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Antifungal activity of amniotic fluid against different Candida species
Actividad antifúngica del líquido amniótico contra diferentes especies de Candida
Sofia Marakia,
Corresponding author
sofiamaraki@yahoo.gr

Corresponding author.
, Dimitra Stafylakia, Spyridon A. Karageorgosb, Filippos Koutroumpakisc, George Hamilosa, Antonis Makrigiannakisd, George Samonisc
a Department of Clinical Microbiology and Microbial Pathogenesis, University Hospital of Heraklion, Crete, Greece
b Division of Infectious Diseases, Children's Hospital of Philadelphia, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA
c Infectious Diseases Unit, University Hospital of Heraklion and University of Crete Medical School, Heraklion, Crete, Greece
d Department of Obstetrics and Gynecology, Medical School, University of Crete, Heraklion, Greece
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          "en" => "<p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">Kinetics of growth of <span class="elsevierStyleItalic">Candida</span> clinical isolates in the presence of amniotic fluid <span class="elsevierStyleItalic">versus</span> Sabouraud broth &#40;control&#41;&#46; Each line represents the growth curve over time of a sole <span class="elsevierStyleItalic">Candida</span> isolate&#44; grown either in amniotic fluid or in Sabouraud broth &#40;control&#41;&#46; Each symbol represents the log10 CFU value at different time points&#46; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;0001&#59; Student&#39;s <span class="elsevierStyleItalic">t</span> test&#46;</p>"
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    "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Candida</span> species are part of the commensal genital microbiota of approximately 20&#37; of asymptomatic&#44; healthy women during reproductive age&#46;<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">2</span></a> Colonization rates increase to about 30&#37; in pregnant women&#44; particularly during the third trimester&#44; due to the high levels of circulating estrogens that promote yeast adhesion and germination&#46;<a class="elsevierStyleCrossRefs" href="#bib0160"><span class="elsevierStyleSup">12&#44;15</span></a> Among <span class="elsevierStyleItalic">Candida</span> species&#44; <span class="elsevierStyleItalic">Candida albicans</span> is the most frequently isolated&#46; However&#44; due to the widespread use of azoles&#44; other multidrug-resistant species&#44; including <span class="elsevierStyleItalic">Candida glabrata</span>&#44; <span class="elsevierStyleItalic">Candida parapsilosis</span> and <span class="elsevierStyleItalic">Candida tropicalis</span>&#44; are emerging causes of systemic infections worldwide&#46;<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">5</span></a> Despite the high vaginal <span class="elsevierStyleItalic">Candida</span> colonization rates&#44; intrauterine fetal infections due to these yeasts are rarely encountered&#46;<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">4</span></a> This observation is consistent with the antifungal properties of the amniotic fluid &#40;AF&#41; against <span class="elsevierStyleItalic">Candida albicans</span>&#46;<a class="elsevierStyleCrossRefs" href="#bib0145"><span class="elsevierStyleSup">9&#44;11</span></a> However&#44; there is no information on AF activity against non-<span class="elsevierStyleItalic">C&#46; albicans Candida</span> species&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">In this study we evaluated the antifungal effect of AF obtained during the 38th&#8211;41st week of gestation against <span class="elsevierStyleItalic">C&#46; albicans</span>&#44; <span class="elsevierStyleItalic">C&#46; glabrata</span>&#44; and <span class="elsevierStyleItalic">C&#46; parapsilosis</span> clinical isolates&#46; The study included 23 pregnant women followed up at the Obstetrics Department of the University Hospital of Heraklion&#44; in Crete&#44; Greece&#44; from November 2015 to May 2016&#46; The demographics and clinical details of the 23 AF donors are shown in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#46; The requirements to be enrolled were being in a gestational age of 38&#8211;41 weeks at delivery&#44; and giving birth by cesarean section without having taken antibiotics in the previous month&#46; Ethical approval for the study was obtained by the IRB of the hospital &#40;15095&#47;30-3-2016&#41;&#46; Written consent was signed by each study participant&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0015" class="elsevierStylePara elsevierViewall">Amniotic fluid samples were obtained under aseptic conditions by aspirating through the amniotic sac during cesarean section&#46; All women had intact membranes&#46; Samples