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Brief report
First survey on antibiotic resistance markers in Enterobacteriaceae in Cochabamba, Bolivia
Primer relevamiento de marcadores de resistencia a antibióticos en Enterobacteriaceae en Cochabamba, Bolivia
Paola M. Saba Villarroela, Gabriel O. Gutkinda, José A. Di Conzaa,b, Marcela A. Radicea,
Corresponding author
a Universidad de Buenos Aires, Facultad de Farmacia y Bioquímica, Ciudad Autónoma de Buenos Aires, CP 1113, Argentina
b Universidad Nacional del Litoral, Facultad de Bioquímica y Ciencias Biológicas, Santa Fe, CP 3000, Argentina
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CTX-M-enzymes are clustered in different groups&#44; CTX-M-1 group&#44; CTX-M-2 group&#44; CTX-M-8 group&#44; CTX-M-9 group and CTX-M-25 group&#59; many of these groups include different allelic variants&#46; CTX-M-15&#44; corresponding to the CTX-M-1 group and CTX-M-14&#44; belonging to the CTX-M-9 group&#44; are by far the most clinically relevant ESBL worlwide<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">3</span></a>&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall">Spontaneous chromosomal mutations in <span class="elsevierStyleItalic">gyrA</span> and <span class="elsevierStyleItalic">parC</span>&#44; within the quinolone resistance-determining region &#40;QRDR&#41;&#44; constitute the main mechanism conferring high level quinolone resistance&#46; Plasmid-mediated quinolone resistance &#40;PMQR&#41; determinants&#44; such as Qnr proteins &#40;A&#44; B&#44; C&#44; D and S&#41;&#44; Aac&#40;6&#8242;&#41;-Ib-cr enzyme&#44; QepA and OqxAB efflux pumps are increasingly reported<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">12</span></a>&#46; Even though these markers only provide low level quinolone resistance by themselves&#44; it has been shown that they facilitate the selection of chromosomal mutations in QRDR&#44; <span class="elsevierStyleItalic">in vitro</span><a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">12</span></a>&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">No surveillance studies on resistance markers in clinical isolates have been previously conducted in Cochabamba&#44; Bolivia&#46; The aim of this study was to characterize &#946;-lactam and quinolone resistance mechanisms in TGC resistant <span class="elsevierStyleItalic">Enterobacteriaceae</span>&#46; Therefore&#44; a prospective&#44; observational&#44; descriptive and transversal study was carried out&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">All cefotaxime and&#47;or ceftazidime-resistant <span class="elsevierStyleItalic">Enterobacteriaceae</span> recovered from 5 health centers in Cochabamba&#44; Bolivia&#44; from December 2012 to March 2013 were included&#46; Identification was performed by conventional biochemical tests&#46; Antimicrobial susceptibility profiles were determined by disk diffusion and agar dilution methods in accordance with CLSI&#44; 2014&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">Total DNA was obtained by boiling bacterial suspensions&#44; and plasmid DNA was extracted by alkaline lysis&#46; Screening of ESBL coding genes&#44; <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">SHV</span>&#44; <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-1</span> group&#44; <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-2</span> group&#44; <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-8</span> group&#44; <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-9</span> group&#44; <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-25</span> group&#44; <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">OXA-1</span>&#44; <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">OXA-2</span>&#44; <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">OXA-10</span>&#44; <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">OXA-48</span>&#44; <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">PER-2</span>&#44; <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">KPC</span> and <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">GES</span>&#44; was performed by simple PCR amplifications&#46; Primers used and the expected amplicon sizes are shown in a supplementary table &#40;Table S1&#41;&#46; Plasmid encoded <span class="elsevierStyleItalic">ampC</span> genes<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">8</span></a> and <span class="elsevierStyleItalic">Escherichia coli</span> phylogenetic