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Original article
Interhospital dissemination of KPC-3 producing-Klebsiella pneumoniae ST512. Detection by MALDI-TOF
Diseminación interhospitalaria de Klebsiella pneumoniae ST512 productora de KPC-3. Detección por MALDI-TOF
María Ángeles Asencio Egeaa,
Corresponding author
marian_asencio@yahoo.es

Corresponding author.
, Jorge Gaitán Piteraa, María Huertas Vaqueroa, Rafael Carranza Gonzáleza, Carmen Román Ortizb, Noelia Lara Fuellac
a Laboratorio de Microbiología, Hospital General La Mancha Centro, Alcázar de San Juan, Ciudad Real, Spain
b Servicio de Medicina Preventiva, Hospital General La Mancha Centro, Alcázar de San Juan, Ciudad Real, Spain
c Laboratorio de Resistencia a Antibióticos, Centro Nacional de Microbiología, ISCIII, Majadahonda, Madrid, Spain
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In recent years&#44; rapid phenotypic and molecular tests have been developed to detect CPE&#44; including MALDI-TOF technology&#46;<a class="elsevierStyleCrossRefs" href="#bib0020"><span class="elsevierStyleSup">4&#8211;7</span></a> In 2014&#44; an 11&#44;109-Da peak was identified on the spectrum provided by MALDI-TOF mass spectrometry &#40;MS&#41;&#44; corresponding to the pKpQIL&#95;p019 protein&#44; encoded in a plasmid carrying the <span class="elsevierStyleItalic">bla<span class="elsevierStyleInf">KPC</span></span> gene&#46;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">Our objectives were to review KPC-3 carbapenemase-producing <span class="elsevierStyleItalic">Klebsiella pneumoniae</span> &#40;KPN&#41; isolates from 2 hospitals in Castilla&#8211;La Mancha&#44; and to determine the diagnostic efficacy of MALDI-TOF in their detection&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Material and methods</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Design and variables collected</span><p id="par0020" class="elsevierStylePara elsevierViewall">A retrospective study of the KPC-3&#8211;producing KPN strains isolated at 2 hospitals in Ciudad Real &#40;Hospital General La Mancha Centro &#91;Central La Mancha General Hospital&#93;&#44; HGMC&#44; and Hospital General de Tomelloso &#91;Tomelloso General Hospital&#93;&#44; HGT&#41; between 2016 and June 2019 &#40;one isolate per patient&#41;&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">Patients&#8217; medical records were reviewed and the following data were collected&#58; name&#44; age&#44; sample type&#44; strain sensitivity&#44; infection acquisition &#40;hospital-acquired&#44; community-acquired or healthcare-related&#58; nursing home or admission in the previous 6 months&#41;&#44; underlying diseases&#44; antibiotic therapy received in the previous 6 months&#44; instrument use &#40;catheter&#44; parenteral&#47;enteral nutrition or other&#41;&#44; antibiotic therapy received to treat the infection&#44; and death within a month from isolation&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Microbiology and clonality study</span><p id="par0030" class="elsevierStylePara elsevierViewall">Identification of bacteria and testing for sensitivity to antimicrobials were performed using the Vitek2&#174; and Vitek-MS&#174; system &#40;version 3&#46;2 IVD&#41; and Etest diffusion gradient strips &#40;BioM&#233;rieux&#41;&#44; according to EUCAST criteria&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">In cases in which we detected a decrease in sensitivity to any carbapenem&#44; we confirmed the presence or absence of carbapenemase production using the &#946; CARBA test &#40;Bio-Rad&#41;&#59; in positive cases&#44; the phenotype study was extended through synergy of meropenem with phenylboronic acid&#44; cloxacillin&#44; dipicolinic acid and sensitivity to temocillin &#40;Rosco Diagnostica&#41;&#46; To detect intestinal colonisation by the study strain&#44; chromID&#8482; Carba SMART Agar screening plates &#40;BioM&#233;rieux&#41; were used&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">A total of 31 isolates were sent to the Antibiotic Resistance Laboratory at the Centro Nacional de Microbiolog&#237;a &#91;National Centre for Microbiology&#93; for genotypic characterisation of the mechanism of resistance involved &#40;PCR and sequencing&#41; and molecular epidemiology testing using pulsed-field gel electrophoresis &#40;PFGE&#41; following digestion of total DNA with the <span class="elsevierStyleItalic">XbaI</span> restriction enzyme and multilocus sequence typing &#40;MLST&#41;&#46; Representative strains were selected &#40;isolates from the 4 study years&#44; from different sources and locations&#41;&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">The KPC-specific peak &#40;11&#46;109<span class="elsevierStyleHsp" style=""></span>kDa<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>15&#41;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a> was detected prospectively &#40;January 2019&#41; by means of a visual search on the spectrum provided by MALDI-TOF for KPN isolates&#46;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a> The isolates came from colonies and positive blood cultures following short-term subculture &#40;4<span class="elsevierStyleHsp" style=""></span>h on chocolate agar&#41;&#46; Only the matrix was added to the colony&#44; with processing once dry&#46; The results were compared to the results of the &#946; CARBA test and the disc synergy test&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Epidemiological study</span><p