L&#41;&#46; Amoxicillin is not considered in <span class="elsevierStyleItalic">K&#46; pneumoniae</span> because of its intrinsic resistance&#46; We also determined the global prevalence of ESBL producing <span class="elsevierStyleItalic">E&#46; coli</span> and <span class="elsevierStyleItalic">K&#46; pneumoniae</span> &#40;MDR and non-MDR&#41; and the proportion of both&#44; MDR <span class="elsevierStyleItalic">E&#46; coli</span> and MDR <span class="elsevierStyleItalic">K&#46; pneumoniae</span> isolates harbouring ESBL&#46; Positive results derived from ESBL producing enterobacteriaceae isolates are routinely introduced in the database when phenotypic studies are developed in the suspected ESBL producers&#46;</p></span></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Results</span><p id="par0055" class="elsevierStylePara elsevierViewall">In total&#44; the laboratory counted 39&#44;980 positive urine samples over the 12-year period&#46; 34&#44;564 positive urine samples &#40;3786 from hospitalized patients and 30&#44;778 from non-hospitalized patients&#41; had <span class="elsevierStyleItalic">E&#46; coli</span> as the infecting organism and 5&#44;422 positive urine cultures &#40;774 from hospitalized patients and 4&#44;648 from non-hospitalized patients&#41; had <span class="elsevierStyleItalic">K&#46; pneumoniae</span> as the etiological organism&#46;</p><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Prevalence and evolution of MDR profiles</span><p id="par0060" class="elsevierStylePara elsevierViewall">The prevalence of UTI due to MDR <span class="elsevierStyleItalic">E&#46; coli</span> &#40;resistance at least to amoxicillin&#44; ciprofloxacin&#44; gentamicin and trimethoprim&#8211;sulphamethoxazole&#41; in hospitalized patients increased from 5&#46;89&#37; &#91;70 out of 1&#44;188 isolates&#93; in the period 2007&#8211;2010 to 8&#46;18&#37; &#91;79 out of 966 isolates&#93; in the period 2011&#8211;2014 &#40;1&#46;4-fold increase&#41; &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;038&#41;&#46; Similar results were observed in the same period when outpatient population was analyzed&#58; 3&#46;13&#37; &#91;332 out of 10&#44;615 isolates&#93; <span class="elsevierStyleItalic">versus</span> 4&#46;58&#37; &#91;456 out of 9&#44;947 isolates&#93;&#44; respectively &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;001&#41;&#46; No significant differences were observed between the first and the second periods of the study &#40;2003&#8211;2006 and 2007&#8211;2010&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>A&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0065" class="elsevierStylePara elsevierViewall">However&#44; the prevalence of UTI caused by MDR <span class="elsevierStyleItalic">K&#46; pneumoniae</span> &#40;resistance at least to ciprofloxacin&#44; gentamicin and trimethoprim&#8211;sulphamethoxazole&#41; suffered a more drastic change between 2007&#8211;2010 and 2011&#8211;2014&#46; <a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>B shows a 4-fold increase in hospitalized patients &#40;2&#46;38&#37; &#91;6 out of 252 isolates&#93; in 2007&#8211;2010 <span class="elsevierStyleItalic">versus</span> 9&#46;35&#37; &#91;23 out of 246 isolates&#93; in 2011&#8211;2014&#59; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;001&#41;&#46; This change in prevalence was even more pronounced &#40;8-fold increase&#41; when outpatient population was analyzed &#40;0&#46;47&#37; &#91;8 out of 1&#44;689 isolates&#93; in 2007&#8211;2010 <span class="elsevierStyleItalic">versus</span> 3&#46;78&#37; &#91;67 out of 1&#44;774 isolates&#93; in 2011&#8211;2014&#59; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;001&#41; A slight but not significant increase was also observed between the first and second periods &#40;2003&#8211;2006 <span class="elsevierStyleItalic">versus</span> 2007&#8211;2010&#41; in both hospitalized and non-hospitalized patients &#40;1&#46;45&#37; &#91;4 out of 276 isolates&#93; <span class="elsevierStyleItalic">versus</span> 2&#46;38&#37; &#91;6 out of 252 isolates&#93; and 0&#46;08&#37; &#91;1 out of 1&#44;185 isolates&#93; <span class="elsevierStyleItalic">versus</span> 0&#46;47&#37; &#91;8 out of 1&#44;689 isolates&#93; respectively&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>B&#41;&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">Therefore&#44; higher percentages of MDR <span class="elsevierStyleItalic">E&#46; coli</span> in hospitalized patients with respect to outpatients &#40;1&#46;8-fold increase in all the time periods&#41; were evident and maintained constant over time &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>A&#41;&#46; Similar results were observed in the percentage of MDR <span class="elsevierStyleItalic">K&#46; pneumoniae</span> isolates&#44; but the differences with respect to the non-hospitalized patients were more marked &#40;&#62;1&#46;8-fold increase in all the time periods&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>B&#41;&#46; It is important to note that the increase observed in the prevalence of MDR <span class="elsevierStyleItalic">E&#46; coli</span> isolates is mainly due to the individual resistance to ciprofloxacin and gentamicin regardless of the patient hospitalization&#44; while individual resistance to amoxicillin and trimethoprim&#8211;sulphamethoxazole remained stable during the period of the study &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>A&#41;&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0075" class="elsevierStylePara