groups<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">4</span></a> were determined by multiplex PCR as previously reported&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">PMQR genes &#40;<span class="elsevierStyleItalic">qepA&#44; oqxAB&#44; aac&#40;6&#8217;&#41;-Ib-cr&#44; qnr</span> &#40;A&#44; B&#44; C&#44; D&#44; S&#41;&#41; were investigated by PCR amplification using specific primers<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">9</span></a>&#46; Amplicons identity was assessed by digestion and&#47;or sequencing&#46; Nucleotide sequences were compared with NCBI-BLAST databases&#46; Statistical analysis was performed using the Fisher&#39;s exact test &#40;SPSS version 22&#41;&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">Clonal relatedness was analyzed by REP&#47;ERIC-PCR and dendrograms were constructed using the Treecon 1&#46;3b program&#46; Isolates displaying more than 90&#37; identity were considered to be clonally related&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">A total of 101 TGC-resistant enterobacteria&#44; corresponding to <span class="elsevierStyleItalic">E&#46; coli</span> &#40;87&#41;&#44; <span class="elsevierStyleItalic">K&#46; pneumoniae</span> &#40;11&#41;&#44; <span class="elsevierStyleItalic">C&#46; freundii</span> &#40;1&#41;&#44; <span class="elsevierStyleItalic">M&#46; morganii</span> &#40;1&#41; and <span class="elsevierStyleItalic">E&#46; cloacae</span> &#40;1&#41;&#44; were recovered&#46; A high proportion of the samples &#40;71&#46;3&#37;&#41; were recovered from women aged between 50 to 80 years old&#46; Eighty five enterobacteria &#40;84&#46;0&#37;&#41; were isolated from urine&#44; 7 from wound secretions&#44; 4 from blood&#44; 4 from tracheal secretions and the remaining from ear secretions&#46; A similar distribution was observed between outpatients and inpatients &#40;49&#46;0&#37; and 51&#46;0&#37;&#44; respectively&#41;&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">High resistance rates to nalidixic acid&#44; ciprofloxacin&#44; levofloxacin and gentamicin were observed&#46; Eighty five percent of the isolates were not susceptible to ceftazidime and 90&#37; to cefepime&#46; Resistance to cefoxitin&#44; kanamycin and amikacin was less frequent &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0055" class="elsevierStylePara elsevierViewall">MIC<span class="elsevierStyleInf">50</span> and MIC<span class="elsevierStyleInf">90</span> values were as follows&#58; cefotaxime 128<span class="elsevierStyleHsp" style=""></span>&#956;g&#47;ml and &#62;128<span class="elsevierStyleHsp" style=""></span>&#956;g&#47;ml&#44; ceftazidime 16<span class="elsevierStyleHsp" style=""></span>&#956;g&#47;ml and 128<span class="elsevierStyleHsp" style=""></span>&#956;g&#47;ml&#44; cefepime 8<span class="elsevierStyleHsp" style=""></span>&#956;g&#47;ml and 32<span class="elsevierStyleHsp" style=""></span>&#956;g&#47;ml&#44; nalidixic acid &#62;64<span class="elsevierStyleHsp" style=""></span>&#956;g&#47;ml and ciprofloxacin &#62;32<span class="elsevierStyleHsp" style=""></span>&#956;g&#47;ml&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">All isolates were CTX-M producers&#44; 89&#47;101 &#40;88&#46;1&#37;&#41; harbored <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-1</span> group markers corresponding to&#58; <span class="elsevierStyleItalic">E&#46; coli</span> &#40;78&#41;&#44; <span class="elsevierStyleItalic">K&#46; pneumoniae</span> &#40;9&#41;&#44; <span class="elsevierStyleItalic">E&#46; cloacae</span> &#40;1&#41; and <span class="elsevierStyleItalic">M&#46; morganii</span> &#40;1&#41;&#46; Ten isolates carried <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-9</span> group markers belonging to&#58; <span class="elsevierStyleItalic">E&#46; coli</span> &#40;9&#41; and <span class="elsevierStyleItalic">K&#46; pneumoniae</span> &#40;1&#41;&#46; The only <span class="elsevierStyleItalic">C&#46; freundii</span> displayed a <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-2</span> group gene&#44; showing a very low prevalence of this marker&#46; Finally&#44; one <span class="elsevierStyleItalic">K&#46; pneumoniae</span> isolate was positive for both <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-1</span> and <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-9</span> group markers&#46; In good agreement with the South American scene&#44; a radical change of the CTX-M-2 group to CTX-M-1 and CTX-M-9 groups was noted<a class="elsevierStyleCrossRefs" href="#bib0095"><span