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Original article
Assessment of anaerobic blood cultures in pediatric oncology patients
Valoración del hemocultivo anaerobio en pacientes oncológicos pediátricos
Manuel Monsonís Cabedoa, Susana Rives Soláb, Antoni Noguera-Julianc, Mireia Urrea Ayalad, Ofelia Cruz Martinezb, Amadeu Gené Giralta,
Corresponding author
agene@hsjdbcn.org

Corresponding author.
a Department of Microbiology, Hospital Sant Joan de Déu, Esplugues de Llobregat, Barcelona, Spain
b Department of Haematology and Oncology, Hospital Sant Joan de Déu, Esplugues de Llobregat, Barcelona, Spain
c Infectious Diseases Unit, Department of Pediatrics, Hospital Sant Joan de Déu, Esplugues de Llobregat, Barcelona, Spain
d Infections Control Unit, Hospital Sant Joan de Déu, Esplugues de Llobregat, Barcelona, Spain
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according to our protocol&#44; blood samples from pediatric patients are inoculated only in pediatric aerobic bottles&#44; except in selected patients presenting with clinical conditions that increase the risk of anaerobic infection&#44; such as neutropenia&#44; corticosteroid therapy or central venous catheters&#46;<a class="elsevierStyleCrossRefs" href="#bib0080"><span class="elsevierStyleSup">1&#8211;3</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">Although chemotherapy and treatment procedures for malignant diseases have evolved swiftly in recent years&#44; updated information on anaerobic etiology of BSI in this specific group of pediatric patients is lacking&#46; The aim of this study was to assess the current etiology of BSI in our geographical area and the usefulness of routinely performing anaerobic BC in pediatric oncology patients presenting with fever&#44; usually in the setting of chemotherapy-induced neutropenia &#40;FN&#41;&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Material and methods</span><p id="par0020" class="elsevierStylePara elsevierViewall">We present an observational prospective study in a cohort of oncology pediatric patients &#40;&#60;18 years at inclusion&#41; that present with fever during chemotherapy&#44; in most cases during neutropenia periods&#44; in Hospital Sant Joan de D&#233;u &#40;Barcelona&#41;&#44; a tertiary-care pediatric-maternal university hospital with 350 beds that serves a geographical area containing approximately two million people&#59; our center also receives patients from the rest of Catalonia and Spain who require treatment for severe illnesses&#46; The local ethics committee approved the study&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">Blood samples were routinely taken by trained officers&#44; splitted in two equal volumes and inoculated into one pediatric aerobic BacT&#47;Alert PF bottle and into one standard anaerobic BacT&#47;Alert SN bottle&#44; to be later processed using BacT&#47;Alert &#40;BioM&#233;rieux&#44; Durham&#44; NC&#44; USA&#41; automatic incubation system&#46; Our BC collection protocol recommends an optimal blood sample of at least 4<span class="elsevierStyleHsp" style=""></span>mL per bottle&#46; In this study&#44; due to the characteristics of the patients&#44; the final volume was usually only between 1 and 2<span class="elsevierStyleHsp" style=""></span>mL per bottle&#44; although any volume available was accepted&#46; Most samples were obtained from intravascular devices &#40;IVD&#41;&#44; usually a one-lumen tunneled central venous catheter &#40;Port-A-Cath&#41;&#46; BC were performed at onset of each FN episode&#44; and again after 48&#8211;72<span class="elsevierStyleHsp" style=""></span>h if fever persisted despite antibiotics&#46; Isolates were considered clinically significant if one of the following criteria were met&#58; &#40;a&#41; when the isolated microorganism was considered a usual pathogen &#40;e&#46;g&#46; enteric gram-negative rods&#41;&#59; &#40;b&#41; when a microorganism usually considered contaminant &#40;e&#46;g&#46; coagulase-negative staphylococci&#41; was isolated in both aerobic and anaerobic bottles during the first 48<span class="elsevierStyleHsp" style=""></span>h of incubation&#59; &#40;c&#41; when the same usually contaminant strain was persistently isolated in consecutive BC&#59; or &#40;d&#41; was IVD-related&#58; BSI was judged to be IVD-related when fever coincided with the use of the device&#44; when the same strain was isolated from BC and the device exit site&#44; when resolution of symptoms coincided with the removal of the IVD or when the same microorganism was isolated from the device culture after its removal&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">In order to establish the clinical significance of each isolate&#44; clinical and microbiological data were collected and assessed prospectively together with the physician in charge of the patient&#46; Dubious cases under full antibiotic treatment were