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Brief report
Report of two events of nosocomial outbreak and pseudo-outbreak due to contamination with Achromobacter spp.
Comunicación de 2 eventos de brote y seudobrote nosocomial debido a contaminación con Achromobacter spp
Liliana Claraa,b, María Ines Stanelonia,b, Estela Salazara, Graciela Grecoc, Mariangeles Visusc, Alicia Lizzib, Valeria Alexanderc, Gabriel Gutkindd,e, Marcela Radiced,e,
Corresponding author
mradice@ffyb.uba.ar

Corresponding author.
, Mariana Papaliad,e
a Hospital Italiano de Buenos Aires, Sección Infectología, Servicio de Clínica Médica, Pres. Tte. Gral. Juan Domingo Perón 4190, Ciudad Autónoma de Buenos Aires, C1199, Argentina
b Hospital Italiano de Buenos Aires, Comité de Control de Infecciones, Pres. Tte. Gral. Juan Domingo Perón 4190, Ciudad Autónoma de Buenos Aires, C1199, Argentina
c Hospital Italiano de Buenos Aires, Sección Bacteriología Laboratorio Central, Pres. Tte. Gral. Juan Domingo Perón 4190, Ciudad Autónoma de Buenos Aires, C1199, Argentina
d Universidad de Buenos Aires, Facultad de Farmacia y Bioquímica, IBaViM, Laboratorio de Resistencia Bacteriana, Junín 956, 8vo. Piso, Ciudad Autónoma de Buenos Aires, CP 1113, Argentina
e Consejo Nacional de Investigaciones Científicas y Técnicas de Argentina (CONICET), Ciudad Autónoma de Buenos Aires, Argentina
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for that reason clinical isolates are mostly referred to as <span class="elsevierStyleItalic">A&#46; xylosoxidans</span>&#46; Accurate identification at species level can only be achieved using genotypic methods although these techniques are not used for routine identification<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">12</span></a>&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Achromobacter</span> spp&#46; have been usually associated with aquatic environments&#44; and frequently colonize aqueous solutions in the hospital settings from where they may infect compromised patients<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">1</span></a>&#46; <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; are increasingly recognized as important emerging nosocomial pathogens&#44; mainly in immunocompromised hosts&#44; as well as in patients with cystic fibrosis<a class="elsevierStyleCrossRefs" href="#bib0085"><span class="elsevierStyleSup">1&#44;13</span></a>&#46; Although increasingly reported&#44; it is difficult to interpret their clinical significance&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">Effective treatment of <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; infections can be challenging due to their natural and acquired multidrug resistance patterns<a class="elsevierStyleCrossRefs" href="#bib0110"><span class="elsevierStyleSup">6&#44;7</span></a>&#46; Moreover&#44; antiseptics and disinfectants are not always able to eliminate the source of <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; in the hospital environments<a class="elsevierStyleCrossRefs" href="#bib0095"><span class="elsevierStyleSup">3&#44;10</span></a>&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">Several outbreaks and pseudo-outbreaks caused by <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; have been reported&#44; and many of them have contaminated fluids such as chlorhexidine as the epidemiological &#8220;common denominator&#8221;<a class="elsevierStyleCrossRefs" href="#bib0090"><span class="elsevierStyleSup">2&#44;3&#44;10</span></a>&#46; Both outbreaks and pseudo-outbreaks are negative as hospital quality indicators&#44; as well as the inappropriate use of antibiotics&#46; Institutional multidisciplinary management is required to prevent infections&#44; outbreaks and pseudo-outbreaks&#44; and the consequent inappropriate use of antibiotics&#44; since antimicrobial stewardship constitutes another indicator of nosocomial quality&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">Starting 2013 an increased presence of <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; in blood cultures and clinical samples was observed in a tertiary hospital in Buenos Aires city&#44; leading to this epidemiological study&#46;</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Event report 1</span><p id="par0055" class="elsevierStylePara elsevierViewall">A descriptive study of <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; positive blood samples&#44; recovered between 2013 and 2016&#44; was carried out retrospectively&#44; in order to characterize a possible outbreak and identify probable sources of contamination&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">The incidence of <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; contaminated blood cultures&#44; with respect to the total blood samples&#44; was 51&#47;36<span class="elsevierStyleHsp" style=""></span>286 &#40;0&#46;14&#37;&#41; in 2013&#44; 