elsevierViewall">By contrast&#44; the increase in prevalence of MDR <span class="elsevierStyleItalic">K&#46; pneumoniae</span> isolates is due to the individual resistance to ciprofloxacin&#44; gentamicin and trimethoprim&#8211;sulphamethoxazole &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>B&#41;&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">ESBL contribution to the MDR profile</span><p id="par0080" class="elsevierStylePara elsevierViewall">The global prevalence of UTI due to ESBL producing <span class="elsevierStyleItalic">E&#46; coli</span> in hospitalized patients increased from 8&#46;1&#37; in the period 2003&#8211;2006 to 10&#46;3&#37; in the period 2011&#8211;2014 &#40;1&#46;27 fold-increase&#41; while this increase in prevalence was more marked when non-hospitalized patients were analyzed &#40;2&#46;7&#37; in 2003&#8211;2006 <span class="elsevierStyleItalic">versus</span> 5&#46;7&#37; in 2011&#8211;2014&#59; 2 fold-increase&#41;&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">However&#44; the rise in global prevalence of UTI due to ESBL producing <span class="elsevierStyleItalic">K&#46; pneumoniae</span> in both&#44; hospitalized and outpatients was more pronounced &#40;6&#46;1&#37; in 2003&#8211;2006 <span class="elsevierStyleItalic">versus</span> 15&#37; in 2011&#8211;2014&#59; 2&#46;4 fold-increase and 1&#46;1&#37; in 2003&#8211;2006 <span class="elsevierStyleItalic">versus</span> 5&#46;5&#37; in 2011&#8211;2014&#59; 5 fold-increase&#44; respectively&#41;&#46; <a class="elsevierStyleCrossRefs" href="#tbl0005">Table 1</a> show an analysis for linear trend in ESBL-producing <span class="elsevierStyleItalic">E&#46; coli</span> and ESBL-producing <span class="elsevierStyleItalic">K&#46; pneumoniae</span> in hospitalized patients &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1A</a>&#41; and non-hospitalized patients &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 1B</a>&#41; over the period of the study&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0090" class="elsevierStylePara elsevierViewall">In order to determine the contribution of ESBL in the MDR phenotype of both <span class="elsevierStyleItalic">K&#46; pneumoniae</span> and <span class="elsevierStyleItalic">E&#46; coli</span>&#44; Microb Dynamic software was used to analyze the percentage of MDR isolates harbouring an ESBL&#46;</p><p id="par0095" class="elsevierStylePara elsevierViewall">The results show that the prevalence of UTI due to ESBL producing MDR <span class="elsevierStyleItalic">E&#46; coli</span> in hospitalized patients increased from 0&#46;86&#37; in the period 2003&#8211;2006 to 3&#46;11&#37; in the period 2011&#8211;2014 &#40;3&#46;6 fold-increase&#41; while this increase in prevalence was more marked&#44; as above&#44; when non-hospitalized patients were analyzed &#40;0&#46;18&#37; in 2003&#8211;2006 <span class="elsevierStyleItalic">versus</span> 1&#46;08&#37; in 2011&#8211;2014&#59; 6 fold-increase&#41;&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">By contrast&#44; the prevalence of UTI due to ESBL producing MDR <span class="elsevierStyleItalic">K&#46; pneumoniae</span> in hospitalized patients increased from 1&#46;09&#37; in the period 2003&#8211;2006 to 7&#46;72&#37; in the period 2011&#8211;2014 &#40;7&#46;6 fold-increase&#41; while this increase in prevalence was more marked when non-hospitalized patients were analyzed &#40;0&#46;08&#37; in 2003&#8211;2006 <span class="elsevierStyleItalic">versus</span> 2&#46;82&#37; in 2011&#8211;2014&#59; 35&#46;2 fold-increase&#41;&#46; In hospitalized patients&#44; 14 out of 70 &#40;20&#37;&#41; MDR <span class="elsevierStyleItalic">E&#46; coli</span> isolates were MDR ESBL-producing <span class="elsevierStyleItalic">E&#46; coli</span> in 2007&#8211;2010&#46; This percentage increased to 38&#37; &#40;30 out of 79&#41; in 2011&#8211;2014 &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;016&#41;&#46; However&#44; the increase observed in non-hospitalized patients between the same periods was not as marked &#40;18&#46;2&#37; in 2007&#8211;2010 to 23&#46;6&#37; in 2011&#8211;2014&#41; &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;085&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>A&#41;&#46; The contribution of ESBL to the MDR <span class="elsevierStyleItalic">K&#46; pneumoniae</span> isolated in hospitalized patients was 66&#46;8&#37; &#40;4 out of 6&#41; in 2007&#8211;2010&#59; this percentage rose to 82&#46;6&#37; &#40;19 out of 23&#41; in 2011&#8211;2014 &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;77&#41;&#46; The increase observed in non-hospitalized patients between the same periods was 51&#37; &#40;4 out of 8&#41; in 2007&#8211;2010 to 74&#46;6&#37; &#40;50 out of 67&#41; in 2011&#8211;2014 &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;143&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>B&#41;&#46; The results indicate that the contribution of ESBL to the MDR behaviour was more pronounced in <span class="elsevierStyleItalic">K&#46; pneumoniae</span> isolates&#46; <a class="elsevierStyleCrossRefs" href="#tbl0015">Table 2</a> shows an analysis for linear trend in MDR <span class="elsevierStyleItalic">E&#46; coli</span> and <span class="elsevierStyleItalic">K&#46; pneumoniae</span> in hospitalized patients &#40;<a class="elsevierStyleCrossRef" href="#tbl0015">Table 2A</a>&#41; and MDR <span class="elsevierStyleItalic">E&#46; coli</span> and <span class="elsevierStyleItalic">K&#46; pneumoniae</span> in non-hospitalized