id="par0050" class="elsevierStylePara elsevierViewall">Intestinal colonisation testing was performed on all patients with positive clinical samples and those with whom they shared a room at the time of isolation&#46; To do so&#44; weekly rectal swabs were taken until hospital discharge or acquisition of 3 consecutive negative colonisation results&#46;</p><p id="par0055" class="elsevierStylePara elsevierViewall">In 2019&#44; an active search was conducted for a possible water reservoir &#40;traps&#44; taps and drains&#41;&#59; paper dispensers at both hospitals were also examined as potential reservoirs&#46;</p></span></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Results</span><p id="par0060" class="elsevierStylePara elsevierViewall">KPC-3&#8211;producing KPN was first isolated in 2016 at HGMC in an outbreak that affected 13 patients &#40;11 at HGMC and 2 at HGT&#41; and was managed with standard measures &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; The first isolate at HGT came from a patient who had been admitted to HGMC in the previous month&#59; the second isolate was 6 months later on the same hospital ward&#46; In 2018&#44; a patient who had been hospitalised at the same time and on the same ward as the two patients in 2016 was admitted to HGT&#46; In August 2018&#44; a second outbreak affected 28 patients &#40;26 at HGT and 2 at HGMC&#41;&#46; In 2019&#44; it was once again spread widely by both hospitals &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0065" class="elsevierStylePara elsevierViewall">In the study period&#44; 156 KPC-3&#8211;producing KPN strains were isolated&#59; these accounted for 90&#37; of all CPE and 93&#37; of carbapenemase-producing KPN in the same period &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; Full sequencing revealed the presence of the <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">KPC-3</span> gene&#46; All the strains studied showed a single PFGE profile belonging to ST512 &#40;one of them had been previously detected at another hospital in the same province&#41;&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0070" class="elsevierStylePara elsevierViewall">The median age of the patients was 83 years &#40;45&#8211;98&#41;&#44; and 58&#37; were women&#46; Of the samples&#44; 65&#37; were rectal exudate and 24&#37; were urine&#46; There were 3 cases of bacteraemia&#46; 84&#37; were of nosocomial origin and all others were healthcare-related &#40;31&#37; came from nursing homes&#41;&#46; 90&#37; had received at least one antibiotic in the previous 6 months&#44; instrument use had occurred in 72&#37; of cases&#44; and 92&#37; had an underlying disease&#46; There was a 31&#37; rate of death in the month of isolation&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">The strains showed broad antibiotic resistance&#44; being sensitive only to colistin &#40;apart from 2 strains which tested negative for the <span class="elsevierStyleItalic">mrc</span> gene&#41;&#44; tigecycline &#40;24&#37;&#41; and&#47;or gentamicin &#40;62&#37;&#41;&#46; 25&#37; of patients were infected &#40;3 previously colonised patients developed an infection&#41;&#59; 38&#37; received an aminoglycoside&#44; 31&#37; received a carbapenem and 27&#37; received colistin or tigecycline&#46; 62&#37; received combination therapy&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">The characteristic KPC peak &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41; was detected in 90&#37; of strains carrying the <span class="elsevierStyleItalic">bla<span class="elsevierStyleInf">KPC-3</span></span> gene and enabled direct identification in all blood cultures studied&#44; with a sensitivity of 90&#37;&#44; a specificity and positive predictive value &#40;PPV&#41; of 100&#37; and a negative predictive value &#40;NPV&#41; of 75&#37; &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#41;&#46; The rate of correlation with the phenotype tests examined was 100&#37;&#46; Low adherence to proper hand hygiene was seen among the staff involved&#46; We did not detect any environmental reservoir&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><elsevierMultimedia ident="tbl0010"></elsevierMultimedia></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Discussion</span><p id="par0085" class="elsevierStylePara elsevierViewall">We report the clonal spread of an extremely resistant KPC-3&#8211;producing KPN ST512 strain among the different healthcare levels in a healthcare area in Castilla&#8211;La Mancha &#40;Spain&#41;&#46; This clone is commonly associated with multidrug resistance and is considered to be of high epidemiological risk due to its extensive global distribution&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> It was first detected in Spain in 2012 at a hospital in C&#243;rdoba&#44; where it caused an outbreak with 67 infected patients&#59;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> the index case came from a hospital in Italy&#44;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a> where this clone had been previously reported&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> Following the appearance of the outbreak in our area&#44; the cumulative incidence of CPE went from 0&#46;01 in 2017 to 0&#46;24 in 2018&#59; however&#44; not until 2019 was there rapid spread of the strain due to continuous access on the part of the patients&#44; elderly individuals with multiple diseases&#44; between the internal medicine floor at both hospitals and