91&#47;40<span class="elsevierStyleHsp" style=""></span>285 &#40;0&#46;22&#37;&#41; in 2014 and 79&#47;43<span class="elsevierStyleHsp" style=""></span>450 &#40;0&#46;18&#37;&#41; in 2015&#46; True bloodstream infections were confirmed by clinical evaluation and a second positive blood culture<a class="elsevierStyleCrossRefs" href="#bib0105"><span class="elsevierStyleSup">5&#44;16</span></a>&#46; Many of these contaminated samples came from emergency wards &#40;61&#46;5&#37;&#41;&#44; and in some cases&#44; other unusual non-fermenting gram negative bacilli were also present&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">From June to October 2015&#44; the probable sources of contamination were investigated&#44; including heparin tubes&#44; povidone-iodine solutions&#44; and EDTA and sodium citrate lab tubes&#46; Out of a total of 48 analyzed samples&#44; 4 sodium citrate tubes were positive for <span class="elsevierStyleItalic">Achromobacter</span> spp&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">Species identification of the isolates recovered from blood samples &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>6&#41; and blood collection test tubes &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>4&#41; was achieved using genotypic approaches&#46; The <span class="elsevierStyleItalic">nrdA</span> sequences were determined according to Spilker et al&#46;&#44; and compared with databases &#40;<a href="https://pubmlst.org/achromobacter/"><span class="elsevierStyleUnderline">https&#58;&#47;&#47;pubmlst&#46;org&#47;achromobacter&#47;</span></a>&#41;<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">12</span></a>&#46; The presence of species-specific markers&#44; <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">OXA-114</span>&#44; <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">OXA-258</span>&#44; <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">OXA-364</span> and <span class="elsevierStyleItalic">bla</span><span class="elsevierStyleInf">OXA-243</span>&#44; intrinsic for <span class="elsevierStyleItalic">A&#46; xylosoxidans</span>&#44; <span class="elsevierStyleItalic">Achromobacter ruhlandii</span>&#44; <span class="elsevierStyleItalic">Achromobacter dolens</span>&#44; and <span class="elsevierStyleItalic">Achromobacter insuavis</span>&#44; respectively&#44; were investigated according to Traglia et al&#46; and Papalia et al&#46;<a class="elsevierStyleCrossRefs" href="#bib0135"><span class="elsevierStyleSup">11&#44;14</span></a>&#46; All these bacterial isolates were identified as <span class="elsevierStyleItalic">A&#46; insuavis&#46;</span></p><p id="par0075" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Xba</span>I-pulsed-field gel electrophoresis &#40;PFGE&#41; was performed to compare the isolates recovered from sodium citrate tubes among them&#44; and with those recovered from blood cultures<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">9</span></a>&#46; A single pulsotype indicative of the presence of the same strain in all samples was observed &#40;<a class="elsevierStyleCrossRef" href="#sec0035">Suppl&#46; Fig&#46; S1</a>&#41;&#46; Based on these results&#44; it was assumed that these pseudo-bacteremias were originated by the use of contaminated sodium citrate tubes and the subsequent incorrect technique of loading the blood culture bottles&#44; <span class="elsevierStyleItalic">i&#46;e&#46;</span>&#44; first inoculating the blood collection test tubes that were contaminated with <span class="elsevierStyleItalic">A&#46; insuavis</span> followed by the inoculation of the blood culture bottles with the same needle generating false positive blood cultures&#46; In order to avoid these pseudo-outbreaks&#44; personnel retraining regarding the correct sample loading technique was conducted and institutional guidelines were designed <span class="elsevierStyleItalic">ad hoc&#46;</span></p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Event report 2</span><p id="par0080" class="elsevierStylePara elsevierViewall">A strikingly high number of <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; isolates in clinical specimens other than blood samples was also detected in our hospital&#44; which led to an epidemiological study to characterize a possible outbreak and to identify a common denominator&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">A total of 94 <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; positive samples&#44; recovered from 59 patients from March 2014 to June 2016&#44; were included in this study &#40;<a class="elsevierStyleCrossRef" href="#sec0035">Suppl&#46; Fig&#46; 2</a>&#41;&#46;</p><p id="par0090" class="elsevierStylePara elsevierViewall">Each of these episodes was classified as <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; infection or colonization after reviewing the patients&#8217; clinical histories&#46; Patients with a