patients &#40;<a class="elsevierStyleCrossRef" href="#tbl0020">Table 2B</a>&#41; over the period of the study&#46;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia><elsevierMultimedia ident="tbl0015"></elsevierMultimedia><elsevierMultimedia ident="tbl0020"></elsevierMultimedia></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Susceptibility to other antibiotics in MDR isolates</span><p id="par0105" class="elsevierStylePara elsevierViewall">In order to study the role of alternative antibiotic treatments in the MDR isolates&#44; susceptibility to fosfomycin&#44; meropenem and amoxicillin&#47;clavulanate was analyzed&#46; All the MDR <span class="elsevierStyleItalic">E&#46; coli</span> isolates &#40;from both&#44; inpatients and outpatients&#41; were sensitive to fosfomycin during the first 8 years &#40;first and second periods&#41;&#46; The proportion of susceptible isolates diminished during the last period &#40;82&#37; from inpatients and 86&#37; from outpatients&#41;&#46;</p><p id="par0110" class="elsevierStylePara elsevierViewall">In the same way&#44; all the isolates studied were susceptible to meropenem &#40;except one isolate of MDR <span class="elsevierStyleItalic">K&#46; pneumoniae</span> from a hospitalized patient harbouring a carbapenemase OXA-48 in 2013&#41;&#46;</p><p id="par0115" class="elsevierStylePara elsevierViewall">Susceptibility to amoxicillin&#47;clavulanate decreased along the period of the study in both&#44; MDR <span class="elsevierStyleItalic">E&#46; coli</span> and MDR <span class="elsevierStyleItalic">K&#46; pneumoniae</span>&#46; Susceptibility to amoxicillin&#47;clavulanate in MDR <span class="elsevierStyleItalic">E&#46; coli</span> isolates from hospitalized patients decreased from 84&#46;5&#37; in the period 2003&#8211;2006 to 46&#46;8&#37; in the period 2011&#8211;2014 &#40;1&#46;8-fold decreased&#41;&#46; Comparable results were obtained in the same period when outpatient population was analyzed&#58; 86&#46;6&#37; <span class="elsevierStyleItalic">versus</span> 51&#46;7&#37; respectively&#46; Susceptibility to amoxicillin&#47;clavulanate in MDR <span class="elsevierStyleItalic">K&#46; pneumoniae</span> suffered a more drastic change between 2003&#8211;2006 and 2011&#8211;2014&#46; All the MDR <span class="elsevierStyleItalic">K&#46; pneumoniae</span> isolates from hospitalized patients were resistant to amoxicillin&#47;clavulanate in 2011&#8211;2014 respect to the first period &#40;49&#46;6&#37; were susceptible&#41;&#46; Susceptibility to amoxicillin&#47;clavulanate in MDR <span class="elsevierStyleItalic">K&#46; pneumoniae</span> isolates from outpatients decreased from 100&#37; in the period 2003&#8211;2006 to 16&#46;4&#37; in the period 2011&#8211;2014 &#40;6-fold decrease&#41;&#46;</p></span></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0110">Discussion</span><p id="par0120" class="elsevierStylePara elsevierViewall">The increase of bacterial resistance to antibiotics is a cause of global concern&#46; Infections caused by multiresistant microorganisms frequently fail to respond to a suitable empirical therapy and often times&#44; do not achieve treatment success&#46;<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">13</span></a></p><p id="par0125" class="elsevierStylePara elsevierViewall">Few studies have reported on the MDR patterns expressed by Gram negative uropathogens in both&#44; hospitalized and non-hospitalized patients&#44; and the evolution over time of such patterns&#46;<a class="elsevierStyleCrossRefs" href="#bib0185"><span class="elsevierStyleSup">7&#44;14&#8211;16</span></a> Some studies performed at community level have showed a high percentage &#40;about 38&#37;&#41; of MDR in <span class="elsevierStyleItalic">E&#46; coli</span>&#44; the most prevalent bacteria involved in the community-acquired UTI<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">17</span></a> while&#44; on the other hand&#44; MDR-<span class="elsevierStyleItalic">Klebsiella</span> species are considered as one of the most common bacteria involved in nosocomial and urinary tract infections&#46;<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">18</span></a></p><p id="par0130" class="elsevierStylePara elsevierViewall">The goal of this work was to analyze the evolution of multidrug resistance in both&#44; outpatients and inpatients&#44; to antibiotics commonly used in the treatment of urinary tract infection over a 12-year period&#46; As expected&#44; MDR phenotypes were more usually associated with hospitalization&#44; but the results show that MDR bacteria at the community level are increasing almost at the same rate as in hospitalized patients&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">The multiresistance could be associated with the high prescription of these antibiotics groups at community level in Spain&#46;<a class="elsevierStyleCrossRefs" href="#bib0245"><span class="elsevierStyleSup">19&#44;20</span></a></p><p id="par0140" class="elsevierStylePara elsevierViewall">Quinolone resistance is frequently associated with ESBL-production&#44; and according to the literature&#44; CTX-M represent the most common ESBL produced among bacteria implicated in community-acquired UTI worldwide&#46;<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">21</span></a> In our study&#44; a high percentage of strains producing ESBL were detected in MDR isolates from both inpatients and outpatients&#46; The prevalence of infection due to MDR ESBL-producing <span class="elsevierStyleItalic">K&#46; pneumoniae</span> in