considered clinically significant in this study&#46;</p><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Statistical analysis</span><p id="par0035" class="elsevierStylePara elsevierViewall">Categorical variables were described as percentages&#44; and continuous variables as mean&#47;standard deviation &#40;SD&#41; or median&#47;ranges&#46;</p></span></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Results</span><p id="par0040" class="elsevierStylePara elsevierViewall">During the 21-month study period &#40;January 2014&#8211;September 2015&#41;&#44; 876 BC &#40;aerobic and anaerobic paired bottles&#41; from 228 patients &#40;43&#46;4&#37; females&#44; mean age&#58; 6&#46;7 years &#40;SD&#58; 4&#46;9&#41;&#44; ranging from 6 months to 18 years&#41; were processed in the microbiology laboratory&#46; Baseline diagnosis included solid tumors <span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>143 &#40;affecting central nervous system&#44; <span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>62&#59; muscular and skeletal&#44; <span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>28&#59; kidney <span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>12&#59; histiocytosis <span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>10&#59; and others <span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>31&#41;&#44; acute leukemia &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>67&#41; and lymphoma &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>18&#41;&#46; Among patients with solid tumors&#44; there were 22 patients that had received an autologous peripheral blood stem cell transplantation&#46; No patient included in this study underwent an allogeneic stem cell transplantation&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">Bacterial growth&#44; yielding 95 isolates&#44; was detected in 90 BC &#40;10&#46;2&#37;&#41; of which 62 &#40;7&#46;1&#37;&#41;&#44; corresponding to 63 isolates&#44; were considered clinically significant and 28 &#40;3&#46;2&#37;&#41;&#44; corresponding to 32 isolates &#40;17 coagulase-negative staphylococci&#44; 5 viridians streptococci group&#44; 5 <span class="elsevierStyleItalic">Micrococcus</span> spp&#46;&#44; 1 <span class="elsevierStyleItalic">Corynebacterium</span> spp&#46;&#44; 1 <span class="elsevierStyleItalic">Moraxella</span> spp&#46; and 3 <span class="elsevierStyleItalic">Propionibacterium acnes</span>&#41;&#44; were deemed contaminants&#46; In 5 BC two different microorganisms were simultaneously isolated&#44; of which only one case &#40;<span class="elsevierStyleItalic">Escherichia coli</span> and <span class="elsevierStyleItalic">Klebsiella pneumoniae</span>&#41; was considered true bacteremia&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">Taking into account only the 63 clinically significant microorganisms &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#44; 38 &#40;60&#46;3&#37;&#41; of them grew in both aerobic and anaerobic bottles&#44; 18 &#40;28&#46;6&#37;&#41; only in aerobic bottles and 7 &#40;11&#46;1&#37;&#41; &#40;1 <span class="elsevierStyleItalic">Staphylococcus aureus</span>&#44; 2 coagulase-negative staphylococci&#44; 1 <span class="elsevierStyleItalic">Streptococcus pneumoniae</span> and 3 <span class="elsevierStyleItalic">E&#46; coli</span>&#41; only in anaerobic bottles&#46; Altogether&#44; 56 clinically significant isolates &#40;88&#46;9&#37;&#41; grew in aerobic bottles and 45 &#40;71&#46;4&#37;&#41; in anaerobic bottles&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0055" class="elsevierStylePara elsevierViewall">Apart from strict aerobes &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>13&#44; 20&#46;6&#37;&#58; <span class="elsevierStyleItalic">Pseudomonas aeruginosa</span>&#44; <span class="elsevierStyleItalic">Acinetobacter lwoffii</span>&#44; <span class="elsevierStyleItalic">Micrococcus</span> spp<span class="elsevierStyleItalic">&#46;</span> and <span class="elsevierStyleItalic">Candida albicans</span>&#41; that usually grow only in aerobic bottles&#44; the rest of clinically significant isolates were facultative aerobic&#47;anaerobic microorganisms of which 37 &#40;74&#37;&#41; grew in both aerobic and anaerobic bottles&#44; 6 &#40;12&#37;&#41; only in aerobic bottles and 7 &#40;14&#37;&#41; only in anaerobic bottles&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">Among clinically significant isolates&#44; gram-negative rods &#40;33&#59; 52&#46;4&#37;&#41;&#44; mainly belonging to the <span class="elsevierStyleItalic">Enterobacteriaceae</span> family &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>25&#59; 75&#46;8&#37;&#41;&#44; were the more frequently isolated microorganisms&#44; followed by gram-positive cocci &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>28&#59; 44&#46;4&#37;&#41;&#44; mainly coagulase-negative staphylococci &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>17&#59; 