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CLINICAL SCIENCES
DIGESTIVE TRACT MICROBIOTA IN HEALTHY VOLUNTEERS
Bruno Zilberstein, Alina G Quintanilha, Manoel A A Santos, Denis Pajecki, Eduardo G Moura, Paulo Roberto Arruda Alves, Fauze Maluf Filho, João Ary Ubriaco de Souza, Joaquim Gama-Rodrigues
Digestive Surgery Division, São Paulo University Medical School – São Paulo/SP, Brazil.
Department of Gastroenterology, São Paulo University Medical School – São Paulo/SP, Brazil.
Institute of Biomedical Sciences, Department of Microbiology, São Paulo University Medical School – São Paulo/SP, Brazil.
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="cesec10" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle120">INTRODUCTION</span><p id="para10" class="elsevierStylePara elsevierViewall">Interest in the microbiologic composition of the normal digestive tract began in the 19th century with Pasteur&#44; who believed that a symbiotic relationship between man and bacteria was essential to life&#46; However&#44; at the beginning of the 20<span class="elsevierStyleSup">th</span> century&#44; several authors including Metchnikoff et al<a class="elsevierStyleCrossRef" href="#bib1"><span class="elsevierStyleSup">1</span></a> believed that microbiota competed with the host organism for nutrients&#46; The development of experimental models to study the relationship between microbiota and the human organism in totally germ-free laboratory animals demonstrated the role of the normal microflora in vitamin synthesis&#44; metabolism of nitrogen compounds and lipids&#44; and especially their participation as a barrier against the invasion of pathogenic microorganisms&#46;<a class="elsevierStyleCrossRefs" href="#bib2"><span class="elsevierStyleSup">2&#8211;4</span></a> In 1964&#44; Donaldson<a class="elsevierStyleCrossRef" href="#bib5"><span class="elsevierStyleSup">5</span></a> standardized the quantitative analysis of bacteria in the feces of healthy volunteers&#44; and in 1966&#44; Kalser<a class="elsevierStyleCrossRef" href="#bib6"><span class="elsevierStyleSup">6</span></a> described an aspiration sampling technique for studying the microbiota of the jejunum and ileum&#46; There have been few advances in collection methods since then&#59; however&#44; there have been some improvements in cultivation techniques and the use of genetic probes for identification of the microorganism&#46;<a class="elsevierStyleCrossRef" href="#bib7"><span class="elsevierStyleSup">7</span></a></p><p id="para20" class="elsevierStylePara elsevierViewall">Over the last 20 years&#44; there has been an increased interest in the study of the microbiota and their role in diseases of the digestive system including neoplasias&#44;<a class="elsevierStyleCrossRefs" href="#bib8"><span class="elsevierStyleSup">8&#44;9</span></a> intestinal inflammatory disease&#44;<a class="elsevierStyleCrossRefs" href="#bib10"><span class="elsevierStyleSup">10&#44;11</span></a> diarrhea associated with antibiotic use&#44;<a class="elsevierStyleCrossRefs" href="#bib12"><span class="elsevierStyleSup">12&#8211;14</span></a> and bacterial translocation&#46;<a class="elsevierStyleCrossRefs" href="#bib15"><span class="elsevierStyleSup">15&#44;16</span></a> However&#44; one of the difficulties in performing conclusive repeatable studies has always been the lack of a standard collection method that can be used to establish a uniform control group of healthy individuals against which the different diseases could be compared&#46;</p><p id="para30" class="elsevierStylePara elsevierViewall">This shortcoming becomes even more important when there is the intention to study the eventual modification of the normal microbiota caused by or as a consequence of digestive diseases&#46;<a class="elsevierStyleCrossRefs" href="#bib11"><span class="elsevierStyleSup">11&#44;17</span></a></p><p id="para40" class="elsevierStylePara elsevierViewall">The aim of this study was to standardize collecting sample methods from the different segments of the digestive tract in healthy volunteers in order to better characterize their microbiota&#46;</p></span><span id="cesec20" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle130">PATIENTS AND METHODS</span><p id="para50" class="elsevierStylePara elsevierViewall">A multidisciplinary prospective investigation was developed involving the Digestive Surgery Division and the Gastrointestinal