class="elsevierStyleSup">3&#44;13&#44;16</span></a>&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">Ten randomly selected PCR products were sequenced&#44; those positive for the <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-1</span> group were identified as <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-15</span>&#44; while those positive for the <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-9</span> group corresponded to <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-14&#46;</span> Neither the <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-8</span> group nor the <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-25</span> group were detected&#46; In accordance with CLSI breakpoints&#44; from 89 <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-1</span> group-harboring isolates&#44; 62 &#40;69&#46;7&#37;&#41; were resistant to ceftazidime&#44; 24 &#40;27&#46;0&#37;&#41; were categorized as intermediate and only 3 &#40;3&#46;3&#37;&#41; were categorized as susceptible&#46; Among the <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-9</span> group positive isolates&#44; 8&#47;10 were categorized as susceptible to ceftazidime&#44; 1 was categorized as intermediate and the remaining as resistant&#46; <span class="elsevierStyleItalic">C&#46; freundii</span> harboring the <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-2</span> group was categorized as intermediate to this agent&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">A <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">OXA-1</span>like marker was detected in 70&#47;101 &#40;69&#46;3&#37;&#41; ESBL-producing isolates&#44; mainly in those carrying <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-1</span> group markers &#40;68&#47;89&#44; 76&#46;4&#37;&#41;&#46; Sequenced amplicons corresponded 100&#37; to <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">OXA-1&#46;</span> None of the <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-9</span> group positive isolates rendered positive amplification for <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">OXA-1&#46;</span> The association of <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-1</span> group markers with <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">OXA-1</span> was confirmed in this study &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;001&#41;&#46; Neither the presence of plasmidic AmpC coding genes nor <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">OXA-2</span>&#44; <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">OXA-10</span>&#44; <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">OXA-48</span>&#44; <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">PER-2</span>&#44; <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">KPC</span> and <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">GES</span> were detected&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">Fifty eight from 87 <span class="elsevierStyleItalic">E&#46; coli</span> isolates &#40;67&#46;0&#37;&#41; belonged to phylogenetic group B2&#44; 17&#46;0&#37; to group A and 16&#46;0&#37; to group D&#46; The CTX-M-1 group producers were mostly associated with the phylogenetic group B2 &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;01&#41;&#44; followed by A and D&#46; CTX-M-9 group producers were mainly associated with phylogenetic group D&#44; followed by A and B2&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall"><a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a> describes the different PMQR detected in this study&#46; The <span class="elsevierStyleItalic">aac&#40;6&#8242;&#41;-Ib-cr</span> gene was present in 83&#46;0&#37; of the isolates&#44; being the most prevalent PMQR determinant among the studied enterobacteria&#46; Other less common markers were also identified&#46; The CTX-M-9 group producers did not harbor any of the analyzed PMQR&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0085" class="elsevierStylePara elsevierViewall">Among Qnr proteins&#44; only <span class="elsevierStyleItalic">qnrB</span> determinants were detected&#44; corresponding to <span class="elsevierStyleItalic">qnrB1</span> &#40;5&#41; and <span class="elsevierStyleItalic">qnrB19</span> &#40;1&#41;&#46; Plasmid-mediated efflux pumps were identified in 7 <span class="elsevierStyleItalic">E&#46; coli</span> isolates corresponding to phylogenetic group B2&#46; A single isolate carried <span