non-hospitalized patients increased significantly during the last 8 years&#46; On the other hand&#44; exposure to penicillins and&#47;or trimethoprim&#8211;sulfamethoxazole has been considered a risk factor for ESBL-producing <span class="elsevierStyleItalic">E&#46; coli</span> isolation&#46;<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">22</span></a> All of these results are in accordance with the results obtained in our study suggesting that resistance to quinolones and trimethoprim&#8211;sulphamethoxazole are associated with ESBL production&#46; By contrast&#44; this phenomenon was less marked in hospitalized patients&#46;</p><p id="par0145" class="elsevierStylePara elsevierViewall">It is important to take into account that alternative therapies such as fosfomycin represent a promising treatment option against MDR urinary isolates&#46; Fosfomycin resistance is usually rare in areas with limited use but it is increasing in countries with higher usage&#46;<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">23</span></a> Our results show that all the MDR <span class="elsevierStyleItalic">E&#46; coli</span> isolates were sensitive to fosfomycin during the first 8 years&#44; but resistant isolates have emerged during the last years&#46; By contrast all the MDR isolates were susceptible to carbapenems due to the absence of carbapenemases&#46;</p><p id="par0150" class="elsevierStylePara elsevierViewall">The emergence and spread of different clones have to be taken into account in order to explain the increase in MDR bacteria&#46; Numerous articles have reported that the well-known high-risk <span class="elsevierStyleItalic">E&#46; coli</span> ST131 and <span class="elsevierStyleItalic">K&#46; pneumoniae</span> ST258 clones have been responsible for the sudden increase in multidrug resistance&#46;<a class="elsevierStyleCrossRefs" href="#bib0270"><span class="elsevierStyleSup">24&#8211;27</span></a> ST131 is responsible of UTI&#44; frequently fluoroquinolone resistant and can be linked with the production of CTX-M-15&#44;<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">28</span></a> while ST258 is also known to cause UTI&#44; respiratory tract infections&#44; and blood stream infections and is associated with carbapenemase production&#44; most often KPC-2 and KPC-3&#46;<a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">29</span></a> Unfortunately&#44; we do not have information about molecular characterization of the strains isolated in our study&#46;</p><p id="par0155" class="elsevierStylePara elsevierViewall">It is also important to take into consideration that mobile elements &#40;plasmids&#44; transposons&#44; integrons&#44; etc&#46;&#41; play an important role in the transfer of other resistance genes and thus allowing a co-selection phenomenon &#40;see for a review<a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">30</span></a>&#41;&#46;</p><p id="par0160" class="elsevierStylePara elsevierViewall">The present study has some limitations&#59; it was conducted in an area &#40;Getafe&#41;&#44; which represents a small portion of the total population of Spain and&#44; in this case&#44; the results cannot be extrapolated to other settings because specific epidemiology of different areas have to be taken into consideration&#46; Further studies would be necessary to address the problem at national and global level&#46; Despite the above limitations&#44; some strengths are also remarkable and include data of a large sample size of urinary strains isolated over a 12 year period that demonstrates that MDR is an increasing phenomenon of particular importance over the last few years&#46;</p></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0115">Funding</span><p id="par0165" class="elsevierStylePara elsevierViewall">No specific funding has been received&#46;</p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0120">Conflict of interest</span><p id="par0170" class="elsevierStylePara elsevierViewall">None to declare&#46;</p></span></span>"
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              "titulo" => "Antimicrobial susceptibility"
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              "titulo" => "Prevalence and evolution of MDR profiles"
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              "titulo" => "ESBL contribution to the MDR profile"
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              "titulo" => "Susceptibility to other antibiotics in MDR isolates"
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    "fechaRecibido" => "2015-10-30"
    "fechaAceptado" => "2016-02-20"
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            2 => "<span class="elsevierStyleItalic">Escherichia coli</span>"
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            0 => "Multirresistencia a antibi&#243;ticos"
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    "resumen" => array:2 [