various long-term care institutions&#44; resulting in an endemic caused by this clone in our healthcare area&#46;</p><p id="par0090" class="elsevierStylePara elsevierViewall">Multiple factors contributed to the spread of these isolates&#46; Given the fact that a reservoir was not located and the high rate of rectal colonisation&#44; indicating cross-contamination among patients and healthcare staff&#44; it was proposed that staff members&#8217; hands be screened&#46; This initiative was ultimately abandoned&#44; given the low rate of compliance with the hand-washing protocol&#44; ranging from 5&#37; to 89&#37;&#44;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> and a dearth of actions to be taken in the event of a positive result&#46;</p><p id="par0095" class="elsevierStylePara elsevierViewall">Visualisation of the characteristic peak on the MALDI-TOF spectrum enabled detection of KPC-3&#8211;producing KPN in routine culture identification&#44; though with a rate of diagnostic efficacy lower than that found in other studies&#44;<a class="elsevierStyleCrossRefs" href="#bib0070"><span class="elsevierStyleSup">14&#44;15</span></a> rendering it the fastest and cheapest phenotypic method for KPC detection&#46; As we did not directly detect carbapenemase&#44; sensitivity for detection will depend on the prevalence of clones carrying the plasmid in a given area&#46; The lack of a peak may have been due to a lack of protein expression or subjectivity in visualising the peak&#44; representing a study limitation&#46; The next step would be an automated search for the peak using the software on the apparatus&#46;<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a></p><p id="par0100" class="elsevierStylePara elsevierViewall">In conclusion&#44; we detected clonal spread of a strain of KPC-3&#8211;producing KPN ST512 at 3 hospitals in Ciudad Real&#46; To date&#44; the measures implemented have not proven effective for controlling the outbreak&#44; giving rise to an endemic situation&#46; We also demonstrated MALDI-TOF&#8217;s efficacy in the early detection of these strains&#44; with the clinical implications that this entails&#44; at no additional cost&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Conflicts of interest</span><p id="par0105" class="elsevierStylePara elsevierViewall">None&#46;</p></span></span>"
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        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Introduction&#47;Objective</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">To describe an outbreak of KPC-3-producing <span class="elsevierStyleItalic">Klebsiella pneumoniae</span> &#40;KPN&#41; and determine the diagnostic efficacy of MALDI-TOF in its detection&#46;</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Methods</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Retrospective study of the KPC-3-KPN isolated in 2 hospitals in Ciudad Real&#46; The peak at 11&#44;109<span class="elsevierStyleHsp" style=""></span>kDa<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>15 was sought in the KPN spectra provided by MALDI-TOF&#46;</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">We isolated 156 KPN strains that carried the <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">KPC-3</span> gene&#44; with a unique profile belonging to ST512 &#40;31 strains studied&#41;&#46; There was 25&#37; of infected patients&#44; 84&#37; were nosocomial or related to health care and 93&#37; had some underlying disease &#40;31&#37; of exitus in the first month&#41;&#46;</p><p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">The detection of the peak showed 90&#37; sensitivity and 100&#37; specificity&#46;</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Conclusions</span><p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">We detected the clonal spread of a KPN ST512 strain producing KPC-3 in 3 hospitals in Ciudad Real&#46; In addition&#44; we show the profitability of MALDI-TOF in the early detection of KPC-KPN&#46;</p></span>"
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        "resumen" => "<span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Introducci&#243;n&#47;Objetivo</span><p id="spar0060" class="elsevierStyleSimplePara elsevierViewall">Describir un brote por <span class="elsevierStyleItalic">Klebsiella pneumoniae</span> &#40;KPN&#41; productora de KPC-3 y determinar la eficacia diagn&#243;stica de MALDI-TOF en su detecci&#243;n&#46;</p></span> <span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">M&#233;todos</span><p id="spar0065" class="elsevierStyleSimplePara elsevierViewall">Estudio retrospectivo de las KPN-KPC-3 aisladas en 2 hospitales de Ciudad Real&#46; Se busc&#243; el pico a 11&#44;109<span class="elsevierStyleHsp" style=""></span>kDa<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>15 en el espectro proporcionado por MALDI-TOF para KPN&#46;</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0070" class="elsevierStyleSimplePara elsevierViewall">Se aislaron 156 cepas de KPN que portaban el gen <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">KPC-3</span>&#44; con un &#250;nico perfil perteneciente al ST512 &#40;31 cepas estudiadas&#41;&#46; Hubo un 25&#37; de infectados&#46; Un 84&#37; tuvieron origen nosocomial o relacionado con la asistencia sanitaria&#46; El 93&#37; ten&#237;a alguna enfermedad de base &#40;31&#37; de exitus en el primer mes&#41;&#46;</p><p id="spar0075" class="elsevierStyleSimplePara elsevierViewall">La detecci&#243;n del pico mostr&#243; una sensibilidad del 90&#37; y una especificidad del 100&#37;&#46;</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusiones</span><p id="spar0080" class="elsevierStyleSimplePara elsevierViewall">Detectamos la diseminaci&#243;n clonal de una cepa de KPN ST512 productora de KPC-3 en 3 hospitales de Ciudad Real&#46; Adem&#225;s&#44; evidenciamos la rentabilidad de MALDI-TOF en la detecci&#243;n precoz de KPN-KPC&#46;</p></span>"