class="elsevierStyleItalic">oqxAB</span> while the other 6 harbored <span class="elsevierStyleItalic">qepA1&#46;</span> The latter isolates also harbored <span class="elsevierStyleItalic">aac&#40;6&#8242;&#41;-Ib-cr</span> and <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-15</span>&#44; however they clustered in three different groups in accordance with REP-PCR profiles &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46; Each cluster contains isolates collected from different health centers&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0090" class="elsevierStylePara elsevierViewall">All enterobacteria included in this study were ESBL producers&#44; corresponding to different CTX-M groups&#46; In this work&#44; CTX-M-1 group enzymes were prevalent in good agreement with different studies conducted by Bartoloni et al&#46; in the Bolivian Chaco &#40;in healthy children and urinary tract infection samples&#41;&#44; and also with other recent studies carried in other South American countries<a class="elsevierStyleCrossRefs" href="#bib0090"><span class="elsevierStyleSup">2&#44;3&#44;13&#44;16</span></a>&#46;</p><p id="par0095" class="elsevierStylePara elsevierViewall">Although all isolates were cefotaximase producers&#44; 10&#46;9&#37; and 9&#46;9&#37; were categorized as susceptible to ceftazidime in accordance with the current breakpoints of the CLSI and EUCAST&#44; respectively&#46; Ceftazidime susceptible isolates were strongly associated with the production of CTX-M-9 group ESBLs &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;001&#41;&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">Most CTX-M-15-producing <span class="elsevierStyleItalic">E&#46; coli</span> belong to phylogenetic group B2&#46; These strains display a high virulence potential and have been mainly associated with ST 131 constituting a major public health problem worldwide<a class="elsevierStyleCrossRefs" href="#bib0090"><span class="elsevierStyleSup">2&#44;4&#44;13&#44;16</span></a>&#46; Accordingly&#44; in this study&#44; CTX-M-1 group enzymes were strongly associated with phylogroup B2 &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;001&#41;&#46; However&#44; in Venezuela it was reported that phylogenetic group A was prevalent among CTX-M-15-producing uropathogenic <span class="elsevierStyleItalic">E&#46; coli</span> isolates<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">6</span></a>&#46;</p><p id="par0105" class="elsevierStylePara elsevierViewall">Different PMQR markers were identified&#44; with <span class="elsevierStyleItalic">aac&#40;6&#8242;&#41;-Ib-cr</span> by large as the most predominant&#46; This variant has been reported in previous studies performed in different Latin American countries such as Argentina&#44; Brazil&#44; Chile&#44; Mexico&#44; Peru and Uruguay<a class="elsevierStyleCrossRefs" href="#bib0105"><span class="elsevierStyleSup">5&#44;9&#44;14&#44;16</span></a>&#46; A higher <span class="elsevierStyleItalic">aac&#40;6&#8242;&#41;-Ib-cr</span> rate was observed in this study with respect to previous reports in Bolivia&#59; nevertheless comparisons between these studies should be performed carefully due to the different bacterial selection criteria used<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">2</span></a>&#46;</p><p id="par0110" class="elsevierStylePara elsevierViewall">Among the <span class="elsevierStyleItalic">qnrB</span> genes detected&#44; <span class="elsevierStyleItalic">qnrB1</span> was dominant&#44; in agreement with studies conducted in Mexico and Brazil<a class="elsevierStyleCrossRefs" href="#bib0150"><span class="elsevierStyleSup">14&#44;15</span></a>&#46; Moreover&#44; in previous studies conducted in Bolivia and Argentina <span class="elsevierStyleItalic">qnrB19</span>&#44; <span class="elsevierStyleItalic">qnrB10</span> and <span class="elsevierStyleItalic">qnrB2</span> genes<a class="elsevierStyleCrossRefs" href="#bib0115"><span class="elsevierStyleSup">7&#44;9</span></a> were reported&#46; To the best of our knowledge&#44; this constitutes the first report of <span class="elsevierStyleItalic">qnrB1</span> in Bolivia&#44; and even the description of its association with <span class="elsevierStyleItalic">aac&#40;6&#8242;&#41;-Ib-cr</span> and <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">CTX-M-1</span> group resistance determinants in <span class="elsevierStyleItalic">E&#46; coli</span> isolated from clinical samples&#46;</p><p id="par0115" class="elsevierStylePara elsevierViewall">There