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Original article
Reporting antimicrobial susceptibilities and phenotypes of resistance to vancomycin in vancomycin-resistant Enterococcus spp. clinical isolates: A nationwide proficiency study
Informe de sensibilidad antimicrobiana y fenotipos de resistencia a vancomicina en aislados clínicos de Enterococcus spp. resistentes a vancomicina: estudio multicéntrico nacional
Felipe Fernández-Cuencaa,b,c,
Corresponding author
felipefc@us.es

Corresponding author.
, Inmaculada López-Hernándeza,b,c, Emilia Cercenadod,e,f, María Carmen Conejog, Nuria Tormoh,i, Concepción Gimenoh,i, Alvaro Pascuala,b,c,g
a Unidad Clínica de Enfermedades Infecciosas y Microbiología Clínica, Hospital Universitario Virgen Macarena, Sevilla, Spain
b Instituto de Biomedicina de Sevilla (IBIs), Hospital Universitario Virgen Macarena/CSIC/Universidad de Sevilla, Sevilla, Spain
c Spanish Network for the Research in Infectious Diseases (REIPI RD16/0016), Instituto de Salud Carlos III, Madrid, Spain
d Servicio de Microbiología y Enfermedades Infecciosas. Hospital General Universitario Gregorio Marañón, Madrid, Spain
e Departamento de Medicina, Facultad de Medicina, Universidad Complutense, Madrid, Spain
f CIBERES, Centro de Investigación Biomédica en Red de Enfermedades Respiratorias, CB06/06/0058, Madrid, Spain
g Departamento de Microbiología, Universidad de Sevilla, Sevilla, Spain
h Servicio de Microbiología, Hospital General de Valencia, Valencia, Spain
i Quality Control Programme (CCS), Spanish Society of Clinical Microbiology and Infectious Diseases (SEIMC), Valencia, Spain
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such as cephalosporins and aminoglycosides&#59; <span class="elsevierStyleItalic">E&#46; faecium&#44;</span> included in the ESKAPE group of pathogens&#44; is more frequently resistant to vancomycin and ampicillin than <span class="elsevierStyleItalic">E&#46; faecalis</span>&#46;<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">1</span></a> Vancomycin is frequently used as first-line treatment for severe infections caused by ampicillin-resistant enterococci&#59; however&#44; vancomycin resistance &#40;VR&#41; is increasingly being reported worldwide&#46; In Europe&#44; according to the 2019 European Antimicrobial Resistance Surveillance Network &#40;EARS-Net&#41;&#44; VR among <span class="elsevierStyleItalic">E&#46; faecalis</span> isolates remained low in most EU&#47;EEA countries&#44; whereas among <span class="elsevierStyleItalic">E&#46; faecium</span>&#44; the population-weighted mean percentage increased from 10&#46;5&#37; in 2015 to 17&#46;3&#37; in 2019&#46;<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">2</span></a> The main mechanism of VR in enterococci involves a substitution of the <span class="elsevierStyleSmallCaps">d</span>-Alanine-<span class="elsevierStyleSmallCaps">d</span>-Alanine in the peptidoglycan leading to variable expressions of VR&#46; Most operons related to VR in enterococci &#40;<span class="elsevierStyleItalic">vanA&#44; -B&#44; -C&#44; -D&#44; -E&#44; -G&#44; -L&#44; -M</span>&#44; and <span class="elsevierStyleItalic">N</span>&#41; differ in their degree of VR&#44; location &#40;chromosome and plasmid&#41;&#44; transferability&#44; and phenotypic expression &#40;constitutive or inducible&#41;&#46; The <span class="elsevierStyleItalic">vanA</span> and <span class="elsevierStyleItalic">vanB</span> gene clusters are the most frequently implicated in VRE outbreaks&#46; The <span class="elsevierStyleItalic">vanA</span> gene cluster is associated frequently with transposons &#40;Tn&#41;&#44; such as Tn<span class="elsevierStyleItalic">1546</span>&#44; and it is formed by seven genes&#46; The <span class="elsevierStyleItalic">vanR</span> &#40;response regulator&#41; and <span class="elsevierStyleItalic">vanS</span> &#40;sensor kinase&#41; gene products constitute the two-component system regulatory apparatus&#46; The <span class="elsevierStyleItalic">vanHXA</span> gene cluster is essential for VR&#46; The <span class="elsevierStyleItalic">vanH</span> and <span class="elsevierStyleItalic">vanA</span> code for a dehydrogenase that converts pyruvate to lactate &#40;VanH&#41;&#44; and for a ligase that forms <span class="elsevierStyleSmallCaps">d</span>-Alanine-<span class="elsevierStyleSmallCaps">d</span>-lactate dipeptide &#40;VanA&#41;&#44; which are implicated in the modification of peptidoglycan precursors&#44; whereas the <span class="elsevierStyleItalic">vanX</span> &#40;dipeptidase that cleaves <span class="elsevierStyleSmallCaps">d</span>-Alanine-<span class="elsevierStyleSmallCaps">d</span>-Alanine&#41; and <span class="elsevierStyleItalic">vanY</span> &#40;<span class="elsevierStyleSmallCaps">d</span>&#44;<span class="elsevierStyleSmallCaps">d</span>-carboxypeptidase&#41; are implicated in the hydrolysis and interruption of the pentapeptides&#46; VanA-resistant strains show high-level resistance to vancomycin &#40;MICs<span class="elsevierStyleHsp" style=""></span>&#8805;<span class="elsevierStyleHsp" style=""></span>64<span class="elsevierStyleHsp" style=""></span>mg&#47;l&#41; and teicoplanin &#40;MICs&#44; &#8805;16<span class="elsevierStyleHsp" style=""></span>mg&#47;l&#41;&#46;<a class="elsevierStyleCrossRefs" href="#bib0165"><span class="elsevierStyleSup">3&#8211;5</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">The typical <span class="elsevierStyleItalic">vanB</span> operon has a similar genetic backbone to <span class="elsevierStyleItalic">vanA</span>&#46; The <span class="elsevierStyleItalic">vanHBX</span> gene cluster is essential for VR and it can be associated to transposons such as Tn<span class="elsevierStyleItalic">1547</span>&#44; Tn<span class="elsevierStyleItalic">1549</span>&#44; and Tn<span class="elsevierStyleItalic">5382</span>&#46; The conjugative Tn<span class="elsevierStyleItalic">1549</span> is widely prevalent and it is mainly a chromosomal transposon&#46; Isolates with the VanB resistance phenotype &#40;<span class="elsevierStyleItalic">vanB-1</span> and <span class="elsevierStyleItalic">vanB-2</span> subtypes&#41; are resistant to variable levels of vancomycin &#40;MICs&#44; 4&#8211;&#62;1000<span class="elsevierStyleHsp" style=""></span>mg&#47;l&#41; but are generally susceptible