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">2019<a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Total&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">KPC&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">13&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">28&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">113&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">156&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">OXA-48&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">6&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">10&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">VIM&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Total&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">19&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">6&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">29&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">113&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">167&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
              ]
              "imagenFichero" => array:1 [
                0 => "xTab2510826.png"
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            0 => array:3 [
              "identificador" => "tblfn0005"
              "etiqueta" => "a"
              "nota" => "<p class="elsevierStyleNotepara" id="npar0005">January to July 2019&#46;</p>"
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          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Carbapenemase-producing <span class="elsevierStyleItalic">Klebsiella pneumoniae</span> isolates during outbreak&#46;</p>"
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          0 => array:3 [
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        "tabla" => array:2 [
          "leyenda" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">KPN&#58; <span class="elsevierStyleItalic">K&#46; pneumoniae</span>&#46;</p>"
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            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="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Presence of peak &#40;11&#44;109<span class="elsevierStyleHsp" style=""></span>kDa<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>15&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Absence of peak &#40;11&#44;109<span class="elsevierStyleHsp" style=""></span>kDa<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>15&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Total&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">KPC-3-producing KPN&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">102&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">11&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">113&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">KPN&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">54&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">54&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
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      "titulo" => "References"
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        0 => array:2 [
          "identificador" => "bibs0005"
          "bibliografiaReferencia" => array:15 [
            0 => array:3 [
              "identificador" => "bib0005"
              "etiqueta" => "1"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "The threat of the carbapenemase-producing Enterobacteriaceae in Spain&#58; Positioning report of the SEIMC study groups&#44; GEIH and GEMARA"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => true
                          "autores" => array:6 [
                            0 => "J&#46; Oteo"
                            1 => "E&#46; Calbo"
                            2 => "J&#46; Rodr&#237;guez-Ba&#241;o"
                            3 => "A&#46; Oliver"
                            4 => "A&#46; Hornero"
                            5 => "P&#46; Ruiz-Garbajosa"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1016/j.eimc.2014.02.011"
                      "Revista" => array:6 [
                        "tituloSerie" => "Enferm Infecc Microbiol Clin"
                        "fecha" => "2014"
                        "volumen" => "32"
                        "paginaInicial" => "666"
                        "paginaFinal" => "670"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/24767691"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            1 => array:3 [
              "identificador" => "bib0010"
              "etiqueta" => "2"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Carbapenemase-producing <span class="elsevierStyleItalic">Enterobacteriaceae</span> in Spain in 2012"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => true
                          "autores" => array:6 [
                            0 => "J&#46; Oteo"
                            1 => "D&#46; Saez"
                            2 => "V&#46; Bautista"
                            3 => "S&#46; Fern&#225;ndez-Romero"