contaminated with meconium or blood were excluded&#46; The first 10<span class="elsevierStyleHsp" style=""></span>ml of the amniotic fluid were discarded in order to avoid blood&#44; and the remainder was collected in sterile tubes and immediately centrifuged at 3000<span class="elsevierStyleHsp" style=""></span>rpm for 15<span class="elsevierStyleHsp" style=""></span>min&#46; The supernatant was frozen at &#8722;80<span class="elsevierStyleHsp" style=""></span>&#176;C until further processing&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">The strains used to assay the inhibitory activity of AF were recovered from patients with invasive candidiasis and identified by sequencing of the internal transcribed spacer 1 and 2 &#40;ITS1-5&#46;8SrRNA-ITS2&#41;&#46; The isolates are stored in the library of the Department of Clinical Microbiology and Microbial Pathogenesis of the University Hospital of Heraklion&#44; Greece and are available upon request&#46; The sequences of all three isolates were submitted to Genbank&#44; being assigned the following accession numbers&#58; <span class="elsevierStyleItalic">Candida albicans</span> B 8268 &#40;GenBank accession no&#46; MW616800&#41;&#44; <span class="elsevierStyleItalic">Candida glabrata</span> B 81348 &#40;GenBank accession no&#46; MW616799&#41;&#44; and <span class="elsevierStyleItalic">Candida parapsilosis</span> B 81524 &#40;GenBank accession no&#46; MW616798&#41;&#46; The activity of the main antifungal agents against these isolates are shown in <a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#46; Yeasts grown overnight on Sabouraud dextrose agar &#40;bioM&#233;rieux&#44; Marcy L&#8217; Etoile&#44; France&#41; were suspended in sterile normal saline&#46; Serial dilutions of the suspensions with additional normal saline to achieve a concentration of 10<span class="elsevierStyleSup">4</span><span class="elsevierStyleHsp" style=""></span>yeasts&#47;ml were made&#46; From this final dilution&#44; 0&#46;2<span class="elsevierStyleHsp" style=""></span>ml were added to 1&#46;8<span class="elsevierStyleHsp" style=""></span>ml of amniotic fluid&#44; and other 0&#46;2<span class="elsevierStyleHsp" style=""></span>ml to 1&#46;8<span class="elsevierStyleHsp" style=""></span>ml of Sabouraud broth&#46; The latter was the positive control for <span class="elsevierStyleItalic">Candida</span> growth&#46; Amniotic fluids and controls were incubated at 37<span class="elsevierStyleHsp" style=""></span>&#176;C for 48<span class="elsevierStyleHsp" style=""></span>h&#46; Aliquots of 0&#46;2<span class="elsevierStyleHsp" style=""></span>ml were collected both from the amniotic fluids under testing and the controls at 0&#44; 4&#44; 8&#44; 12&#44; 24&#44; and 48<span class="elsevierStyleHsp" style=""></span>h&#44; being serially diluted with normal saline up to 10<span class="elsevierStyleSup">&#8722;12</span>&#46; Samples of 0&#46;1<span class="elsevierStyleHsp" style=""></span>ml of each dilution were streaked on Sabouraud dextrose agar plates&#44; which were incubated for 48<span class="elsevierStyleHsp" style=""></span>h at 37<span class="elsevierStyleHsp" style=""></span>&#176;C&#44; and colony forming units &#40;CFUs&#41; were counted&#46;<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">7</span></a> All experiments were performed in triplicate&#44; in order to check the reproducibility of the results&#46; Differences in CFUs between control and AF samples were compared by unpaired Student&#39;s <span class="elsevierStyleItalic">t</span>-test&#46; Statistical significance was set at <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#46; All statistical analyses were performed with Graphpad Prism&#44; V&#46;4 &#40;GraphPad Software Inc&#44; CA&#44; USA&#41;&#46;</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0025" class="elsevierStylePara elsevierViewall">As shown in <a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#44; all 23 AF samples possessed a significant inhibitory activity against all three clinical isolates of <span class="elsevierStyleItalic">Candida</span>&#46; The antifungal activity of AF was more pronounced against <span class="elsevierStyleItalic">C&#46; glabrata</span>&#44; since all AF samples prevented this species from growing &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; In contrast&#44; when compared to the initial inoculum &#40;0<span class="elsevierStyleHsp" style=""></span>h&#41;&#44; minimal growth was observed in <span class="elsevierStyleItalic">C&#46; albicans</span> &#40;with certain AF samples&#41; and <span class="elsevierStyleItalic">C&#46; parapsilosis</span> &#40;all AF samples&#41; at 48<span class="elsevierStyleHsp" style=""></span>h &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0030" class="elsevierStylePara elsevierViewall">Azole-resistant