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        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Introduction</span><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">The aim of this study was to identify multi-drug resistance &#40;MDR&#41; in the main enterobacteriaceae implicated in urinary tract infections &#40;<span class="elsevierStyleItalic">Escherichia coli</span> and <span class="elsevierStyleItalic">Klebsiella pneumoniae</span>&#41; from both&#44; community and hospitalized patients and to analyze the evolution over a 12-year period&#46;</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Methods</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Microb Dynamic software was used to analyze the microbiology laboratory database and a chi square test was applied to compare differences in group proportions and to determine the linear trend over 12 years in three different periods&#58; 2003&#8211;2006&#44; 2007&#8211;2010&#44; 2011&#8211;2014&#46; We chose amoxicillin&#44; gentamicin&#44; ciprofloxacin and trimethoprim&#8211;sulphamethoxazole as MDR markers&#46;</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">A total of 39&#44;980 positive urine samples were analyzed&#44; 34&#44;564 &#40;3786 from hospitalized patients and 30&#44;778 from non-hospitalized patients&#41; <span class="elsevierStyleItalic">E&#46; coli</span> isolates&#44; and 5&#44;422 &#40;774 from hospitalized patients and 4&#44;648 from non-hospitalized patients&#41; <span class="elsevierStyleItalic">K&#46; pneumoniae</span> isolates&#46; The prevalence of UTI due to MDR <span class="elsevierStyleItalic">E&#46; coli</span> and MDR <span class="elsevierStyleItalic">K&#46; pneumoniae</span> significantly increased in the period studied&#44; both in hospitalized and outpatients&#46; A higher percentage of MDR <span class="elsevierStyleItalic">E&#46; coli</span> &#40;5&#46;89&#37; in 2007&#8211;2010 <span class="elsevierStyleItalic">versus</span> 8&#46;18&#37; in 2011&#8211;2014&#41; and MDR <span class="elsevierStyleItalic">K&#46; pneumoniae</span> &#40;2&#46;38&#37; in 2007&#8211;2010 <span class="elsevierStyleItalic">versus</span> 9&#46;35&#37; in 2011&#8211;2014&#41; was evident and maintained constant over time in hospitalized patients in comparison to non-hospitalized ones&#46; Infection due to MDR ESBL-producing <span class="elsevierStyleItalic">E&#46; coli</span> and <span class="elsevierStyleItalic">K&#46; pneumoniae</span> increased significantly during the last 8 years in both&#44; hospitalized &#40;20&#37; <span class="elsevierStyleItalic">versus</span> 38&#37; and 66&#46;8&#37; <span class="elsevierStyleItalic">versus</span> 82&#46;6&#37;&#44; respectively&#41; and non-hospitalized patients &#40;18&#46;2&#37; <span class="elsevierStyleItalic">versus</span> 23&#46;6&#37; and 51&#37; <span class="elsevierStyleItalic">versus</span> 74&#46;6&#37;&#44; respectively&#41;&#46;</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Conclusions</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">This study includes data of a large sample size of urinary strains isolated over a 12 year period and demonstrates that MDR is an increasing phenomenon of particular importance in the main UTI-causing species&#46;</p></span>"
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            "titulo" => "Methods"
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        "resumen" => "<span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Introducci&#243;n</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">El objetivo principal de este estudio fue identificar multirresistencia a antibi&#243;ticos &#40;<span class="elsevierStyleItalic">multi-drug resistance</span> &#91;MDR&#93;&#41; en las principales enterobacterias implicadas en infecciones del tracto urinario &#40;ITU&#41; &#40;<span class="elsevierStyleItalic">Escherichia coli</span> y <span class="elsevierStyleItalic">Klebsiella pneumoniae</span>&#41; procedentes de pacientes hospitalizados y ambulatorios&#44; y analizar su evoluci&#243;n durante un periodo de 12<span class="elsevierStyleHsp" style=""></span>a&#241;os&#46;</p></span> <span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">M&#233;todos</span><p id="spar0065" class="elsevierStyleSimplePara elsevierViewall">Se eligieron como marcadores de MDR amoxicilina&#44; gentamicina&#44; ciprofloxacino y trimetoprim-sulfametoxazol&#46; Se realiz&#243; un tratamiento estad&#237;stico por chi cuadrado de los resultados obtenidos de nuestra base de datos y se analiz&#243; la tendencia lineal de la MDR en 3 periodos de 4 a&#241;os&#58; 2003-2006&#44; 2007-2010 y 2011-2014&#46;</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Se analizaron un total de 39&#46;980 muestras de orina con cultivo positivo para <span class="elsevierStyleItalic">E&#46;</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">coli</span> &#40;3&#46;786 de pacientes hospitalizados y 30&#46;778 de pacientes ambulatorios&#41; y 5&#46;422 con cultivo positivo para <span class="elsevierStyleItalic">K&#46;</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">pneumoniae</span> &#40;774 de pacientes hospitalizados y 4&#46;648 de pacientes ambulatorios&#41;&#46; La prevalencia de ITU debida a MDR <span class="elsevierStyleItalic">E&#46;</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">coli</span> y MDR <span class="elsevierStyleItalic">K&#46;</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">pneumoniae</span> aument&#243; significativamente en el periodo estudiado&#44; tanto en pacientes hospitalizados como en pacientes ambulatorios&#44; observ&#225;ndose un mayor porcentaje de MDR <span class="elsevierStyleItalic">E&#46;</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">coli</span> &#40;5&#44;89&#37; en 2007-2010 <span class="elsevierStyleItalic">versus</span> 8&#44;18&#37; en 2011-2014&#41; y MDR <span class="elsevierStyleItalic">K&#46;</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">pneumoniae</span> &#40;2&#44;38&#37; in 2007-2010 <span class="elsevierStyleItalic">versus</span> 9&#44;35&#37; en 