are few reports of plasmid-mediated fluoroquinolone efflux pumps in Latin America&#46; In good agreement with studies performed in Bolivia and Mexico&#44; <span class="elsevierStyleItalic">qepA1</span> was detected in CTX-M-15-producing <span class="elsevierStyleItalic">E&#46; coli</span> isolates<a class="elsevierStyleCrossRefs" href="#bib0090"><span class="elsevierStyleSup">2&#44;14</span></a>&#46; The <span class="elsevierStyleItalic">qepA</span> gene was also described in CTX-M-14 producing <span class="elsevierStyleItalic">E&#46; coli</span> clinical isolates in Peru&#44; and in CTX-M-2 producing <span class="elsevierStyleItalic">E&#46; coli</span> in Colombia &#40;Rinc&#243;n Cruz G&#46;&#44; PhD&#46; Thesis&#44; 2015&#41;&#59; however&#44; in Argentina <span class="elsevierStyleItalic">qepA</span>1 was found in non-ESBL producing <span class="elsevierStyleItalic">E&#46; coli</span><a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">10</span></a>&#46;</p><p id="par0120" class="elsevierStylePara elsevierViewall">Finally&#44; regarding efflux pump OqxAB&#44; which is uncommon in enterobacteria other than <span class="elsevierStyleItalic">K&#46; pneumoniae</span>&#44; 1 isolate of <span class="elsevierStyleItalic">E&#46; coli</span> carrying <span class="elsevierStyleItalic">oqxAB</span> was identified&#44; being the first report in Bolivia and one of the first descriptions in Latin America&#46; Recently 3<span class="elsevierStyleItalic">oqxAB-</span> positive <span class="elsevierStyleItalic">E&#46; coli</span> were detected in Peru and 1 in Argentina<a class="elsevierStyleCrossRefs" href="#bib0085"><span class="elsevierStyleSup">1&#44;11</span></a>&#46;</p><p id="par0125" class="elsevierStylePara elsevierViewall">This study constitutes the first molecular survey on &#946;-lactam and quinolone resistance markers in clinical isolates of <span class="elsevierStyleItalic">Enterobactericeae</span>&#44; in Cochabamba&#44; Bolivia&#46; These results contribute to the regional knowledge of the epidemiological situation regarding the resistance to frequently used antibiotics&#46; The molecular epidemiology of CTX-M-enzymes and its association with PMQR&#44; mainly <span class="elsevierStyleItalic">aac&#40;6&#8242;&#41;-Ib-cr</span>&#59; observed herein resembles the scene reported recently in South America&#46;</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Ethical responsibilities</span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Protection of human and animal subjects</span><p id="par0130" class="elsevierStylePara elsevierViewall">The authors declare that no experiments were performed on humans or animals for this study&#46;</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Confidentiality of data</span><p id="par0135" class="elsevierStylePara elsevierViewall">The authors declare that no patient data appear in this article&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Right to privacy and informed consent</span><p id="par0140" class="elsevierStylePara elsevierViewall">The authors declare that no patient data appear in this article&#46;</p></span></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Conflict of interest</span><p id="par0145" class="elsevierStylePara elsevierViewall">The authors claim that they have no conflicts of interest to declare&#46;</p></span></span>"
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        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">A molecular survey was conducted in Cochabamba&#44; Bolivia&#44; to characterize the mechanism involved in the resistance to clinically relevant antibiotics&#46; Extended Spectrum &#946;-lactamase encoding genes and plasmid-mediated quinolone resistance &#40;PMQR&#41; markers were investigated in a total of 101 oxyimino-cephalosporin-resistant enterobacteria recovered from different health centers during four months &#40;2012&#8211;2013&#41;&#46; CTX-M enzymes were detected in all isolates&#44; being the CTX-M-1 group the most prevalent &#40;88&#46;1&#37;&#41;&#46; The presence of <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">OXA-1</span> was detected in 76&#46;4&#37; of these isolates&#46; A high quinolone resistance rate was observed among the included isolates&#46; The <span class="elsevierStyleItalic">aac&#40;6&#8242;&#41;-Ib-cr</span> gene was the most frequent PMQR identified &#40;83&#46;0&#37;&#41;&#46; Furthermore&#44; 6 isolates harbored the <span class="elsevierStyleItalic">qnrB</span> gene&#46; Interestingly&#44; <span class="elsevierStyleItalic">qepA1</span> &#40;6&#41; and <span class="elsevierStyleItalic">oqxAB</span> &#40;1&#41;&#44; were detected in 7 <span class="elsevierStyleItalic">Escherichia coli</span>&#44; being the latter the first to be reported in Bolivia&#46; This study constitutes the first molecular survey on resistance markers in clinical enterobacterial isolates in Cochabamba&#44; Bolivia&#44; contributing to the regional knowledge of the epidemiological situation&#46; The molecular epidemiology observed herein resembles the scene reported in South America&#46;</p></span>"