to teicoplanin&#46; VanB strains however may also exhibit resistance to teicoplanin and thus be phenotypically indistinguishable from VanA strains&#46;<a class="elsevierStyleCrossRefs" href="#bib0165"><span class="elsevierStyleSup">3&#8211;5</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">The <span class="elsevierStyleItalic">vanC</span> operon is genetically different from <span class="elsevierStyleItalic">vanA</span> and <span class="elsevierStyleItalic">vanB</span>&#44; and it is typically present in &#8220;less virulent&#8221; enterococci than those carrying inducible <span class="elsevierStyleItalic">vanA</span> and <span class="elsevierStyleItalic">vanB</span> gene clusters&#46; The <span class="elsevierStyleItalic">vanC</span>-resistant subtypes&#44; <span class="elsevierStyleItalic">vanC-1</span>&#44; <span class="elsevierStyleItalic">vanC-2</span>&#44; and <span class="elsevierStyleItalic">vanC-3</span>&#44; are known to be intrinsically present in <span class="elsevierStyleItalic">E&#46; gallinarum</span>&#44; <span class="elsevierStyleItalic">E&#46; casseliflavus</span>&#44; and <span class="elsevierStyleItalic">E&#46; flavescens</span>&#44; respectively&#44; which display low-level resistance to vancomycin &#40;MICs&#44; 4&#8211;32<span class="elsevierStyleHsp" style=""></span>mg&#47;ml&#41; and susceptibility to teicoplanin&#46;<a class="elsevierStyleCrossRefs" href="#bib0165"><span class="elsevierStyleSup">3&#8211;5</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">Reliable antimicrobial susceptibility results and the recognition of VR phenotypes in the laboratory can directly impact outcome in VRE-infected patients because the treatment options available are limited and the probability of therapeutic failure is high&#46;<a class="elsevierStyleCrossRefs" href="#bib0180"><span class="elsevierStyleSup">6&#44;7</span></a></p><p id="par0030" class="elsevierStylePara elsevierViewall">Unreliable antimicrobial susceptibility results have been related to several factors&#44; such as species identification&#44; type of acquired resistance mechanism&#44; and the methodology used &#40;broth microdilution <span class="elsevierStyleItalic">versus</span> disk diffusion&#41;&#46;<a class="elsevierStyleCrossRefs" href="#bib0190"><span class="elsevierStyleSup">8&#8211;11</span></a> The clinical breakpoints applied&#44; as well as the inducibility of resistance and the possibility of resistance development during treatment&#44; can also affect the interpretation of susceptibility results&#46;<a class="elsevierStyleCrossRefs" href="#bib0210"><span class="elsevierStyleSup">12&#8211;14</span></a> These challenges led us to perform the present study with the aim of evaluating the ability of Spanish clinical microbiology laboratories &#40;a&#41; to determine the antimicrobial susceptibility of VRE&#44; and &#40;b&#41; to correctly detect different VR phenotypes&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Materials and methods</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Bacterial isolates&#44; species identification and antimicrobial susceptibility testing</span><p id="par0035" class="elsevierStylePara elsevierViewall">Three <span class="elsevierStyleItalic">Enterococcus</span> spp&#46; isolates &#40;CC-01&#44; CC-02 and CC-03&#41; representing the VanA&#44; VanB and VanC-1 VR phenotypes were selected for this study &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; These VR phenotypes were characterized phenotypically&#44; determining the MICs of vancomycin and teicoplanin &#40;see below&#41;&#44; and genetically&#44; detecting the vancomycin resistance genes <span class="elsevierStyleItalic">vanA</span>&#44; <span class="elsevierStyleItalic">vanB</span> and <span class="elsevierStyleItalic">vanC-1</span> by PCR amplification and DNA sequencing with specific primers for <span class="elsevierStyleItalic">vanA</span>&#44; <span class="elsevierStyleItalic">vanB</span> and <span class="elsevierStyleItalic">vanC&#46;</span><a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">12</span></a> All isolates were collected from patients admitted to the University Hospital Gregorio Mara&#241;&#243;n &#40;Madrid&#44; Spain&#41;&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0040" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">E&#46; faecalis</span> ATCC 29212 was used as quality control strain for antimicrobial susceptibility testing&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">Bacterial identification&#44; antimicrobial susceptibility and confirmation of the phenotype and genotype of VR were verified independently by two clinical microbiology reference laboratories&#58; the Hospital Universitario Virgen Macarena &#40;Seville&#44; Spain&#41;&#44; and the Hospital General Universitario Gregorio Mara&#241;&#243;n &#40;Madrid&#44; Spain&#41;&#46; The isolates were identified using conventional microbiological tests and MALDI-TOF &#40;Bruker Daltonics&#44; Madrid&#44; Espa&#241;a&#41;&#46; The antimicrobials tested were&#58; ampicillin&#44; imipenem&#44; vancomycin&#44; teicoplanin&#44; linezolid&#44; daptomycin&#44; ciprofloxacin&#44; levofloxacin&#44; gentamicin &#40;high-level resistance&#41;&#44; streptomycin &#40;high-level resistance&#41; and quinupristin&#8211;dalfopristin&#46; All antimicrobials were tested in duplicate at each reference center by broth microdilution and disk diffusion&#44; according to EUCAST and CLSI guidelines&#46;<a class="elsevierStyleCrossRefs" href="#bib0225"><span class="elsevierStyleSup">15&#44;16</span></a> The 2018 EUCAST and CLSI breakpoints were used for the interpretation of clinical categories&#46;<a class="elsevierStyleCrossRefs" href="#bib0225"><span class="elsevierStyleSup">15&#44;16</span></a> The EUCAST breakpoints used for ciprofloxacin and levofloxacin were those reported for uncomplicated urinary tract infections&#46; Quinupristin&#8211;Dalfopristin susceptibility results for isolate CC-03 &#40;<span class="elsevierStyleItalic">E&#46; gallinarum vanC-1</span>&#41; were not included in the analysis because neither EUCAST nor CLSI have breakpoints for quinupristin&#8211;dalfopristin in enterococcal species other than <span class="elsevierStyleItalic">E&#46; faecium</span>&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Study