non-<span class="elsevierStyleItalic">C&#46; albicans</span><span class="elsevierStyleItalic">Candida</span> species&#44; including <span class="elsevierStyleItalic">C&#46; glabrata</span>&#44; are increasingly encountered as causes of urogenital infections worldwide&#46;<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">16</span></a> Despite the increased rates of <span class="elsevierStyleItalic">Candida</span> vaginal colonization during pregnancy&#44; intrauterine infections are extremely uncommon&#46;<a class="elsevierStyleCrossRefs" href="#bib0115"><span class="elsevierStyleSup">4&#44;10</span></a> This is suggestive of a host effector mechanism with specific antifungal properties&#44; including the antifungal properties of AF&#46; Antimicrobial components of AF include cytokines and host defense proteins&#44; including defensins&#44; lactoferrin&#44; lysozyme&#44; and other antimicrobial peptides&#46;<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">6</span></a> In particular&#44; beta-defensin 2 &#40;HBD-2&#41; has been documented as a molecule that prevents <span class="elsevierStyleItalic">Candida</span> proliferation <span class="elsevierStyleItalic">in vitro</span>&#46;<a class="elsevierStyleCrossRef" href="#bib0185"><span class="elsevierStyleSup">17</span></a> Previous works also attributed the antifungal activity of AF to spermine&#44;<a class="elsevierStyleCrossRef" href="#bib0170"><span class="elsevierStyleSup">14</span></a> and to anti-<span class="elsevierStyleItalic">Candida</span> antibodies&#46;<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">13</span></a></p><p id="par0035" class="elsevierStylePara elsevierViewall">Several researchers studied the antibacterial activity of AF against aerobic and anaerobic bacteria&#46;<a class="elsevierStyleCrossRefs" href="#bib0110"><span class="elsevierStyleSup">3&#44;18</span></a> The inhibitory activity of AF against <span class="elsevierStyleItalic">C&#46; albicans</span> has been shown previously&#46;<a class="elsevierStyleCrossRefs" href="#bib0100"><span class="elsevierStyleSup">1&#44;8&#44;9&#44;11&#44;13&#44;14</span></a> This is the first study on the activity of AF against <span class="elsevierStyleItalic">C&#46; albicans</span> and other <span class="elsevierStyleItalic">Candida</span> species&#46; Our results show that AF has inhibitory activity not only against <span class="elsevierStyleItalic">C&#46; albicans</span>&#44; but also against <span class="elsevierStyleItalic">C&#46; glabrata</span> and <span class="elsevierStyleItalic">C&#46; parapsilosis</span>&#46; Only <span class="elsevierStyleItalic">C&#46; glabrata</span> growth was completely inhibited by all 23 AF samples&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">The <span class="elsevierStyleItalic">in vitro</span> antifungal activity of AF against <span class="elsevierStyleItalic">C&#46; albicans</span>&#44; <span class="elsevierStyleItalic">C&#46; glabrata</span> and <span class="elsevierStyleItalic">C&#46; parapsilosis</span> likely exists also <span class="elsevierStyleItalic">in vivo</span>&#44; thus contributing to the prevention of intraamniotic fungal infections&#46; It would be interesting to study the activity of AF against <span class="elsevierStyleItalic">Candida auris</span> and other emerging <span class="elsevierStyleItalic">Candida</span> species&#46; In particular&#44; it is important to understand whether the antifungal activity of AF is mediated by the restriction of important growth factors to the pathogen &#40;<span class="elsevierStyleItalic">e&#46;g&#46;</span>&#44; nutritional immunity&#41; or the presence of antimicrobial peptides &#40;<span class="elsevierStyleItalic">e&#46;g&#46;</span> defensins&#41;&#46;</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Funding</span><p id="par0045" class="elsevierStylePara elsevierViewall">This research did not receive any specific grant from funding agencies in the public&#44; commercial&#44; or not-for-profit sectors&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Conflict of interest</span><p id="par0050" class="elsevierStylePara elsevierViewall">The authors declare that they have no competing interests&#46;</p></span></span>"
    "textoCompletoSecciones" => array:1 [
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          "identificador" => "xres1577131"
          "titulo" => "Abstract"
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            0 => array:2 [
              "identificador" => "abst0005"
              "titulo" => "Background"
            ]
            1 => array:2 [
              "identificador" => "abst0010"
              "titulo" => "Aims"
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            2 => array:2 [
              "identificador" => "abst0015"
              "titulo" => "Methods"