60&#46;7&#37;&#41;&#46; One episode of infection &#40;2 isolates&#41; accounted for yeasts&#46; Overall&#44; only 3 isolates were strict anaerobes &#40;<span class="elsevierStyleItalic">Propionibacterium acnes</span>&#41; and all of them were deemed contaminants&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">In 5 patients the same strain &#40;1 coagulase-negative staphylococci&#44; 2 <span class="elsevierStyleItalic">Micrococcus</span> spp&#46;&#44; 1 <span class="elsevierStyleItalic">Acinetobacter lwoffii</span> and 1 <span class="elsevierStyleItalic">Candida albicans</span>&#41; was isolated in two different BC during the same episode of infection&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">In 6 patients the same strain &#40;<span class="elsevierStyleItalic">Escherichia coli</span>&#44; <span class="elsevierStyleItalic">Micrococcus</span> spp<span class="elsevierStyleItalic">&#46;</span> and coagulase-negative <span class="elsevierStyleItalic">Staphylococcus</span>&#44; 2 patients each&#41; was isolated in two or more episodes &#40;one strain of <span class="elsevierStyleItalic">Escherichia coli</span> was isolated in three episodes&#41;&#44; and the infection was considered to be related with persistent IVD colonization&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">Overall&#44; after discarding contaminant microorganisms and taking into account only one isolate of the same strain in each episode of infection&#44; 57 episodes&#44; attributable to 58 microorganisms&#44; of BSI in 50 FN pediatric patients were microbiologically confirmed&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Discussion</span><p id="par0080" class="elsevierStylePara elsevierViewall">Our results show a predominance of isolates belonging to <span class="elsevierStyleItalic">Enterobacteriaceae</span> family and <span class="elsevierStyleItalic">Staphylococcus</span> spp&#46; in pediatric patients with FN&#44; which is in accordance with previous studies&#44; carried out in both pediatric<a class="elsevierStyleCrossRefs" href="#bib0095"><span class="elsevierStyleSup">4&#44;5</span></a> and adult<a class="elsevierStyleCrossRefs" href="#bib0105"><span class="elsevierStyleSup">6&#44;7</span></a> patients&#44; and also with our own previous experience&#44;<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">8</span></a> when anaerobic BC were routinely performed in our hospital&#46; These results confirm that strictly anaerobic bacteria are very seldom involved in oncology pediatric patients with FN&#59; actually&#44; we did not detect a single episode of BSI due to these microorganisms in our large prospective study&#46; Consequently&#44; neutropenia did not enhance the risk of anaerobic BSI as compared with general pediatric patients in our hospital&#46;<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">8</span></a> Therefore&#44; if the only goal of anaerobic bottles were the isolation of strict anaerobes&#44; it would not be worth to use them&#46; Nevertheless&#44; the influence of systematic anaerobic BC bottles in the isolation of facultative aerobic&#47;anaerobic and strict aerobic microorganisms needs to be considered&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">With regard to strict aerobic microorganisms&#44; the isolation of yeasts in BC from patients with FN in our center has progressively decreased in recent years and at present its incidence rate is very low&#44; probably due to antifungal prophylactic treatments&#46; Nevertheless non-fermenting gram-negative rods remain frequently isolated&#46; In our study&#44; strict aerobic microorganisms &#40;including those <span class="elsevierStyleItalic">Micrococcus</span> spp&#46; that were considered clinically significant&#41; accounted for 15&#46;5&#37; of BSI episodes&#46; It is important to point out that many of these microorganisms are clinically less predictable&#44; display greater variability in terms of resistance to antibiotics than anaerobic pathogens&#44;<a class="elsevierStyleCrossRefs" href="#bib0120"><span class="elsevierStyleSup">9&#8211;11</span></a> and may not be covered by standard empirical antibiotic treatment&#59; others&#44; like yeasts&#44; need specific treatment&#46; Therefore&#44; their proper microbiological diagnosis is of greater clinical importance&#46;</p><p id="par0090" class="elsevierStylePara elsevierViewall">We observed that when facultative aerobic&#47;anaerobic microorganisms were detected only in one bottle&#44; there were no differences between aerobic and anaerobic bottles &#40;12&#37; and 14&#37; respectively&#41;&#46; These data suggest that anaerobic BC offer no diagnostic advantage for this group of bacteria in children with FN&#46;</p><p id="par0095" class="elsevierStylePara elsevierViewall">Why facultative aerobic&#47;anaerobic bacteria grew only in one bottle would be explained by a random