design</span><p id="par0050" class="elsevierStylePara elsevierViewall">Isolates were sent in Amies transport medium to 52 participating hospitals in October 2018&#46; The instructions specified that isolates should be treated as blood culture isolates&#46; Participating laboratories were requested to fill in an electronic form for each isolate&#44; which included&#58; &#40;a&#41; method used for AST&#59; &#40;b&#41; MIC values of ampicillin&#44; imipenem&#44; vancomycin&#44; teicoplanin&#44; linezolid&#44; daptomycin&#44; ciprofloxacin&#44; levofloxacin quinupristin&#8211;dalfopristin&#44; and high-level resistance to gentamicin and streptomycin&#59; &#40;c&#41; breakpoint used for clinical category interpretation &#40;CLSI or EUCAST&#41;&#59; and &#40;d&#41; inference or detection of the phenotype of resistance to vancomycin &#40;VanA&#44; Van B or VanC&#41;&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Data analysis</span><p id="par0055" class="elsevierStylePara elsevierViewall">The analysis of results consisted of&#58; &#40;a&#41; a descriptive analysis of AST methods&#44; breakpoints applied&#44; clinical category assigned&#59; &#40;b&#41; an analysis of discrepancies in MIC values&#59; &#40;c&#41; an analysis of category error rates &#91;minor errors &#40;mEs&#41;&#44; major errors &#40;MEs&#41; and very major errors &#40;VMEs&#41;&#59; and &#40;iv&#41; the ability of participating laboratories to accurately infer or detect the phenotype of VR&#46;<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">17</span></a></p><p id="par0060" class="elsevierStylePara elsevierViewall">It was considered that there was a discrepancy in the MIC value of any antimicrobial tested when the MIC provided by the participating laboratory was not within a single 2-fold dilution &#40;&#177;1 doubling dilution&#41; of the reference MIC result&#46;</p></span></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Results</span><p id="par0065" class="elsevierStylePara elsevierViewall">Fifty-one out of the 52 centers invited to participate in this study responded to the questions related to the type of AST system used&#44; the MICs obtained for the antimicrobials tested&#44; the clinical breakpoints applied&#44; and the type of VR phenotype identified&#46;</p><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Type of AST system</span><p id="par0070" class="elsevierStylePara elsevierViewall">One thousand and nine MIC determinations were analyzed&#46; The percentage distribution of MIC determinations obtained with each AST system used was&#58; 60&#46;2&#37; &#40;607&#47;1009&#41; with MicroScan WalkAway &#40;Beckman Coulter Inc&#46;&#44; Brea&#44; CA&#44; USA&#41;&#59; 29&#46;5&#37; &#40;298&#47;1009&#41; with Vitek 2 &#40;bioM&#233;rieux&#44; Marcy-l&#8217;&#201;toile&#44; France&#41;&#59; 5&#46;9&#37; &#40;60&#47;1009&#41; with gradient strips &#40;Etest&#174;&#44; bioM&#233;rieux&#41;&#59; 2&#46;7&#37; &#40;27&#47;1009&#41; using an in-house broth microdilution test&#59; and 1&#46;7&#37; &#40;17&#47;1009&#41; with Phoenix &#40;BD Biosciences&#44; Sparks&#44; MD&#44; USA&#41;&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Discrepancies in the MICs</span><p id="par0075" class="elsevierStylePara elsevierViewall">Analysis of discrepant MICs according to AST system revealed that the gradient strip from bioM&#233;rieux was the least accurate method for AST&#44; with 21&#46;3&#37; of discrepant MICs &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#41;&#46;</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0080" class="elsevierStylePara elsevierViewall">By antimicrobial&#44; the percentages of discrepant MICs were 16&#46;7&#37; for imipenem&#44; 13&#46;0&#37; for ampicillin&#44; 9&#46;2&#37; for teicoplanin&#44; 2&#46;0&#37; for vancomycin&#44; 1&#46;9&#37; for quinupristin&#8211;dalfopristin&#44; 1&#46;4&#37; for ciprofloxacin&#44; 0&#46;7&#37; for linezolid&#44; and no discrepancies in the MICs of daptomycin&#44; levofloxacin&#44; and HLR to gentamicin or streptomycin were observed &#40;<a class="elsevierStyleCrossRef" href="#tbl0015">Table 3</a>&#41;&#46;</p><elsevierMultimedia ident="tbl0015"></elsevierMultimedia></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Clinical breakpoints used and category errors</span><p id="par0085" class="elsevierStylePara elsevierViewall">With respect to clinical breakpoint&#44; 65&#46;3&#37; of MICs reported were interpreted using EUCAST-2018 breakpoints&#44; and 34&#46;7&#37; with CLSI-2018 breakpoints&#46;</p><p id="par0090" class="elsevierStylePara elsevierViewall">Regarding clinical category errors according to AST system &#40;see <a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#41;&#44; VMEs were observed with all the AST methods used&#44; particularly gradient strips &#40;14&#46;8&#37; with EUCAST breakpoints and 12&#46;1&#37; with CLSI&#41;&#46; The percentage of MEs was 0&#46;5&#37; with CLSI&#44; and no mEs were obtained&#46;</p><p id="par0095" class="elsevierStylePara elsevierViewall">With respect to the breakpoint used&#44; the overall percentage of VMEs obtained was 5&#46;3&#37; with EUCAST and 4&#46;6&#37; with CLSI breakpoints&#46; By contrast&#44; the percentage of MEs were 0&#46;2&#37; with EUCAST and 0&#46;3&#37; with CLSI breakpoints&#44; and no mEs were obtained with either EUCAST or CLSI&#46; According to antimicrobial&#44; clinical category errors were detected for teicoplanin&#44; vancomycin&#44; ciprofloxacin&#44; and linezolid &#40;<a class="elsevierStyleCrossRef" href="#tbl0015">Table 3</a>&#41;&#46; VMEs occurred only with teicoplanin &#40;27&#46;1&#37; using EUCAST&#44; 33&#46;3&#37; with CLSI&#41; and vancomycin &#40;5&#46;7&#37; with EUCAST&#44; 2&#46;3&#37; with CLSI&#41; whereas the MEs were observed with ciprofloxacin &#40;5&#46;0&#37; using CLSI&#41; and linezolid &#40;1&#46;1&#37; using EUCAST&#41; &#40;<a class="elsevierStyleCrossRef" href="#tbl0015">Table 3</a>&#41;&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">For teicoplanin&#44; the percentage of VMEs related to clinical categorization obtained was associated with use of AST system &#40;62&#46;1&#37; MicroScan&#44; 24&#46;1&#37; Vitek 2&#44; 10&#46;3&#37; in-house broth microdilution&#44; and 3&#46;4&#37; Phoenix&#41;&#44; however these AST systems did not produce