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        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Se llev&#243; a cabo un relevamiento molecular de la resistencia a antibi&#243;ticos de importancia cl&#237;nica en aislamientos recuperados en Cochabamba&#44; Bolivia&#46; Se estudiaron los genes codificantes de &#946;-lactamasas de espectro extendido y de resistencia a quinolonas de localizaci&#243;n plasm&#237;dica &#40;PMQR&#41; en un total de 101 aislamientos de enterobacterias resistentes a oximinocefalosporinas recuperados en distintos centros de salud&#44; durante 4 meses &#40;2012-2013&#41;&#46; En todos ellos se detect&#243; la presencia de cefotaximasas&#44; las CTX-M grupo 1 fueron las m&#225;s prevalentes &#40;88&#44;1&#37;&#41;&#46; La presencia de <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf"><span class="elsevierStyleItalic">OXA-1</span></span> se detect&#243; en el 76&#44;4&#37; de estos aislamientos&#46; Se observ&#243; una elevada proporci&#243;n de aislamientos resistentes a quinolonas&#46; El gen <span class="elsevierStyleItalic">aac&#40;6&#8242;&#41;-Ib-cr</span> fue el determinante PMQR m&#225;s frecuentemente identificado &#40;83&#37;&#41;&#46; Adem&#225;s&#44; 6 aislamientos resultaron ser portadores de <span class="elsevierStyleItalic">qnrB</span>&#46; Por otro lado&#44; cabe remarcar que 7 <span class="elsevierStyleItalic">Escherichia coli</span> presentaron <span class="elsevierStyleItalic">qepA1</span> &#40;6&#41; y <span class="elsevierStyleItalic">oqxAB</span> &#40;1&#41;&#59; se documenta as&#237; por primera vez la presencia de <span class="elsevierStyleItalic">oqxAB</span> en Bolivia&#46; Este estudio constituye el primer relevamiento de marcadores de resistencia en aislamientos cl&#237;nicos de enterobacterias en Cochabamba&#44; Bolivia&#59; de este modo se contribuye al conocimiento regional de la situaci&#243;n epidemiol&#243;gica&#44; la cual presenta un escenario similar al observado en el resto de Latinoam&#233;rica&#46;</p></span>"
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8211;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">M&#46; morganii &#40;1&#41;</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">&#8211;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">C&#46; freundii &#40;1&#41;</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleItalic">aac&#40;6</span>&#8242;&#41;<span class="elsevierStyleItalic">-Ib-cr</span><span class="elsevierStyleHsp" style=""></span>&#43;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">qepA1</span> &#40;6&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">CTX-M-1 group&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">B2 &#40;6&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">CTX-M-1 group&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">B2 &#40;2&#41;&#44; A &#40;1&#41;&#44; D &#40;1&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">CTX-M-1 group&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="table-entry  " align="left" valign="top">-&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
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        "titulo" => "Acknowledgements"
        "texto" => "<p id="par0155" class="elsevierStylePara elsevierViewall">This work was partly supported by UBACyT to GG and MR&#59; by CAI&#43;D-UNL to JDC&#59; by PIP-CONICET to GG&#44; MR y JDC and PICT-ANPCyT to GG and MR&#46; GG&#44; MR and JDC are members of CONICET&#46;</p> <p id="par0160" class="elsevierStylePara elsevierViewall">We would like to thank Mirtha Villarroel Garc&#237;a&#44; Virginia Aguilar&#44; Tatiana Pimentel&#44; Leovegildo &#193;lvarez&#44; Norah Balderrama for their help in collecting the samples and Giovanna Rinc&#243;n for her technical assistance and collaboration&#46;</p>"
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ISSN: 03257541
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