positive culture and symptoms compatible with infection without any other apparent focus and with specific antibiotic treatment selected for these microorganisms were categorized as infected by <span class="elsevierStyleItalic">Achromobacter</span> spp&#46;&#44; while patients with a positive culture for <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; without any clinical symptoms compatible with infection were categorized as colonized &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; Twenty eight percent &#40;28&#37;&#41; of the analyzed cases were interpreted as infections and the remaining 72&#37; as <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; colonization&#46; Mortality rate after 30 days was 1&#37;&#44; although it was unrelated to the presence of <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; in cultures&#46; Ninety five percent &#40;95&#37;&#41; of these cultures were recovered from patients that either were hospitalized for 48<span class="elsevierStyleHsp" style=""></span>h&#44; or with previous hospitalization &#40;less than 90 days&#41;&#44; or that underwent surgery&#44; thus categorized as hospital-acquired infections&#47;colonizations&#46; Clinical specimens are shown in <a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0095" class="elsevierStylePara elsevierViewall">Among <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; positive samples&#44; a broad dominance was observed in those recovered from trauma surgeries and surgeries with anfractuous open wounds&#44; performed at the orthopedic operating room &#40;64&#47;94&#41;&#46; Twenty nine percent &#40;29&#37;&#41; of the patients were assisted in clinical areas and 59&#37; in critical care areas&#59; in 23&#37; previous washing with soapy chlorhexidine was recorded&#46; Likewise&#44; <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; were also recovered from other clinical samples&#44; and other areas of the institution&#44; suggesting a common source of extensive use throughout the hospital&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">In April 2016&#44; environmental&#44; instrumental&#44; antiseptic and disinfectant samples from 5 different operating rooms were analyzed&#46; <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; was identified in 15&#47;17 samples of 4&#37; soapy chlorhexidine&#44; recovered from all operating rooms&#44; as well as in unopened containers stored in this center since 2014&#44; indicating intrinsic contamination&#46; Soapy chlorhexidine samples were removed from the spray bottle with pipettes to avoid touching the container&#46; The soapy chlorhexidine samples were cultured in a PF Bact-Alert&#174; flask &#40;bioM&#233;rieux&#41;&#46; Incubation was carried out for 5 days to rule out the possibility of a negative result&#46; Prior to inoculation&#44; a two-fold dilution of the sample was performed using sterile human plasma&#46; The final inoculation volume was 5<span class="elsevierStyleHsp" style=""></span>ml &#40;2&#46;5<span class="elsevierStyleHsp" style=""></span>ml of antiseptic solution and 2&#46;5<span class="elsevierStyleHsp" style=""></span>ml of human plasma&#41;&#46;</p><p id="par0105" class="elsevierStylePara elsevierViewall">Twenty-five &#40;25&#41; isolates recovered from clinical specimens and from the chlorhexidine soap solution were identified by <span class="elsevierStyleItalic">nrd</span>A sequencing<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">12</span></a>&#44; corresponding to <span class="elsevierStyleItalic">A&#46; xylosoxidans</span> &#40;n&#58; 1&#41; and <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; &#40;n&#58; 24&#41;&#46; A multilocus sequence-typing &#40;MLST&#41; scheme was conducted to identify those isolates which could not be unambiguously identified by <span class="elsevierStyleItalic">nrd</span>A sequencing&#46; For this purpose&#44; amplification and sequencing of inner fragments of seven housekeeping genes were conducted&#46; Concatenate sequences &#40;2254 nucleotides&#41; of these seven fragments were obtained for those isolates included in this study and for 362 <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; available in the database &#40;<a class="elsevierStyleCrossRef" href="#sec0035">Suppl&#46; Table 1</a>&#41;&#46; An alignment of all concatenates was performed using the program ClustalX 2&#46;1&#46; The statistical selection of best-fit model of nucleotide substitution was assessed by JModelTest&#46; Maximum Likelihood estimation was conducted using MEGA 5&#46;05&#46; Bootstraps with 1000 re-sample matrices were executed to assess the statistical support for the identified groups&#46; The dendrogram obtained with Maximum Likelihood is depicted in <a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a>&#44; showing that these isolates grouped with <span class="elsevierStyleItalic">Achromobacter</span> genogroup 