discrepant MIC values &#40;all &#8804;4<span class="elsevierStyleHsp" style=""></span>mg&#47;l&#41;&#46; On the contrary&#44; the VMEs were related to erroneous interpretation of MIC results &#40;see below&#41;&#46; For vancomycin&#44; and in contrast to teicoplanin&#44; the percentage of VMEs was caused by discrepant MICs &#8804;4<span class="elsevierStyleHsp" style=""></span>mg&#47;l &#40;MIC underestimation&#41;&#44; obtained using MicroScan &#40;83&#46;3&#37;&#41; and gradient strips &#40;16&#46;7&#37;&#41;&#46;</p><p id="par0105" class="elsevierStylePara elsevierViewall">The percentage of ciprofloxacin MEs was due to discrepant MICs of &#62;2<span class="elsevierStyleHsp" style=""></span>mg&#47;l &#40;MIC overestimation&#41;&#44; obtained using MicroScan and interpreted following CLSI breakpoints &#40;5&#46;0&#37;&#41;&#46; Similarly&#44; for linezolid&#44; the percentage of MEs was caused by MIC discrepancies of &#62;4<span class="elsevierStyleHsp" style=""></span>mg&#47;l &#40;MIC overestimation&#41; using MicroScan and EUCAST breakpoints &#40;1&#46;1&#37;&#41;&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0110">Identification of VR phenotypes</span><p id="par0110" class="elsevierStylePara elsevierViewall">The VanA and VanB phenotypes were correctly identified by 86&#46;4&#37; of the centers&#46; The VanC phenotype was reported by 95&#37; of the centers&#44; which reported this result as follows&#58; intrinsic resistance to glycopeptides &#40;10&#37;&#41;&#44; vanC phenotype &#40;47&#37;&#41;&#44; vanC-1 phenotype &#40;8&#37;&#41;&#44; and intrinsic resistance and VanC phenotype &#40;33&#37;&#41;&#46; All clinical category errors obtained for vancomycin and teicoplanin &#40;VMEs&#41; occurred with the VanB isolate&#59; for linezolid&#44; the errors &#40;MEs&#41; occurred with the VanA isolate&#44; and for ciprofloxacin &#40;MEs&#41;&#44; with the VanC isolate&#46;</p></span></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0115">Discussion</span><p id="par0115" class="elsevierStylePara elsevierViewall">Accurate AST in enterococci is essential for proper guidance of therapy&#44; particularly in immunocompromised patients with severe infections&#44; because of the high associated morbidity and mortality&#44; and for surveillance of antimicrobial resistance&#46;<a class="elsevierStyleCrossRefs" href="#bib0180"><span class="elsevierStyleSup">6&#44;18&#44;19</span></a></p><p id="par0120" class="elsevierStylePara elsevierViewall">The use of unreliable MIC-based AST systems can lead to inaccurately or wrongly estimated MIC values&#44; and to false-susceptible or false-resistant results&#44; which could in turn lead to failure in detecting nosocomial outbreaks caused by VRE isolates&#44; including those produced by hospital-associated linages and high risk clones&#44; such as clade A of <span class="elsevierStyleItalic">E&#46; faecium</span> and clusters PP2&#44; PP6&#44; PP7&#44; PP8 and PP20 of <span class="elsevierStyleItalic">E&#46; faecalis</span>&#46;<a class="elsevierStyleCrossRefs" href="#bib0250"><span class="elsevierStyleSup">20&#44;21</span></a></p><p id="par0125" class="elsevierStylePara elsevierViewall">The results of the present study show that discrepant MICs and category errors&#44; whether or not associated with erroneous MIC results&#44; are related to the AST system used&#44; the antimicrobial agent&#44; and the VR phenotype&#46;</p><p id="par0130" class="elsevierStylePara elsevierViewall">The gradient strip method was the least reliable form of AST&#44; due to both the high percentage of discrepant MIC results and the percentage of category errors&#44; especially VMEs for vancomycin and teicoplanin in the isolate with the VanB phenotype&#46; These results are similar to those described in previous reports&#44; in which gradient strips from Oxoid&#44; Liofilchem and bioM&#233;rieux showed very low sensitivity &#40;61&#37;&#8211;63&#37;&#41; for detection of teicoplanin resistance in a collection of <span class="elsevierStyleItalic">E&#46; faecium</span> isolates&#46;<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">22</span></a> The lack of reliability of MIC results using gradient strips could be related to several microbiological factors&#44; such as inappropriate inoculum preparation or problems related to growth visualization&#46; The limitation observed with gradient strips of vancomycin and teicoplanin would justify the use of more reliable alternative assays to avoid erroneous MIC results that could lead to false results of susceptibility &#40;VMEs&#41; and resistance &#40;MEs&#41;&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">The other non-automated AST method tested in the present study was an in-house broth microdilution method&#44; which also produced a high percentage of VMEs for teicoplanin&#59; nevertheless&#44; these results should be interpreted with caution due to the low number of MIC results reported by those centers that used this AST method&#46; As mentioned for gradient strips&#44; vancomycin and teicoplanin MIC results obtained by in-house broth microdilution assays should be confirmed with other more reliable AST assays because of the clinical relevance of these microbiological results&#46;</p><p id="par0140" class="elsevierStylePara elsevierViewall">The semi-automated AST systems used in this study &#40;MicroScan&#44; Vitek 2 and Phoenix&#41; produced a low and acceptable percentage of discrepant MICs&#44; and a high percentage of VMEs&#44; which were not related&#44; as discussed below&#44; with the use of the system&#44; indicating that they are reliable AST method for VRE&#46;</p><p id="par0145" class="elsevierStylePara elsevierViewall">With respect to the breakpoints used for clinical categorization&#44; those established by EUCAST were used twice as frequently as those of CLSI&#44; which is in line with the gradual implementation of EUCAST guidelines in Europe&#46;<a class="elsevierStyleCrossRefs" href="#bib0235"><span class="elsevierStyleSup">17&#44;23&#44;24</span></a> The errors obtained using EUCAST were slightly higher than those obtained with CLSI&#44; which may be related to factors such as the &#8220;I&#8221; category &#40;intermediate&#44; as for EUCAST 2018&#41;&#44; which was not defined by EUCAST for various antimicrobials &#40;e&#46;g&#46; glycopeptides&#44; linezolid&#44; imipenem and levofloxacin&#41;&#44; the wide MIC interval of the intermediate category&#41; for some antimicrobials using CLSI &#40;e&#46;g&#46; vancomycin&#41;&#44; the lower breakpoints defined by EUCAST for some antimicrobials &#40;e&#46;g&#46; teicoplanin&#41;&#44; or the absence of breakpoints for some antimicrobials &#40;e&#46;g&#46; daptomycin&#41; with respect to CLSI &#40;see below&#41;&#46;</p><p id="par0150" class="elsevierStylePara elsevierViewall">The type of antimicrobial was another factor contributing to MIC discrepancies and category errors&#46; The highest percentages of discrepant MICs were obtained with imipenem and ampicillin&#44; although the discrepancies were not associated with clinical category errors and should have no clinical impact&#46; On the other hand&#44; for teicoplanin&#44; vancomycin and ciprofloxacin&#44; although the discrepancies in MICs were low &#40;&#60;10&#37;&#41;&#44; they were associated with important errors &#40;VMEs for teicoplanin and vancomycin&#44; and MEs for ciprofloxacin&#41; which could have significant clinical and epidemiological impact&#46;</p><p id="par0155" class="elsevierStylePara elsevierViewall">There was an unexpectedly very high percentage of VMEs obtained with teicoplanin&#44; which was not related with obtaining discrepant MIC results with the AST system&#44; but due to the interpretation of the VanB phenotype as teicoplanin-susceptible&#44; in contrast to the EUCAST recommendations&#46; The results of previous studies have highlighted the development of teicoplanin resistance in VanB <span class="elsevierStyleItalic">E&#46; faecium</span> isolates&#44; both <span class="elsevierStyleItalic">in vitro</span> and <span class="elsevierStyleItalic">in vivo</span>&#44; leading to a high probability of therapeutic failure&#46;<a class="elsevierStyleCrossRefs" href="#bib0220"><span class="elsevierStyleSup">14&#44;25</span></a></p><p id="par0160" class="elsevierStylePara elsevierViewall">The VMEs obtained with vancomycin&#44; unlike those obtained with teicoplanin&#44; were much lower and were related to discrepant MICs&#44; particularly those generated by the use of MicroScan&#46; All the vancomycin VMEs were observed in the CC-2 VanB isolate&#44; and were true false susceptibilities associated with the reported vancomycin MICs&#44; which were in the susceptible range &#40;MIC of &#8804;4<span class="elsevierStyleHsp" style=""></span>mg&#47;l&#41;&#44; in an isolate that was VR&#46; It is important to highlight that false vancomycin susceptibility can represent a serious problem because this result is not routinely confirmed in the laboratory&#46; Furthermore&#44; failure to identify VRE isolates can lead to treatment failures that may be associated with increased mortality&#44; poor clinical outcome&#44; prolonged length of stay&#44; or reinfections&#46; Failure to recognize VRE may also have important epidemiological consequences&#44; since <span class="elsevierStyleItalic">vanA</span> and <span class="elsevierStyleItalic">vanB</span> can be mobilized via plasmid transfer&#44; contributing to the emergence of nosocomial outbreaks&#46;</p><p id="par0165" class="elsevierStylePara elsevierViewall">Ciprofloxacin was the only antimicrobial tested for which there were MEs &#40;5&#46;0&#37;&#41;&#44; but they may not have significant clinical implications&#46; Ciprofloxacin is not frequently used as a first-line treatment for VRE infections&#44; so that the clinical repercussions of reporting false ciprofloxacin resistance in VRE are scarce&#46; Nevertheless&#44; a report of ciprofloxacin as resistant may lead to the use of other antimicrobials with a broader spectrum and more toxic or with secondary effects&#44; such as vancomycin or teicoplanin&#46; The epidemiological impact of ciprofloxacin MEs is probably of low relevance since&#44; in general&#44; clinical ciprofloxacin resistance is not plasmid-encoded&#44; and ciprofloxacin&#44; is very infrequently used for the treatment of enterococcal infections&#46;</p><p id="par0170" class="elsevierStylePara elsevierViewall">The MEs with linezolid were acceptably low &#40;1&#46;1&#37;&#41;&#44; and their clinical implications should be similar to those reporting false ciprofloxacin resistance&#46; From a microbiological point of view&#44; it is important to confirm linezolid resistance with other AST systems&#44; or by using a molecular assay to detect plasmid-encoded <span class="elsevierStyleItalic">cfr</span>&#44; <span class="elsevierStyleItalic">optrA</span> and <span class="elsevierStyleItalic">poxtA</span> determinants&#44; due to their potential clinical and epidemiological relevance&#46;<a class="elsevierStyleCrossRef" href="#bib0280"><span class="elsevierStyleSup">26</span></a> The epidemiological importance of linezolid resistance&#44; in contrast to ciprofloxacin resistance&#44; lies in the fact that acquired linezolid resistance may be plasmid-encoded &#40;<span class="elsevierStyleItalic">cfr</span>&#44; <span class="elsevierStyleItalic">optrA</span> and <span class="elsevierStyleItalic">poxtA</span> determinants&#41;&#44; which could lead to the implementation of unnecessary control measures&#46;</p><p id="par0175" class="elsevierStylePara elsevierViewall">With respect to VR phenotype&#44; most of the discrepant antimicrobial MICs and errors occurred with the VanB phenotype&#44; which is consistent with the results of previous reports&#46;<a class="elsevierStyleCrossRefs" href="#bib0260"><span class="elsevierStyleSup">22&#44;27</span></a></p><p id="par0180" class="elsevierStylePara elsevierViewall">An analysis of the potential factors that contribute to erroneous antimicrobial susceptibility results should be a priority for clinical laboratories&#46; One way to address this problem is to participate in quality control programs&#44; which can be very helpful for detecting potential laboratory problems and enabling corrective measures aimed at optimizing the processing and quality of the reports offered to clinicians to be established&#46; This information is very useful for optimizing the best therapeutic strategies&#44; improving the rational use of antimicrobials &#40;reducing resistance rates&#41;&#44; facilitating the control of