2011-2014&#41; en pacientes hospitalizados&#46; La infecci&#243;n debida a MDR <span class="elsevierStyleItalic">E&#46;</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">coli</span> y <span class="elsevierStyleItalic">K&#46;</span><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">pneumoniae</span> productoras de &#946;-lactamasas de espectro extendido &#40;BLEA&#41; aument&#243; tambi&#233;n de forma significativa durante los &#250;ltimos 8<span class="elsevierStyleHsp" style=""></span>a&#241;os&#44; tanto en pacientes hospitalizados &#40;20&#37; <span class="elsevierStyleItalic">versus</span> 38&#37; y 66&#44;8&#37; <span class="elsevierStyleItalic">versus</span> 82&#44;6&#37;&#44; respectivamente&#41; como en los no hospitalizados &#40;18&#44;2&#37; <span class="elsevierStyleItalic">versus</span> 23&#44;6&#37; y 51&#37; <span class="elsevierStyleItalic">versus</span> 74&#44;6&#37;&#44; respectivamente&#41;&#46;</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusiones</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">En este estudio se demuestra que la MDR es un fen&#243;meno en aumento de particular importancia en las principales enterobacterias implicadas en ITU&#46;</p></span>"
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                  \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">Hospitalized patients&nbsp;\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">2003&#8211;2006&nbsp;\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">2007&#8211;2010&nbsp;\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">2011&#8211;2014&nbsp;\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">&#967;</span><span class="elsevierStyleSup">2</span> for trend &#40;<span class="elsevierStyleItalic">p</span>&#41;&nbsp;\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">ESBL-producing <span class="elsevierStyleItalic">E&#46; coli</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">8&#46;15&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">12&#46;21&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">10&#46;35&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">4&#46;88 &#40;0&#46;027&#41;&nbsp;\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">ESBL-producing <span class="elsevierStyleItalic">K&#46; pneumoniae</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">6&#46;16&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">7&#46;54&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">15&#46;04&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">11&#46;19 &#40;&#60;0&#46;001&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
              ]
              "imagenFichero" => array:1 [
                0 => "xTab1714380.png"
              ]
            ]
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">Percentage of global ESBL-producing <span class="elsevierStyleItalic">E&#46; coli</span> &#40;A&#41; and <span class="elsevierStyleItalic">K&#46; pneumoniae</span> &#40;B&#41; urinary isolates from both&#44; hospitalized patients and outpatients over the periods of the study &#40;2003&#8211;2006&#44; 2007&#8211;2010&#44; and 2011&#8211;2013&#41;&#44; and chi square test for trend&#46; A <span class="elsevierStyleItalic">p</span>-value<span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05 was considered as statistically significant&#46;</p>"
        ]
      ]
      4 => array:6 [
        "identificador" => "tbl0010"
        "etiqueta" => "Table 1B"
        "tipo" => "MULTIMEDIATABLA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "tabla" => array:1 [
          "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">Outpatients&nbsp;\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">2003&#8211;2006&nbsp;\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">2007&#8211;2010&nbsp;\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">2011&#8211;2014&nbsp;\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">&#967;</span><span class="elsevierStyleSup">2</span> for trend &#40;<span class="elsevierStyleItalic">p&#41;</span>&nbsp;\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">ESBL-producing <span class="elsevierStyleItalic">E&#46; coli</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&#46;75&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">5&#46;29&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">5&#46;69&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">100&#46;03 &#40;&#60;0&#46;001&#41;&nbsp;\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">ESBL-producing <span class="elsevierStyleItalic">K&#46; pneumoniae</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;18&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;60&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">5&#46;52&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">51&#46;86 &#40;&#60;0&#46;001&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
              ]
              "imagenFichero" => array:1 [
                0 => "xTab1714383.png"
              ]
            ]
          ]
        ]
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      5 => array:8 [
        "identificador" => "tbl0015"
        "etiqueta" => "Table 2A"
        "tipo" => "MULTIMEDIATABLA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "detalles" => array:1 [
          0 => array:3 [
            "identificador" => "at2"
            "detalle" => "Table 2"
            "rol" => "short"
          ]
        ]
        "tabla" => array:1 [