20&#46; However&#44; they could correspond to a new species of the genus <span class="elsevierStyleItalic">Achromobacter</span> &#40;a long-term analysis out of the scope for the present study&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0110" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Xba</span>I-pulsed-field gel electrophoresis &#40;PFGE&#41; was performed to compare the <span class="elsevierStyleItalic">Achromobacter</span> genogroup 20 isolates&#44; recovered both from clinical specimens and from the chlorhexidine soap solution&#59; PFGE analysis showed 4 different pulsotypes &#40;<a class="elsevierStyleCrossRef" href="#sec0035">Suppl&#46; Fig&#46; 3</a>&#41;&#46;</p><p id="par0115" class="elsevierStylePara elsevierViewall">Surgical wound lavage with chlorhexidine soap solution was interpreted as possibly responsible for the high colonization&#47;infection rate in trauma surgeries&#44; although this practice could only be confirmed in a low percentage of patients by surgery records&#46; It should be mentioned that surgical wound lavage with sterile physiological solution is recommended in this institution&#46;</p><p id="par0120" class="elsevierStylePara elsevierViewall">The intrinsic contamination of the antiseptic soapy chlorhexidine solution prompted the following measures&#58; removal of all 4&#37; chlorhexidine soap solution bottles from the entire facility&#59; notification to the supplier about the presence of <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; in unopened bottles of 4&#37; chlorhexidine soap solution&#59; and the complaint to the relevant health authorities&#44; the National Administration for Drugs&#44; Food and Medical Technology &#40;<span class="elsevierStyleItalic">Administraci&#243;n Nacional de Medicamentos&#44; Alimentos y Tecnolog&#237;a M&#233;dica</span> &#40;ANMAT&#41;&#41;&#46;</p><p id="par0125" class="elsevierStylePara elsevierViewall">Since this antiseptic was removed&#44; between May and June 2016&#44; the presence of <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; was detected only once in the course of the next 18 months&#44; corresponding to in a clinical sample from the orthopedic operating room in a post-intervention toilet&#44; which was interpreted as contamination&#46; The withdrawal of all the vials in the institution continued to be reinforced&#46;</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Discussion</span><p id="par0130" class="elsevierStylePara elsevierViewall">In this study we describe two simultaneous events attributable to two different <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; contaminated sources&#44; in addition to incorrect procedures that facilitated their dissemination&#46; One event was related to an episode of pseudo-bacteremia due to sodium citrate blood collection tubes contaminated with <span class="elsevierStyleItalic">A&#46; insuavis</span> added to a deficient technique in the loading of blood culture bottles&#44; which caused their contamination&#46; The other corresponded to <span class="elsevierStyleItalic">Achromobacter</span> genogroup 20 infections and colonizations caused by an intrinsically contaminated chlorhexidine soap solution&#44; which was probably used in surgical wound healing and other clinical scenarios&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">The undesirable effect of contaminated blood culture and their financial impact is well known&#44; being independently associated with increased laboratory charges&#44; hospitalization admission and inappropriate use of intravenous antibiotics<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">4</span></a>&#46;</p><p id="par0140" class="elsevierStylePara elsevierViewall">The risk of antiseptic solution contamination&#44; especially by gram negative bacilli&#44; is well documented in the medical literature<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">15</span></a>&#46; Moreover&#44; pseudo-bacteremia outbreaks have been already associated with <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; contaminated chlorhexidine aqueous solutions<a class="elsevierStyleCrossRefs" href="#bib0095"><span class="elsevierStyleSup">3&#44;10</span></a>&#46; However&#44; outbreaks with a predominance of clinical samples related to surgical wounds&#44; such as the one described in this study&#44; are infrequent&#46; In other <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; pseudo-outbreaks&#44; contamination of the chlorhexidine spray pipette has been described&#44; although it was ruled out in this study by direct sampling of chlorhexidine with sterile pipettes avoiding the passage through the spray pipette of the container&#46;</p><p id="par0145" class="elsevierStylePara elsevierViewall">The investigation process of these events was cumbersome&#44; in part due to the presence of two different species of the same genus that could not