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            3 => array:2 [
              "identificador" => "abst0020"
              "titulo" => "Results"
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            4 => array:2 [
              "identificador" => "abst0025"
              "titulo" => "Conclusions"
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        1 => array:2 [
          "identificador" => "xpalclavsec1421266"
          "titulo" => "Keywords"
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        2 => array:3 [
          "identificador" => "xres1577132"
          "titulo" => "Resumen"
          "secciones" => array:5 [
            0 => array:2 [
              "identificador" => "abst0030"
              "titulo" => "Antecedentes"
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            1 => array:2 [
              "identificador" => "abst0035"
              "titulo" => "Objetivos"
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            2 => array:2 [
              "identificador" => "abst0040"
              "titulo" => "M&#233;todos"
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            3 => array:2 [
              "identificador" => "abst0045"
              "titulo" => "Resultados"
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            4 => array:2 [
              "identificador" => "abst0050"
              "titulo" => "Conclusiones"
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        3 => array:2 [
          "identificador" => "xpalclavsec1421265"
          "titulo" => "Palabras clave"
        ]
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          "titulo" => "Funding"
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          "titulo" => "References"
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    ]
    "pdfFichero" => "main.pdf"
    "tienePdf" => true
    "fechaRecibido" => "2020-05-24"
    "fechaAceptado" => "2021-02-26"
    "PalabrasClave" => array:2 [
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        0 => array:4 [
          "clase" => "keyword"
          "titulo" => "Keywords"
          "identificador" => "xpalclavsec1421266"
          "palabras" => array:5 [
            0 => "Amniotic fluid"
            1 => "Antifungal activity"
            2 => "<span class="elsevierStyleItalic">Candida albicans</span>"
            3 => "<span class="elsevierStyleItalic">Candida glabrata</span>"
            4 => "<span class="elsevierStyleItalic">Candida parapsilosis</span>"
          ]
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          "clase" => "keyword"
          "titulo" => "Palabras clave"
          "identificador" => "xpalclavsec1421265"
          "palabras" => array:5 [
            0 => "L&#237;quido amni&#243;tico"
            1 => "Actividad antif&#250;ngica"
            2 => "<span class="elsevierStyleItalic">Candida albicans</span>"
            3 => "<span class="elsevierStyleItalic">Candida glabrata</span>"
            4 => "<span class="elsevierStyleItalic">Candida parapsilosis</span>"
          ]
        ]
      ]
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    "tieneResumen" => true
    "resumen" => array:2 [
      "en" => array:3 [
        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Background</span><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Although <span class="elsevierStyleItalic">Candida</span> is a commensal of the urogenital tract&#44; intrauterine fungal infections are extremely uncommon in clinical practice&#46;</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Aims</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">In the present work we evaluated whether amniotic fluid &#40;AF&#41; possesses direct antifungal activity against clinical isolates of <span class="elsevierStyleItalic">Candida</span><span class="elsevierStyleItalic">albicans</span> and other <span class="elsevierStyleItalic">Candida</span> species&#46;</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Methods</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">A total of 23 AF samples from pregnant women with gestational age of 38&#8211;41 weeks were obtained under aseptic conditions by the aspiration of the amniotic sac during cesarean section&#46; Different <span class="elsevierStyleItalic">Candida</span> species were inoculated in amniotic fluid and Sabouraud broth&#44; used as control&#44; and were incubated at 37<span class="elsevierStyleHsp" style=""></span>&#176;C for 48<span class="elsevierStyleHsp" style=""></span>h&#46; Quantitative cultures of test samples and controls were performed at 0&#44; 4&#44; 8&#44; 12&#44; 24&#44; and 48<span class="elsevierStyleHsp" style=""></span>h&#46;</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Results</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">AF