                            4 => "J&#46;M&#46; Hern&#225;ndez-Molina"
                            5 => "M&#46; P&#233;rez-V&#225;zquez"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1128/AAC.01513-13"
                      "Revista" => array:6 [
                        "tituloSerie" => "Antimicrob Agents Chemother"
                        "fecha" => "2013"
                        "volumen" => "57"
                        "paginaInicial" => "6344"
                        "paginaFinal" => "6347"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/24041898"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            2 => array:3 [
              "identificador" => "bib0015"
              "etiqueta" => "3"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "The epidemiology of carbapenem-resistant Enterobacteriaceae&#46; The impact and evolution of a global menace"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:2 [
                            0 => "L&#46; Logan"
                            1 => "R&#46; Weinstein"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1093/infdis/jiw521"
                      "Revista" => array:7 [
                        "tituloSerie" => "J Infect Dis"
                        "fecha" => "2017"
                        "volumen" => "215"
                        "numero" => "Suppl&#46; 1&#58;S2"
                        "paginaInicial" => "8"
                        "paginaFinal" => "36"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/27803170"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            3 => array:3 [
              "identificador" => "bib0020"
              "etiqueta" => "4"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Comparison of Carba NP-Direct&#44; Carbapenem Inactivation Method&#44; and &#946;-CARBA Tests for Detection of Carbapenemase Production in <span class="elsevierStyleItalic">Enterobacteriaceae</span>"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:5 [
                            0 => "B&#46; Bayraktar"
                            1 => "A&#46; Bar&#305;&#351;"
                            2 => "G&#46; Malko&#231;o&#287;lu"
                            3 => "D&#46; Erdemir"
                            4 => "N&#46; K&#305;na"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1089/mdr.2017.0427"
                      "Revista" => array:6 [
                        "tituloSerie" => "Microb Drug Resist"
                        "fecha" => "2019"
                        "volumen" => "25"
                        "paginaInicial" => "97"
                        "paginaFinal" => "102"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/29694266"
                            "web" => "Medline"
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                      ]
                    ]
                  ]
                ]
              ]
            ]
            4 => array:3 [
              "identificador" => "bib0025"
              "etiqueta" => "5"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Rapid detection of carbapenemase genes by multiplex real-time PCR"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:5 [
                            0 => "J&#46; Monteiro"
                            1 => "R&#46;H&#46; Widen"
                            2 => "A&#46;C&#46; Pignatari"
                            3 => "C&#46; Kubasek"
                            4 => "S&#46; Silbert"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1093/jac/dkr563"
                      "Revista" => array:6 [
                        "tituloSerie" => "J Antimicrob Chemother&#46;"
                        "fecha" => "2012"
                        "volumen" => "67"
                        "paginaInicial" => "906"
                        "paginaFinal" => "909"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/22232516"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            5 => array:3 [
              "identificador" => "bib0030"
              "etiqueta" => "6"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Detection of NDM-1&#44; VIM-1&#44; KPC&#44; OXA-48&#44; and OXA-162 carbapenemases by matrixassisted laser desorption ionization&#8211;time of flight mass spectrometry"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => true
                          "autores" => array:6 [
                            0 => "J&#46; Hrab&#225;k"
                            1 => "V&#46; Studentov&#225;"
                            2 => "R&#46; Walkov&#225;"
                            3 => "H&#46; Zemlickov&#225;"
                            4 => "V&#46; Jakubu"
                            5 => "E&#46; Chud&#225;ckov&#225;"
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1128/JCM.01002-12"
                      "Revista" => array:6 [
                        "tituloSerie" => "J Clin Microbiol"
                        "fecha" => "2012"
                        "volumen" => "50"
                        "paginaInicial" => "2441"
                        "paginaFinal" => "2443"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/22553235"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            6 => array:3 [
              "identificador" => "bib0035"
              "etiqueta" => "7"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
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ISSN: 2529993X
Original language: English
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es en pt

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