          "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">Hospitalized patients&nbsp;\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">2003&#8211;2006&nbsp;\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">2007&#8211;2010&nbsp;\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">2011&#8211;2014&nbsp;\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">&#967;</span><span class="elsevierStyleSup">2</span> for trend &#40;<span class="elsevierStyleItalic">p</span>&#41;&nbsp;\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">MDR <span class="elsevierStyleItalic">E&#46; coli</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">5&#46;58&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">5&#46;89&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">8&#46;18&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">5&#46;99 &#40;&#60;0&#46;014&#41;&nbsp;\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">MDR <span class="elsevierStyleItalic">K&#46; pneumoniae</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;45&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&#46;38&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">9&#46;35&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">18&#46;38 &#40;&#60;0&#46;001&#41;&nbsp;\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">MDR ESBL-producing <span class="elsevierStyleItalic">E&#46; coli</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;86&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;18&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">3&#46;11&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">17&#46;65 &#40;&#60;0&#46;001&#41;&nbsp;\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">MDR ESBL-producing <span class="elsevierStyleItalic">K&#46; pneumoniae</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;09&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;59&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">7&#46;72&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">16&#46;10 &#40;&#60;0&#46;001&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
              ]
              "imagenFichero" => array:1 [
                0 => "xTab1714382.png"
              ]
            ]
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0060" class="elsevierStyleSimplePara elsevierViewall">Percentage of MDR <span class="elsevierStyleItalic">E&#46; coli</span> &#40;A&#41; and <span class="elsevierStyleItalic">K&#46; pneumoniae</span> &#40;B&#41; urinary isolates from both&#44; hospitalized patients and outpatients over the periods of the study &#40;2003&#8211;2006&#44; 2007&#8211;2010&#44; and 2011&#8211;2013&#41;&#44; and chi square test for trend&#46; A <span class="elsevierStyleItalic">p</span>-value<span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05 was considered as statistically significant&#46;</p>"
        ]
      ]
      6 => array:6 [
        "identificador" => "tbl0020"
        "etiqueta" => "Table 2B"
        "tipo" => "MULTIMEDIATABLA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "tabla" => array:1 [
          "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">Outpatients&nbsp;\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">2003&#8211;2006&nbsp;\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">2007&#8211;2010&nbsp;\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">2011&#8211;2014&nbsp;\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">&#967;</span><span class="elsevierStyleSup">2</span> for trend &#40;<span class="elsevierStyleItalic">p</span>&#41;&nbsp;\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">MDR <span class="elsevierStyleItalic">E&#46; coli</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">3&#46;21&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">3&#46;13&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">4&#46;58&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">26&#46;74 &#40;&#60;0&#46;001&#41;&nbsp;\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">MDR <span class="elsevierStyleItalic">K&#46; pneumoniae</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;08&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;47&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">3&#46;78&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">67&#46;27 &#40;&#60;0&#46;001&#41;&nbsp;\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">MDR ESBL-producing <span class="elsevierStyleItalic">E&#46; coli</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;18&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;57&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&#46;08&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">67&#46;07 &#40;&#60;0&#46;001&#41;&nbsp;\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">MDR ESBL-producing <span class="elsevierStyleItalic">K&#46; pneumoniae</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;17&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">0&#46;24&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&#46;82&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">47&#46;54 &#40;&#60;0&#46;001&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
              ]
              "imagenFichero" => array:1 [
                0 => "xTab1714381.png"
              ]
            ]
          ]
        ]
      ]
    ]
    "bibliografia" => array:2 [
      "titulo" => "References"
      "seccion" => array:1 [
        0 => array:2 [
          "identificador" => "bibs0005"
          "bibliografiaReferencia" => array:30 [
            0 => array:3 [