nosocomial infections &#40;by reducing the spread of MDR clones&#41;&#44; and preventing outbreaks&#46;<a class="elsevierStyleCrossRefs" href="#bib0290"><span class="elsevierStyleSup">28&#8211;30</span></a></p><p id="par0185" class="elsevierStylePara elsevierViewall">The main limitation of the present study is its small sample size&#44; which is typical of this kind of studies&#46;</p><p id="par0190" class="elsevierStylePara elsevierViewall">In conclusion&#44; this study shows that the discrepancies in MIC values and error rates in the clinical categorization of VRE observed with some antimicrobials were associated with the AST system used&#44; the application of EUCAST or CLSI breakpoints&#44; the antimicrobial agent&#44; and the interpretation of the VR phenotype&#46; Most microbiology laboratories in Spain can reliably determine the antimicrobial susceptibility in VRE&#44; although for teicoplanin there is a significant percentage of inadequate interpretations &#40;false susceptibility&#41;&#44; since VanB enterococci showing <span class="elsevierStyleItalic">in vitro</span> susceptibility to teicoplanin must be reported as resistant&#44; with a warning indicating that evidence of resistance development during treatment with this antimicrobial has been reported&#46;</p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0120">Funding</span><p id="par0195" class="elsevierStylePara elsevierViewall">This work was supported by the Instituto de Salud Carlos III&#44; Subdirecci&#243;n General de Redes y Centros de Investigaci&#243;n Cooperativa&#44; Ministerio de Econom&#237;a y Competitividad&#44; the Spanish Network for Research in Infectious Diseases &#40;REIPI RD 16&#47;0016&#41;&#8212;co-financed by European Development Regional Fund &#8216;A way to achieve Europe &#40;<span class="elsevierStyleGrantSponsor" id="gs1">ERDF</span>&#41;&#44; and the Reference Laboratory&#44; Program for the Prevention and Control of Healthcare-Associated Infections and Antimicrobial Stewardship in Andaluc&#237;a &#40;<span class="elsevierStyleGrantSponsor" id="gs2">PIRASOA</span>&#44; Junta de Andaluc&#237;a&#44; Consejer&#237;a de Salud Y Familias&#44; Servicio Andaluz de Salud&#41;&#46;</p></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0125">Conflict of interest</span><p id="par0200" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflict of interest&#46;</p></span></span>"
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        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Introduction</span><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">The ability of Spanish microbiology laboratories to &#40;a&#41; determine antimicrobial susceptibility &#40;AS&#41;&#44; and &#40;b&#41; correctly detect the vancomycin resistance &#40;VR&#41; phenotype in vancomycin-resistant <span class="elsevierStyleItalic">Enterococcus</span> spp&#46; &#40;VRE&#41; was evaluated&#46;</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Methods</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Three VRE isolates representing the VanA &#40;<span class="elsevierStyleItalic">E&#46; faecium</span>&#41;&#44; VanB &#40;<span class="elsevierStyleItalic">E&#46; faecium</span>&#41; and VanC &#40;<span class="elsevierStyleItalic">E&#46; gallinarum</span>&#41; VR phenotypes were sent to 52 laboratories&#44; which were asked for&#58; &#40;a&#41; AS method used&#59; &#40;b&#41; MICs of ampicillin&#44; imipenem&#44; vancomycin&#44; teicoplanin&#44; linezolid&#44; daptomycin&#44; ciprofloxacin&#44; levofloxacin and quinupristin&#8211;dalfopristin&#44; and high-level resistance to gentamicin and streptomycin&#59; &#40;c&#41; VR phenotype&#46;</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">&#40;a&#41; The most frequently used system was MicroScan&#59; &#40;b&#41; according to the system&#44; the highest percentage of discrepant MICs was found with gradient strips &#40;21&#46;3&#37;&#41;&#46; By antimicrobial&#44; the highest rates of discrepant MICs ranged 16&#46;7&#37; &#40;imipenem&#41; to 0&#46;7&#37; &#40;linezolid&#41;&#46; No discrepant MICs were obtained with daptomycin or levofloxacin&#46; Mayor errors &#40;MEs&#41; occurred with linezolid &#40;1&#46;1&#37;&#47;EUCAST&#41; and ciprofloxacin &#40;5&#46;0&#37;&#47;CLSI&#41;&#44; and very major errors &#40;VMEs&#41; with vancomycin &#40;27&#46;1&#37;&#47;EUCAST and 33&#46;3&#37;&#47;CLSI&#41; and teicoplanin &#40;5&#46;7&#37;&#47;EUCAST and 2&#46;3&#37;&#47;CLSI&#41;&#46; For linezolid&#44; ciprofloxacin&#44; and vancomycin&#44; discrepant MICs were responsible for these errors&#44; while for teicoplanin&#44; errors were due to a misassignment of the clinical category&#46; An unacceptable high percentage of VMEs was obtained using gradient strips &#40;14&#46;8&#37;&#41;&#44; especially with vancomycin&#44; teicoplanin and daptomycin&#59; &#40;c&#41; 86&#46;4&#37; of the centers identified VanA and VanB phenotypes correctly&#44; and 95&#46;0&#37; the VanC phenotype&#46;</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Conclusion</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Most Spanish microbiology laboratories can reliably determine AS in VRE&#44; but there is a significant percentage of inadequate interpretations &#40;warning of false susceptibility&#41; for teicoplanin in isolates with the VanB phenotype&#46;</p></span>"
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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">Se evalu&#243; la capacidad de los laboratorios de microbiolog&#237;a espa&#241;oles para&#58; &#40;a&#41; determinar la sensibilidad antimicrobiana &#40;SA&#41;&#59; y &#40;b&#41; detectar correctamente el fenotipo de resistencia a vancomicina &#40;FRV&#41; en <span class="elsevierStyleItalic">Enterococcus</span> spp&#46; resistente a vancomicina &#40;ERV&#41;&#46;</p></span> <span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">M&#233;todos</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Se enviaron 3 aislados de ERV &#40;<span class="elsevierStyleItalic">E&#46; faecium&#47;</span>VanA&#44; <span class="elsevierStyleItalic">E&#46; faecium</span>&#47;VanB y <span class="elsevierStyleItalic">E&#46; gallinarum</span>&#47;VanC&#41; a 52 laboratorios&#44; a los que se les solicit&#243;&#58; &#40;a&#41; m&#233;todo de