event&#44; more likely related with low bacterial concentration in the specimen and small sample volume than with the aerobic or anaerobic atmosphere itself&#46;<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">1</span></a> It is important to point out that the greater the volume of blood inoculated&#44; the greater the yield from blood cultures&#46;<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">12</span></a> This is particularly relevant in pediatrics because of the difficulty of getting an optimal volume of blood sample in some patients&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">Moreover&#44; because a specific pediatric anaerobic bottle is not commercially available&#44; the volume of media in each anaerobic bottle was twice the volume in each pediatric aerobic bottle&#44; but the volume of inoculated blood was the same&#46; This diminishes the concentration of bacteria by one half in the culture medium and might contribute to lower the rate of isolation in anaerobic BC&#46; Therefore&#44; it is likely that bacterial recovery would potentially be enhanced by inoculating the entire sample into the aerobic medium&#46;</p><p id="par0105" class="elsevierStylePara elsevierViewall">An important issue&#44; in practical terms&#44; is how to discriminate contamination from infection when common saprophytic bacteria are involved &#40;coagulase-negative <span class="elsevierStyleItalic">staphylococci</span>&#44; <span class="elsevierStyleItalic">Micrococcus</span> spp&#46;&#44; <span class="elsevierStyleItalic">Corynebacterium</span> spp&#46;&#44; <span class="elsevierStyleItalic">Streptococcus viridans</span>&#44; <span class="elsevierStyleItalic">Propionibacterium</span> spp&#46;&#44; <span class="elsevierStyleItalic">Bacillus</span> spp&#46;&#44; etc&#46;&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">13</span></a> In our study these microorganisms were considered etiologically related with 36&#46;2&#37; of BSI episodes&#46; Usually&#44; in pediatric oncology patients&#44; fever is the most common and earliest symptom of BSI&#46; But fever may also occur due to the administration of blood products or as an adverse event of cytotoxic therapy&#46; In addition&#44; almost all patients carry permanent IVD during the treatment period&#44; which are known to get contaminated by these microorganisms&#44; often leading to BSI&#46;<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">14</span></a> There are not specific and definitive microbiological criteria to discriminate between contamination and BSI&#44; but the isolation of these microorganisms from at least two blood samples would back up their etiological role&#46;<a class="elsevierStyleCrossRefs" href="#bib0080"><span class="elsevierStyleSup">1&#44;14</span></a></p><p id="par0110" class="elsevierStylePara elsevierViewall">In conclusion&#44; considering that strict anaerobes rarely cause BSI in pediatric patients with malignancies and FN and also the difficulty to obtain blood samples of sufficient volume to ensure an optimal diagnostic approach in these patients&#44; we think&#44; consistently with other authors&#8217; opinions&#44;<a class="elsevierStyleCrossRefs" href="#bib0130"><span class="elsevierStyleSup">11&#44;15</span></a> that BC should be solely processed in aerobic medium in these patients&#44; in order to enhance the isolation of the most common microorganisms&#44; especially strict aerobes&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Funding</span><p id="par0115" class="elsevierStylePara elsevierViewall">This article has not received specific funding&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Conflict of interest</span><p id="par0120" class="elsevierStylePara elsevierViewall">The authors of this article have no conflict of interest in relation to its content&#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 routine use of a single aerobic bottle for blood culture in pediatric patients has become commonplace&#44; as anaerobic bacteria are not frequently involved in clinically significant infections&#46; The aim of this study was to assess the usefulness of routinely performing anaerobic blood cultures in pediatric oncology patients&#46;</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Methods</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Prospective study was conducted on pediatric &#40;&#60;18 years&#41; patients affected with febrile syndrome after receiving chemotherapy for hematological or solid malignancies&#46; Samples were inoculated into pediatric aerobic and standard anaerobic bottles &#40;BacT&#47;Alert automatic system&#41;&#46; Strains were considered clinically significant&#44; or deemed as contaminants&#44; depending on isolation circumstances and clinical criteria&#46;</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">A total of 876 blood cultures from 228 patients were processed during the 