Endoscopy Unit of the S&#227;o Paulo University Medical School&#44; and the Institute of Biomedical Sciences of the University of S&#227;o Paulo&#46;</p><p id="para60" class="elsevierStylePara elsevierViewall">The study was approved by the Ethic Committees and informed consent was obtained from all volunteers&#46;</p><p id="para70" class="elsevierStylePara elsevierViewall">The different segments of the digestive tract were studied in separate groups of healthy volunteers&#46; Sample collection methods were specifically developed for each segment&#46; Healthy individuals were selected based on the following exclusion criteria&#58; use of antibiotics and&#47;or anti-inflammatory drugs in the preceding 90 days&#44; dental prostheses&#44; smoking&#44; alcoholism&#44; diabetes&#44; presence of malignant tumors&#44; scleroderma&#44; previous surgical procedures on the digestive tract&#44; or any other problem that could affect the digestive tract&#44; the esophagus&#44; stomach&#44; intestines&#44; or specifically the mouth flora&#59; a dental caries index &#40;CPO &#8211; D&#41; greater than 2&#46;6<span class="elsevierStyleSup">18</span> was also was also an exclusion criterion&#46;</p><p id="para80" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">Standardized collection method from the mouth&#46;</span> Ten healthy individuals were prospectively studied&#44; including 5 men and 5 women&#44; with a mean age of 33&#46;3 years&#46; Samples for microbiological study were collected from saliva&#44; the back of the tongue&#44; and supragingival and subgingival bacterial biofilm&#46; A sterile Petri dish was used for saliva collection after stimulation by masticatory mouth movements&#46; From the back of the tongue&#44; a sterile cotton swab was used with a front-to-back movement&#46; The supragingival bacterial biofilm was collected from the vestibular face of the first lower left molar and from the subgingival vestibular face of the contralateral first molar with a periodontal &#40;Gracey&#41; curette &#40;<a class="elsevierStyleCrossRef" href="#fig1">Figure 1</a>&#41;&#46; The collected materials were placed in a test tube containing phosphate-buffered saline for immediate transport&#46;</p><elsevierMultimedia ident="fig1"></elsevierMultimedia><p id="para90" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">Standardized collection method from the esophagus&#46;</span> Ten individuals were prospectively studied&#44; including 6 women and 4 men&#44; with a mean age of 43&#46;4 years&#46; Volunteers were selected among those who were going to undergo an upper digestive tract endoscopy&#46; After local mouth anesthetic with 10&#37; lidocaine spray and intravenous sedation with diazepam &#40;3-5 mg&#41;&#44; a n&#176;14&#40;Fr&#41; Levine catheter was introduced with extreme care into the mouth through an n&#176;7&#46;5 or 29 Fr orotracheal tube&#46; The catheter was pushed forward to touch the esophagus lumen&#44; where 10 mL of saline was injected using a 20 mL syringe connected to its proximal end&#59; aspiration was then performed&#46; The collected material was transported in a phosphate buffer saline solution &#40;1 mL&#47;9 mL&#41; to the microbiology laboratory within 1 hour &#40;<a class="elsevierStyleCrossRef" href="#fig2">Figure 2</a>&#41;&#46; Upper digestive endoscopy was then immediately performed to identify any abnormality of the upper digestive tract&#46;</p><elsevierMultimedia ident="fig2"></elsevierMultimedia><p id="para100" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">Standardized collection method from the stomach&#44; duodenum&#44; jejunum&#44; and proximal ileum&#46;</span> This was performed in 20 other volunteers&#58; 8 men and 12 women with a mean age of 42 years&#46; All individuals presented normal upper digestive tract endoscopies&#46; A flexible silicone sampling probe was used with a small &#40;3 mm&#41; distal opening and with a lead weight bound in its extremity&#46;<a class="elsevierStyleCrossRefs" href="#bib19"><span class="elsevierStyleSup">19&#8211;23</span></a> This probe was introduced by mouth and swallowed until it reached the stomach&#44; being located by radioscopy&#46; The first sample was collected&#44; aspirating 1 mL of mucus with a 20 mL syringe connected to its proximal end&#46; The probe was allowed to migrate by peristaltic movement to the more distal segments and was periodically monitored by radioscopy &#40;<a class="elsevierStyleCrossRef" href="#fig3">Figure 3</a>&#41;&#46; The same probe was used for collection of material in each intestinal segment&#46; The evaluation of the exact site from which the mucus was obtained was determined by the length of the probe introduced and its location through radioscopy&#46; To avoid contamination and eventual false results&#44; the probe was washed out several times&#44; and the contents were discarded before the actual collection of mucus&#46; A series of 1-mL samples was taken from the duodenum&#44; proximal jejunum&#44; distal jejunum&#44; and proximal ileum&#46; The samples were placed into the test tubes with 9 mL of phosphate buffer saline solution and taken to the microbiology laboratory within the first hour&#46;</p><elsevierMultimedia ident="fig3"></elsevierMultimedia><p id="para110" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">Standardized collection method from distal ileum&#44; colon&#44; and rectum&#46;</span> This method was performed in another 24 volunteers&#44; 10 men and 14 women&#44; with a mean age of 53 years&#44; through colonoscopy after previous colon preparation with a 10&#37; mannitol solution until the stool was liquid&#44; clear&#44; and free of residues&#46;<a class="elsevierStyleCrossRef" href="#bib24"><span class="elsevierStyleSup">24</span></a> Colonoscopy was performed at least 5 hours after the colonic preparation to avoid interference in the determination of the microbiologic contents of the colonic mucus&#46;<a class="elsevierStyleCrossRef" href="#bib25"><span class="elsevierStyleSup">25</span></a> Colonoscopy was performed after sedation with diazepam &#40;to 10 mg&#41; and meperidine &#40;to 100 mg&#41;&#46; The colonoscope was introduced into the distal ileum&#44; checking the integrity of the lower digestive tract &#40;distal ileum&#59; cecum&#59; ascending&#44; transverse&#44; descending&#44; and sigmoid colon&#59; and rectum&#41;&#46; A proper catheter&#44; especially developed for this purpose&#44; was used to pass through the working channel of the colonoscope to collect the samples of mucus from the different segments of the lower digestive tract&#46; This catheter&#44; obtained from a polyethylene probe&#44; was especially designed&#44; being 2&#46;20 m long and 8 Fr in diameter&#59; it was internally coated with silicone &#40;<a class="elsevierStyleCrossRef" href="#fig4">Figure 4</a>&#41;&#46; The distal end of the catheter was covered by a protective membrane&#59; this was ruptured at the time of collection by inflation with air&#46; Sample volume was always 0&#46;1 mL&#44; determined by step marks on the distal end of the catheter<a class="elsevierStyleCrossRefs" href="#bib5"><span class="elsevierStyleSup">5&#44;2&#44;25&#8211;27</span></a> that could be visualized by the colonoscope&#46; A fresh sterile catheter was used at each site of the lower digestive tract for collecting the samples&#46; After collection&#44; the samples were taken to the microbiological laboratory in a sterile Eppendorf tube containing 0&#46;9 mL of VMGA III &#40;viability-maintaining transport medium&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib28"><span class="elsevierStyleSup">28</span></a></p><elsevierMultimedia ident="fig4"></elsevierMultimedia><span id="cesec30" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle140">Culture media</span><p id="para120" class="elsevierStylePara elsevierViewall">The collected materials from all segments were placed in selective culture media for aerobic and anaerobic microorganisms and yeasts&#46;<a class="elsevierStyleCrossRef" href="#bib29"><span class="elsevierStyleSup">29</span></a> The following culture media were used&#58; Sabouraud agar &#42;&#44; MacConkey agar&#42;&#42;-blood&#44; <span class="elsevierStyleItalic">Enterococcus-</span>selective agar&#42;&#42;&#44; reinforced <span class="elsevierStyleItalic">Clostridium</span> medium&#42;&#42;&#59; Phenylethylalcohol agar&#42;&#44; <span class="elsevierStyleItalic">Veillonella</span> medium&#42;&#44; Brain-Heart infusion &#40;BHI&#41; agar&#42; &#43; vitamin K &#43; hemin &#43; streptomycin&#44; Chapman-Stone medium&#42;&#42;&#44; <span class="elsevierStyleItalic">Bacteroides fragilis</span> bile-esculin agar medium &#40;BBE&#41; &#42;&#44; <span class="elsevierStyleItalic">Bifidobacterium</span> medium&#44; <span class="elsevierStyleItalic">Propionibacterium</span> medium&#42;&#44; BHI&#42; &#43; extract