SA&#59; &#40;b&#41; CMI de ampicilina&#44; imipenem&#44; vancomicina&#44; teicoplanina&#44; linezolid&#44; daptomicina&#44; ciprofloxacino&#44; levofloxacino y quinupristina-dalfopristina y resistencia de alto nivel a gentamicina y estreptomicina&#59; y &#40;c&#41; fenotipo de resistencia a vancomicina&#46;</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">&#40;a&#41; El sistema m&#225;s utilizado fue MicroScan&#59; y &#40;b&#41; el mayor porcentaje de CMI discrepantes se produjo con las tiras de gradiente &#40;21&#44;3&#37;&#41;&#46; Las tasas m&#225;s elevadas de CMI discrepantes variaron entre el 16&#44;7&#37; &#40;imipenem&#41; y el 0&#44;7&#37; &#40;linezolid&#41;&#46; Se produjeron errores mayores con linezolid &#40;1&#44;1&#37;&#47;EUCAST&#41; y ciprofloxacino &#40;5&#44;0&#37;&#47;CLSI&#41; y errores m&#225;ximos con vancomicina &#40;27&#44;1&#37;&#47;EUCAST y 33&#44;3&#37; CLSI&#41; y teicoplanina &#40;5&#44;7&#37;&#47;EUCAST y 2&#44;3&#37;&#47;CLSI&#41;&#46; Para linezolid&#44; ciprofloxacino y vancomicina las CMI discrepantes fueron las responsables de estos errores&#44; mientras que para teicoplanina los errores se debieron a una asignaci&#243;n err&#243;nea de la categor&#237;a cl&#237;nica&#46; Se obtuvo un alto porcentaje de errores m&#225;ximos utilizando tiras de gradiente &#40;14&#44;8&#37;&#41;&#44; especialmente con vancomicina&#44; teicoplanina y daptomicina&#59; y &#40;c&#41; el 86&#44;4&#37; de los centros identificaron correctamente los fenotipos VanA y VanB y el 95&#44;0&#37; el fenotipo VanC&#46;</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusi&#243;n</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">La mayor&#237;a de los laboratorios de microbiolog&#237;a espa&#241;oles determinan de forma fiable la SA en ERV&#44; pero existe un porcentaje significativo de interpretaciones inadecuadas &#40;falsa sensibilidad&#41; para teicoplanina en aislados con fenotipo VanB&#46;</p></span>"
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                  \t\t\t\t"><span class="elsevierStyleBold">4</span><a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">b</span></a>&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">Teicoplanin&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="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleBold">64</span>&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="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;25&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="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#8804;0&#46;06&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">Linezolid&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="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleBold">1</span>&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="char" 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="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;5&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">Daptomycin&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="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleBold">4</span>&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="char" 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="char" 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></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">Ciprofloxacin&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="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleBold">&#62;128</span>&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="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleBold">&#62;128</span>&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="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1&nbsp;\t\t\t\t\t\t\n
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                  \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">Levofloxacin&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="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleBold">&#62;128</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleBold">&#62;128</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1&nbsp;\t\t\t\t\t\t\n
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                  \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">HLR<a class="elsevierStyleCrossRef" href="#tblfn0035"><span class="elsevierStyleSup">a</span></a> Gentamicin&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleBold">&#62;128</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#60;128&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="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#60;128&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">HLR<a class="elsevierStyleCrossRef" href="#tblfn0035"><span class="elsevierStyleSup">a</span></a> Streptomycin&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#60;512&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="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleBold">&#62;512</span>&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="char" valign="\n
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                  \t\t\t\t">&#60;512&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">Quinupristin&#8211;Dalfopristin&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">NT&nbsp;\t\t\t\t\t\t\n
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                  """
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                  \t\t\t\t\tvoid\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col">AST system &#40;no&#46; of centers using the system&#47;total no&#46; of centers&#59; &#37;&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col">&#37; Discrepant MICs<a class="elsevierStyleCrossRef" href="#tblfn0010"><span class="elsevierStyleSup">a</span></a>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " colspan="6" align="center" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Clinical category errors &#40;&#37;&#41;<a class="elsevierStyleCrossRef" href="#tblfn0015"><span class="elsevierStyleSup">b</span></a></th></tr><tr title="table-row"><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t" scope="col">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col">&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  " colspan="2" align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Overall</th><th class="td" title="\n