collected from 23 pregnant women had consistent and significant inhibitory activity against all <span class="elsevierStyleItalic">Candida</span> isolates tested&#46; Nonetheless&#44; a complete inhibition of growth by all 23 AF samples tested was observed only against <span class="elsevierStyleItalic">Candida glabrata</span>&#46;</p></span> <span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Conclusions</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">It is likely that the antifungal activity of the AF against <span class="elsevierStyleItalic">C&#46; albicans</span>&#44; <span class="elsevierStyleItalic">C&#46; glabrata</span> and <span class="elsevierStyleItalic">Candida parapsilosis</span> observed <span class="elsevierStyleItalic">in vitro</span> also exists <span class="elsevierStyleItalic">in vivo</span>&#44; contributing to protect against intrauterine fungal infections&#46;</p></span>"
        "secciones" => array:5 [
          0 => array:2 [
            "identificador" => "abst0005"
            "titulo" => "Background"
          ]
          1 => array:2 [
            "identificador" => "abst0010"
            "titulo" => "Aims"
          ]
          2 => array:2 [
            "identificador" => "abst0015"
            "titulo" => "Methods"
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          3 => array:2 [
            "identificador" => "abst0020"
            "titulo" => "Results"
          ]
          4 => array:2 [
            "identificador" => "abst0025"
            "titulo" => "Conclusions"
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      "es" => array:3 [
        "titulo" => "Resumen"
        "resumen" => "<span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Antecedentes</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Aunque <span class="elsevierStyleItalic">Candida</span> es un comensal del tracto urogenital&#44; las infecciones f&#250;ngicas intrauterinas son extremadamente poco frecuentes en la pr&#225;ctica cl&#237;nica&#46;</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Objetivos</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">En el presente trabajo evaluamos si el l&#237;quido amni&#243;tico posee actividad antif&#250;ngica directa contra aislamientos cl&#237;nicos de <span class="elsevierStyleItalic">Candida albicans</span> y otras especies del g&#233;nero <span class="elsevierStyleItalic">Candida</span>&#46;</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">M&#233;todos</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Se obtuvieron un total de 23 muestras de l&#237;quido amni&#243;tico de mujeres embarazadas con edad gestacional de 38 a 41 semanas en condiciones as&#233;pticas por aspiraci&#243;n del saco amni&#243;tico durante la ces&#225;rea&#46; Se inocularon diferentes especies de <span class="elsevierStyleItalic">Candida</span> en l&#237;quido amni&#243;tico y caldo Sabouraud&#44; que se us&#243; como control&#44; y se incubaron a 37<span class="elsevierStyleHsp" style=""></span>&#176;C durante 48<span class="elsevierStyleHsp" style=""></span>h&#46; Se realizaron cultivos cuantitativos de las muestras y controles a las 0&#44; 4&#44; 8&#44; 12&#44; 24 y 48<span class="elsevierStyleHsp" style=""></span>h&#46;</p></span> <span id="abst0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Resultados</span><p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">El l&#237;quido amni&#243;tico recogido de 23 mujeres embarazadas tuvo actividad inhibidora consistente y significativa contra todos los aislamientos de <span class="elsevierStyleItalic">Candida</span> probados&#46; No obstante&#44; la inhibici&#243;n completa del crecimiento con las 23 muestras de l&#237;quido amni&#243;tico analizadas se observ&#243; solo frente a <span class="elsevierStyleItalic">Candida glabrata</span>&#46;</p></span> <span id="abst0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Conclusiones</span><p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">Probablemente la actividad antif&#250;ngica del l&#237;quido amni&#243;tico observada <span class="elsevierStyleItalic">in vitro</span> contra <span class="elsevierStyleItalic">C&#46; albicans</span>&#44; <span class="elsevierStyleItalic">C&#46; glabrata</span> y <span class="elsevierStyleItalic">Candida parapsilosis</span> tambi&#233;n existe <span class="elsevierStyleItalic">in vivo</span>&#44; y contribuye a la protecci&#243;n de las infecciones f&#250;ngicas intrauterinas&#46;</p></span>"
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            "identificador" => "abst0040"
            "titulo" => "M&#233;todos"
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          3 => array:2 [
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            "titulo" => "Resultados"