              "identificador" => "bib0155"
              "etiqueta" => "1"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Antibiotic susceptibility of common pediatric uropathogens in the United States"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:5 [
                            0 => "P&#46;D&#46; Tamma"
                            1 => "D&#46;J&#46; Sklansky"
                            2 => "D&#46;L&#46; Palazzi"
                            3 => "S&#46;K&#46; Swami"
                            4 => "A&#46;M&#46; Milstone"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1093/cid/ciu360"
                      "Revista" => array:6 [
                        "tituloSerie" => "Clin Infect Dis"
                        "fecha" => "2014"
                        "volumen" => "59"
                        "paginaInicial" => "750"
                        "paginaFinal" => "752"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/24825869"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            1 => array:3 [
              "identificador" => "bib0160"
              "etiqueta" => "2"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Evaluation of antimicrobial susceptibility of Enterobacteriaceae causing urinary tract infections in Africa"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:3 [
                            0 => "G&#46;S&#46; Tansarli"
                            1 => "S&#46; Athanasiou"
                            2 => "M&#46;E&#46; Falagas"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1128/AAC.00359-13"
                      "Revista" => array:6 [
                        "tituloSerie" => "Antimicrob Agents Chemother"
                        "fecha" => "2013"
                        "volumen" => "57"
                        "paginaInicial" => "3628"
                        "paginaFinal" => "3639"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/23689709"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            2 => array:3 [
              "identificador" => "bib0165"
              "etiqueta" => "3"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "The ARESC study&#58; an international survey on the antimicrobial resistance of pathogens involved in uncomplicated urinary tract infections"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => true
                          "autores" => array:6 [
                            0 => "G&#46;C&#46; Schito"
                            1 => "K&#46;G&#46; Naber"
                            2 => "H&#46; Botto"
                            3 => "J&#46; Palou"
                            4 => "T&#46; Mazzei"
                            5 => "L&#46; Gualco"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1016/j.ijantimicag.2009.04.012"
                      "Revista" => array:6 [
                        "tituloSerie" => "Int J Antimicrob Agents"
                        "fecha" => "2009"
                        "volumen" => "34"
                        "paginaInicial" => "407"
                        "paginaFinal" => "413"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/19505803"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
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Article information

ISSN: 0213005X
Original language: English

DOI:10.1016/j.eimc.2016.02.018

The statistics are updated each day

Year/Month	Html	Pdf	Total

2024 November	9	1	10
2024 October	37	7	44
2024 September	42	22	64
2024 August	54	16	70
2024 July	38	24	62
2024 June	27	8	35
2024 May	98	34	132
2024 April	34	21	55
2024 March	32	20	52
2024 February	31	7	38
2024 January	36	11	47
2023 December	40	31	71
2023 November	33	11	44
2023 October	32	45	77
2023 September	30	18	48
2023 August	22	38	60
2023 July	16	34	50
2023 June	35	43	78
2023 May	55	7	62
2023 April	48	13	61
2023 March	29	13	42
2023 February	22	7	29
2023 January	29	16	45
2022 December	29	15	44
2022 November	42	28	70
2022 October	44	22	66
2022 September	31	13	44
2022 August	50	36	86
2022 July	40	14	54
2022 June	54	26	80
2022 May	56	24	80
2022 April	62	38	100
2022 March	82	26	108
2022 February	97	27	124
2022 January	84	12	96
2021 December	55	28	83
2021 November	61	19	80
2021 October	102	24	126
2021 September	52	38	90
2021 August	60	22	82
2021 July	58	16	74
2021 June	44	29	73
2021 May	64	12	76
2021 April	122	47	169
2021 March	88	30	118
2021 February	73	24	97
2021 January	63	30	93
2020 December	57	25	82
2020 November	46	26	72
2020 October	47	21	68
2020 September	63	24	87
2020 August	50	35	85
2020 July	39	16	55
2020 June	33	18	51
2020 May	51	32	83
2020 April	46	20	66
2020 March	41	18	59
2020 February	72	44	116
2020 January	90	40	130
2019 December	77	30	107
2019 November	53	34	87
2019 October	70	30	100
2019 September	49	27	76
2019 August	46	20	66
2019 July	23	39	62
2019 June	41	44	85
2019 May	101	153	254
2019 April	45	91	136
2019 March	22	23	45
2019 February	24	27	51
2019 January	21	11	32
2018 December	22	22	44
2018 November	37	12	49
2018 October	37	25	62
2018 September	44	12	56
2018 August	26	17	43
2018 July	21	18	39
2018 June	19	7	26
2018 May	441	12	453
2018 April	64	20	84
2018 March	16	6	22
2018 February	16	7	23
2018 January	25	1	26
2017 December	16	9	25
2017 November	25	12	37
2017 October	27	0	27
2017 September	5	1	6
2017 August	2	0	2
2017 July	4	0	4
2017 June	12	6	18
2017 May	82	83	165
2017 March	0	2	2
2017 February	2	11	13
2017 January	0	8	8
2016 December	2	12	14
2016 November	3	512	515
2016 October	7	23	30
2016 September	7	14	21
2016 August	6	16	22
2016 July	1	6	7

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