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                  \t\t\t\t  " colspan="2" align="center" valign="\n
                  \t\t\t\t\ttop\n
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                  \t\t\t\t  " colspan="2" align="center" valign="\n
                  \t\t\t\t\ttop\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="" 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="" 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
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">EUCAST&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">CLSI&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">EUCAST&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">CLSI&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">EUCAST&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">CLSI&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Gradient strips &#40;19&#47;51&#59; 37&#46;3&#37;&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
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                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">12&#46;1&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;0&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;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="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleBold">14&#46;8</span>&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="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleBold">12&#46;1</span>&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">MicroScan &#40;32&#47;51&#59; 62&#46;7&#37;&#41;&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="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">4&#46;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="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">5&#46;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="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">4&#46;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="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;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="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;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="char" valign="\n
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                  \t\t\t\t"><span class="elsevierStyleBold">5&#46;6</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Broth microdilution &#40;2&#47;51&#59; 3&#46;9&#37;&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Vitek &#40;16&#47;51&#59; 31&#46;4&#37;&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">Phoenix &#40;1&#47;51&#59; 2&#46;0&#37;&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" scope="col">Antimicrobial<a class="elsevierStyleCrossRef" href="#tblfn0020"><span class="elsevierStyleSup">a</span></a> &#40;no&#46;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
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                  \t\t\t\t" scope="col">&#37; of discrepant MICs<a class="elsevierStyleCrossRef" href="#tblfn0025"><span class="elsevierStyleSup">b</span></a>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">No&#46; of MICs interpreted using breakpoints of<a class="elsevierStyleCrossRef" href="#tblfn0030"><span class="elsevierStyleSup">c</span></a></th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
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                  \t\t\t\t" scope="col">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" scope="col">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col">EUCAST&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">CLSI&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " colspan="2" align="center" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">EUCAST&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">CLSI&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">CLSI&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Ampicillin &#40;138&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t"><span class="elsevierStyleBold">13&#46;0</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">95&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">0&#46;0&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Teicoplanin &#40;152&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">45&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Vancomycin &#40;150&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Quinupristin&#8211;dalfopristin &#40;52&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Ciprofloxacin &#40;73&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">Linezolid &#40;135&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Daptomycin &#40;72&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Levofloxacin &#40;91&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">HLR to gentamicin &#40;69&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">HLR to streptomycin &#40;47&#41;&nbsp;\t\t\t\t\t\t\n
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                  """
              ]
              "imagenFichero" => array:1 [
                0 => "xTab3184626.png"
              ]
            ]
          ]
          "notaPie" => array:3 [
            0 => array:3 [
              "identificador" => "tblfn0020"
              "etiqueta" => "a"
              "nota" => "<p class="elsevierStyleNotepara" id="npar0025">The number of MIC determinations reported for each antimicrobial is in parentheses&#46; All the antimicrobials were not tested using the five AST methods&#46; HLR&#58; high-level resistance&#46;</p>"
            ]
            1 => array:3 [
              "identificador" => "tblfn0025"
              "etiqueta" => "b"
              "nota" => "<p class="elsevierStyleNotepara" id="npar0030">Percentages of discrepancies in the MICs&#46; MICs<span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>1 dilution from the reference values were considered discrepant&#46; MIC discrepancies<span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>10&#37; are highlighted in bold&#46;</p>"
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            2 => array:3 [
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