21-month study period &#40;January 2014 to September 2015&#41;&#46; Baseline diagnosis included 143 solid tumors and 67&#47;18 cases of leukemia&#47;lymphoma&#46; Bacterial growth was detected in 90 &#40;10&#46;2&#37;&#41; blood cultures for 95 different isolates&#44; of which 62 &#40;7&#46;1&#37;&#41;&#47;63 isolates were considered clinically significant&#46; Among the latter&#44; 38 &#40;60&#46;3&#37;&#41; microorganisms grew in both aerobic and anaerobic bottles&#44; 18 &#40;28&#46;6&#37;&#41; only in aerobic bottles&#44; and 7 &#40;11&#46;1&#37;&#41; only in anaerobic bottles&#46; Gram-negative bacilli &#40;33&#59; 52&#46;4&#37;&#41;&#44; mainly from the <span class="elsevierStyleItalic">Enterobacteriaceae</span> family&#44; were the most frequently isolated microorganisms&#46; Overall&#44; only 3 out of 90 isolates &#40;3&#46;3&#37;&#41; were strict anaerobes &#40;<span class="elsevierStyleItalic">Propionibacterium acnes</span>&#41;&#44; and all of them were deemed contaminants&#46;</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Conclusion</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Strict anaerobes did not cause significant infections in febrile pediatric oncology patients&#44; and anaerobic blood culture bottles offered no additional advantages over aerobic media&#46; Our results suggest that routine blood cultures should be solely processed in aerobic media in this group of patients&#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">En pacientes pedi&#225;tricos es habitual el procesamiento de hemocultivos &#250;nicamente en medio aerobio&#44; debido a la escasa relevancia de los microorganismos anaerobios en la etiolog&#237;a infecciosa habitual&#46; El objetivo de este estudio es valorar la utilidad del uso rutinario del medio de cultivo anaerobio en pacientes oncol&#243;gicos pedi&#225;tricos&#46;</p></span> <span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">M&#233;todos</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Estudio prospectivo en pacientes pedi&#225;tricos &#40;&#60;18<span class="elsevierStyleHsp" style=""></span>a&#241;os&#41; en tratamiento quimioter&#225;pico de procesos oncol&#243;gicos con s&#237;ndrome febril&#46; Las muestras se inocularon en botellas aerobias pedi&#225;tricas y anaerobias est&#225;ndar &#40;sistema autom&#225;tico BacT&#47;Alert&#41;&#46; Las cepas aisladas fueron consideradas cl&#237;nicamente significativas o contaminantes en funci&#243;n de las circunstancias de aislamiento y la cl&#237;nica del paciente&#46;</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Durante el periodo de estudio &#40;enero 2015-septiembre 2016&#41; se procesaron 876 hemocultivos procedentes de 228 pacientes diagnosticados de tumores s&#243;lidos &#40;143&#41; y leucemia&#47;linfoma &#40;67&#47;18&#41;&#46; Se detect&#243; crecimiento en 90 &#40;10&#44;2&#37;&#41; hemocultivos y se aislaron 95 cepas&#44; de los cuales 62 &#40;7&#44;1&#37;&#41;&#44; correspondientes a 63 cepas&#44; se consideraron cl&#237;nicamente significativos&#46; Entre estos &#250;ltimos&#44; 38 &#40;60&#44;3&#37;&#41; microorganismos crecieron en ambas botellas&#44; 18 &#40;28&#44;6&#37;&#41; &#250;nicamente en aerobiosis y 7 &#40;11&#44;1&#37;&#41; &#250;nicamente en anaerobiosis&#46; Bacilos gram negativos &#40;33&#59; 52&#44;4&#37;&#41;&#44; mayoritariamente enterobacterias&#44; fueron los m&#225;s frecuentemente aislados&#46; Solo 3 &#40;3&#44;3&#37;&#41; de los microorganismos aislados eran anaerobios estrictos &#40;<span class="elsevierStyleItalic">Propionibacterium acnes</span>&#41;&#44; y todos ellos fueron considerados contaminantes&#46;</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusi&#243;n</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Microorganismos anaerobios est&#225;n raramente involucrados en infecciones en pacientes oncol&#243;gicos pedi&#225;tricos&#44; y la utilizaci&#243;n de botellas anaerobias no ofrece ninguna ventaja adicional&#46; Seg&#250;n nuestros resultados es suficiente el uso de medio aerobio en el procesamiento de los hemocultivos en este tipo de pacientes&#46;</p></span>"
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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="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Microorganisms&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Number of isolates&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Aerobic and anaerobic bottle&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Aerobic bottle&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th><th class="td" title="table-head  " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Anaerobic bottle&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="table-entry  " colspan="5" align="left" valign="top"><span class="elsevierStyleItalic">Gram-positive aerobes</span></td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Staphylococcus