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            "titulo" => "Conclusiones"
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          "en" => "<p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">Kinetics of growth of <span class="elsevierStyleItalic">Candida</span> clinical isolates in the presence of amniotic fluid <span class="elsevierStyleItalic">versus</span> Sabouraud broth &#40;control&#41;&#46; Each line represents the growth curve over time of a sole <span class="elsevierStyleItalic">Candida</span> isolate&#44; grown either in amniotic fluid or in Sabouraud broth &#40;control&#41;&#46; Each symbol represents the log10 CFU value at different time points&#46; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;0001&#59; Student&#39;s <span class="elsevierStyleItalic">t</span> test&#46;</p>"
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Age in years &#40;mean<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>SD&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">32&#46;6<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>5&#46;44&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">Ethnicity &#40;Greek&#47;immigrant&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">21&#47;2&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Gestational weeks &#40;mean<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>SD&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">39&#46;3<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;98&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">Previous pregnancies&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">42&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">Use of antibiotics&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t">0&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
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                  \t\t\t\t\ttop\n
                  \t\t\t\t">Use of antifungals&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">0&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Use of steroids&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">5&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t">Smoking&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t">1&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">Diabetes&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">2&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">Other comorbidities&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t">0&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">0&#46;064&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">0&#46;032&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">Posaconazole&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">0&#46;75&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t">0&#46;008&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
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                  \t\t\t\t">Caspofungin&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">0&#46;094&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">0&#46;125&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">Micafungin&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="\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t  " align="char" valign="\n
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                      "titulo" => "The prevalence and clinical significance of intraamniotic infection with <span class="elsevierStyleItalic">Candida</span> species in women with preterm labor"
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                    0 => array:2 [
                      "doi" => "10.1007/BF02718273"
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                      "doi" => "10.1155/2014/615958"
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                        "paginaInicial" => "615958"
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                      "titulo" => "Antimicrobial peptides in amniotic fluid&#58; defensins&#44; calprotectin and bacterial&#47;permeability-increasing protein in patients with microbial invasion of the amniotic cavity&#44; intra-amniotic inflammation&#44; preterm labor and premature rupture of membranes"
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                            3 => "S&#46; Edwin"
                            4 => "C&#46; Rathnasabapathy"
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                        "paginaInicial" => "2"
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                        "paginaInicial" => "11"
                        "paginaFinal" => "17"
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ISSN: 11301406
Original language: English
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