be identified by phenotypic tests in the routine laboratory&#44; added to the great variety of sample types and different hospital areas involved&#46; Molecular approaches were critical to achieving the accurate species identification and to assess the clonal relationship of the isolates&#46; The importance of the multidisciplinary work of microbiologists&#44; infectious disease specialists&#44; epidemiologists and nurses in infection control should be emphasized&#44; with great perseverance in elucidating this epidemiological situation&#46;</p><p id="par0150" class="elsevierStylePara elsevierViewall">This study confirms&#44; once more&#44; the likelihood of aqueous chlorhexidine solution contamination by ubiquitous environmental hydrophilic microorganisms such as <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; with the hazard of related hospital outbreaks and pseudo-outbreaks&#46; In addition&#44; it highlights the importance of conducting outbreak investigations&#44; persisting even with initial disappointing findings&#44; implementing molecular studies&#44; alerting against this type of deviations&#44; and highlighting the need to reinforce microbiological controls &#40;including long-term microbiological stability&#41; in antiseptic production companies&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Funding</span><p id="par0155" class="elsevierStylePara elsevierViewall">This work was partially supported by grants from <span class="elsevierStyleGrantSponsor" id="gs1">UBACyT</span> to M&#46; Radice &#40;<span class="elsevierStyleGrantNumber" refid="gs1">20020150100174BA</span>&#41; and G&#46; Gutkind &#40;<span class="elsevierStyleGrantNumber" refid="gs1">20020130100432BA</span>&#41; and by <span class="elsevierStyleGrantSponsor" id="gs2">ANPCYT</span><span class="elsevierStyleGrantNumber" refid="gs2">PICT-2017-3996</span> to Mariana Papalia&#46;</p><p id="par0160" class="elsevierStylePara elsevierViewall">M&#46; Radice&#44; G&#46; Gutkind&#44; M&#46; Papalia are members of Carrera del Investigador Cient&#237;fico &#40;CONICET&#41;&#46;</p><p id="par0165" class="elsevierStylePara elsevierViewall">Hospital Italiano &#8211; The funds correspond to the budget assigned to the infection committee&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conflict of interest</span><p id="par0170" class="elsevierStylePara elsevierViewall">None declared&#46;</p></span></span>"
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            2 => "Genotyping"
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    "highlights" => array:2 [
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      "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall"><ul class="elsevierStyleList" id="lis0005"><li class="elsevierStyleListItem" id="lsti0005"><span class="elsevierStyleLabel">&#8226;</span><p id="par0005" class="elsevierStylePara elsevierViewall">Description of two events of nosocomial <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; outbreak and pseudo-outbreak&#46;</p></li><li class="elsevierStyleListItem" id="lsti0010"><span class="elsevierStyleLabel">&#8226;</span><p id="par0010" class="elsevierStylePara elsevierViewall">Contamination of sodium citrate blood collection tubes with <span class="elsevierStyleItalic">Achromobacter insuavis&#46;</span></p></li><li class="elsevierStyleListItem" id="lsti0015"><span class="elsevierStyleLabel">&#8226;</span><p id="par0015" class="elsevierStylePara elsevierViewall">Chlorhexidine soap contaminated with <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; caused infections&#46;</p></li><li class="elsevierStyleListItem" id="lsti0020"><span class="elsevierStyleLabel">&#8226;</span><p id="par0020" class="elsevierStylePara elsevierViewall">Molecular approaches were critical to achieve the accurate species identification&#46;</p></li><li class="elsevierStyleListItem" id="lsti0025"><span class="elsevierStyleLabel">&#8226;</span><p id="par0025" class="elsevierStylePara elsevierViewall">The multidisciplinary work was essential to elucidate the epidemiological situation&#46;</p></li></ul></p></span>"
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        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleItalic">Achromobacter</span> spp&#46; are increasingly recognized as emerging pathogens in immunocompromised patients or suffering cystic fibrosis&#44; but unusual in immunocompetent hosts or individuals that underwent surgery&#46; In this study we describe two simultaneous events attributable to two different <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; contaminated sources&#46; One event was related to an episode of pseudo-bacteremia due to sodium citrate blood collection tubes contaminated with <span class="elsevierStyleItalic">Achromobacter insuavis</span> and the other to <span class="elsevierStyleItalic">Achromobacter</span> genogroup 20 infection and colonization caused by an intrinsically contaminated chlorhexidine soap solution&#46; Both threatened the appropriate use of antimicrobials&#46; Molecular approaches were critical to achieving the accurate species identification and to assess the clonal relationship&#44; strengthening the need for dedicated&#44; multidisciplinary and collaborative work of microbiologists&#44; specialists in infectious diseases&#44; epidemiologists and nurses in the control of infections to clarify these epidemiological situations&#46;</p></span>"