aureus</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Coagulase-negative staphylococci&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">17&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">13&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">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="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span>Viridans streptococci group&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&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="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Streptococcus pneumoniae</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Micrococcus</span> spp&#46;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">6&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">6&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " colspan="5" align="left" valign="top"><span class="elsevierStyleVsp" style="height:0.5px"></span></td></tr><tr title="table-row"><td class="td" title="table-entry  " colspan="5" align="left" valign="top"><span class="elsevierStyleItalic">Gram-negative aerobes</span></td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Escherichia coli</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">14&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">8&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">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="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Klebsiella pneumoniae</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&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="elsevierStyleHsp" style=""></span>Other enterobacteriaceae&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">6&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">5&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&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="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Acinetobacter lwoffii</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">3&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&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="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Pseudomonas aeruginosa</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&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="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Campylobacter jejuni</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&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="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Capnocytophaga sputigena</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry  " colspan="5" align="left" valign="top"><span class="elsevierStyleVsp" style="height:0.5px"></span></td></tr><tr title="table-row"><td class="td" title="table-entry  " colspan="5" align="left" valign="top"><span class="elsevierStyleItalic">Yeasts</span></td></tr><tr title="table-row"><td class="td-with-role" title="table-entry ; entry_with_role_rowhead " align="left" valign="top"><span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleItalic">Candida albicans</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="" valign="top">&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="elsevierStyleHsp" style=""></span>Total&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">63&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">38&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">18&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="table-entry  " align="char" valign="top">7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
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          "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Clinically significant microorganisms isolated from blood cultures of pediatric oncology patients and the type of bottle from which they were recovered&#46;</p>"
        ]
      ]
    ]
    "bibliografia" => array:2 [
      "titulo" => "References"
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        0 => array:2 [
          "identificador" => "bibs0005"
          "bibliografiaReferencia" => array:15 [
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                        0 => array:2 [
                          "etal" => false
                          "autores" => array:2 [
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                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:6 [
                        "tituloSerie" => "Pediatr Emerg Care"
                        "fecha" => "2004"
                        "volumen" => "20"
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                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/15232242"
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                  "contribucion" => array:1 [
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es en pt

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