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      "es" => array:2 [
        "titulo" => "Resumen"
        "resumen" => "<span id="abst0015" class="elsevierStyleSection elsevierViewall"><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleItalic">Achromobacter</span> spp&#46; son reconocidas con mayor frecuencia como pat&#243;genos emergentes en pacientes con fibrosis qu&#237;stica e inmunodeprimidos&#44; pero son inusuales en hospedadores inmunocompetentes o quir&#250;rgicos&#46; En este estudio describimos 2 eventos simult&#225;neos atribuibles a 2 fuentes contaminadas con <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; Uno correspondi&#243; a un episodio de seudobacteriemia por tubos de citrato de sodio contaminados con <span class="elsevierStyleItalic">Achromobacter insuavis</span> y el otro a infecciones y colonizaciones debidas al uso de soluci&#243;n jabonosa de clorhexidina intr&#237;nsecamente contaminada con <span class="elsevierStyleItalic">Achromobacter</span> genogrupo 20&#46; Ambos episodios pusieron en peligro el uso apropiado de antimicrobianos&#46; Los enfoques moleculares fueron fundamentales para lograr la identificaci&#243;n precisa de las especies y evaluar la relaci&#243;n clonal de los aislamientos&#44; lo que refuerza la necesidad del trabajo perseverante y multidisciplinario de microbi&#243;logos&#44; especialistas en enfermedades infecciosas&#44; epidemi&#243;logos y enfermeras en el control de infecciones para el esclarecimiento de estas situaciones epidemiol&#243;gicas&#46;</p></span>"
      ]
    ]
    "apendice" => array:1 [
      0 => array:1 [
        "seccion" => array:1 [
          0 => array:4 [
            "apendice" => "<p id="par0180" class="elsevierStylePara elsevierViewall">The following are the supplementary data to this article&#58;<elsevierMultimedia ident="upi0005"></elsevierMultimedia></p>"
            "etiqueta" => "Appendix A"
            "titulo" => "Supplementary data"
            "identificador" => "sec0035"
          ]
        ]
      ]
    ]
    "multimedia" => array:4 [
      0 => array:7 [
        "identificador" => "fig0005"
        "etiqueta" => "Figure 1"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "gr1.jpeg"
            "Alto" => 2749
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            "Tamanyo" => 668995
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        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Dendrogram based on Maximum Likelihood estimation conducted using MEGA 5&#46;05 for <span class="elsevierStyleItalic">Achromobacter</span> spp&#46; concatenated housekeeping genes&#46;</p>"
        ]
      ]
      1 => array:8 [
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        "tipo" => "MULTIMEDIATABLA"
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            "identificador" => "at1"
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                0 => """
                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Patient information &#40;n&#58; 59&#41;&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Number of patients&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Age</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="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">49 years &#40;average&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\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"><span class="elsevierStyleItalic">Sex</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="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">21 female&#47;38 male&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " colspan="2" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleVsp" style="height:0.5px"></span></td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " colspan="2" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Underlying disease</span></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"><span class="elsevierStyleHsp" style=""></span>Immunocompromised patients&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">16&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"><span class="elsevierStyleHsp" style=""></span>Solid organ and bone marrow transplantation&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></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"><span class="elsevierStyleHsp" style=""></span>Solid tumor surgery&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">12 &#40;6 bone tumors&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\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"><span class="elsevierStyleHsp" style=""></span>Others&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " colspan="2" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleVsp" style="height:0.5px"></span></td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " colspan="2" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Other comorbidities</span></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"><span class="elsevierStyleHsp" style=""></span>Diabetes&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">6&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></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"><span class="elsevierStyleHsp" style=""></span>Hepatic failure&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></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"><span class="elsevierStyleHsp" style=""></span>Peripheral cardiovascular disease&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></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"><span class="elsevierStyleHsp" style=""></span>Neurological disease&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">4&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"><span class="elsevierStyleHsp" style=""></span>Chronic respiratory disease&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " colspan="2" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleVsp" style="height:0.5px"></span></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"><span class="elsevierStyleItalic">Orthopedics and traumatology patients</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="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">38 &#40;6 bone tumors&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\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"><span class="elsevierStyleItalic">In-patients in internal medicine</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="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">7&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"><span class="elsevierStyleItalic">In-patients in critical units</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="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">10&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Surgery patients</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="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">4&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"><span class="elsevierStyleItalic">Achromobacter</span> spp&#46; infection&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">16&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"><span class="elsevierStyleItalic">Achromobacter</span> spp&#46; colonization&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">43&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">30-Day mortality&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1 &#40;unrelated death&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
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            ]
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        ]
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          "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Characteristics of patients with microbiological samples &#40;not blood cultures&#41; positive for <span class="elsevierStyleItalic">Achromobacter</span> spp&#46;</p>"
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                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Clinical specimens &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>94&#41;&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">2014 &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>13&#41;&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">2015 &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>54&#41;&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">2016 &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>27&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Respiratory samples&#58; tracheal aspirate&#44; bronchoalveolar lavage&#44; sputum&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">7&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&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">Post-orthopedic surgery samples&#58; bone&#44; soft tissue&#44; wound&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
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ISSN: 03257541
Original language: English
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es en pt

¿Es usted profesional sanitario apto para prescribir o dispensar medicamentos?

Are you a health professional able to prescribe or dispense drugs?

Você é um profissional de saúde habilitado a prescrever ou dispensar medicamentos