of yeast&#44; Blood-trypticase soy agar &#40;TSA&#41; &#42; &#43; vitamin K &#43; hemin &#40;&#42;DIFCO&#46; St&#46; Louis&#44; MO&#44; USA&#59; &#42;&#42;MERCK DIAGNOSTICA&#44; RJ&#44; Brazil&#41;&#46;</p></span><span id="cesec40" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle150">Statistical analysis</span><p id="para130" class="elsevierStylePara elsevierViewall">Descriptive analysis of findings from the mouth&#44; esophagus&#44; and upper digestive tract was done&#46; The chi square &#40;X<span class="elsevierStyleSup">2</span>&#41; test was used to verify the difference in distribution of each bacterial species in the various regions of the lower digestive tract&#46; The expected frequency of each bacterial species in different regions of the lower digestive tract was calculated using nonparametric tests&#46;<a class="elsevierStyleCrossRef" href="#bib30"><span class="elsevierStyleSup">30</span></a></p><p id="para140" class="elsevierStylePara elsevierViewall">The results of the concentration of microorganisms were expressed in units of colony formation&#47;mL &#40;ucf&#41; expressed in logarithm base 10 &#40;log<span class="elsevierStyleInf">10</span>&#41;&#46; Significance was assigned to a <span class="elsevierStyleItalic">P</span> value of &#60; 0&#46;05&#46;</p></span></span><span id="cesec50" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle160">RESULTS</span><p id="para150" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">Mouth microbiota&#46;</span><a class="elsevierStyleCrossRef" href="#tbl1">Table 1</a> shows the frequency and locations of microorganisms found in the mouth&#46; Mixed microbiota were identified here&#44; with as predominance of Gram-positive aerobic and anaerobic cocci</p><elsevierMultimedia ident="tbl1"></elsevierMultimedia><p id="para160" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">Esophagus microbiota&#46;</span><a class="elsevierStyleCrossRef" href="#tbl2">Table 2</a> shows the frequency and average concentration of microorganisms found in the esophagus&#46; It can be seen that in this segment the flora is transitional&#46;</p><elsevierMultimedia ident="tbl2"></elsevierMultimedia><p id="para170" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">Stomach&#44; duodenum&#44; jejunum&#44; and proximal ileum microbiota&#46;</span><a class="elsevierStyleCrossRef" href="#tbl3">Table 3</a> shows the mean concentrations and prevalence of the different microorganisms found in each segment of the upper digestive tract&#46; <span class="elsevierStyleItalic">Veillonella</span> sp&#44; <span class="elsevierStyleItalic">Lactobacillus</span> sp&#44; and <span class="elsevierStyleItalic">Clostridium</span> sp are predominant in the stomach and duodenum&#59; while <span class="elsevierStyleItalic">Bacteroides</span> sp&#44; <span class="elsevierStyleItalic">Proteus</span> sp&#44; and <span class="elsevierStyleItalic">Staphylococcus</span> sp&#44; in addition to <span class="elsevierStyleItalic">Veillonella</span> sp are predominant in the jejunum and upper ileum&#59;</p><elsevierMultimedia ident="tbl3"></elsevierMultimedia><p id="para180" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleBold">Distal ileum&#44; colon&#44; and rectum microbiota&#46;</span><a class="elsevierStyleCrossRef" href="#tbl4">Table 4</a> shows the different microorganisms found in each segment&#46; The most distinctive feature here is the presence of &#8220;nonpathogenic&#8221; anaerobic bacteria <span class="elsevierStyleItalic">Veillonella</span> sp &#40;average 10<span class="elsevierStyleSup">5</span> UFC&#41;</p><elsevierMultimedia ident="tbl4"></elsevierMultimedia><p id="para190" class="elsevierStylePara elsevierViewall"><a class="elsevierStyleCrossRef" href="#tbl5">Table 5</a> shows the association between microorganisms and sites of the lower digestive tract&#46;</p><elsevierMultimedia ident="tbl5"></elsevierMultimedia></span><span id="cesec60" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle170">DISCUSSION</span><p id="para200" class="elsevierStylePara elsevierViewall">The complex interactions between the different microorganisms or between them and healthy hosts or their interaction in digestive diseases are poorly understood&#46; The study of the microbiota in humans starts with the need for standardizing sample collection methods from the different segments of the digestive tract&#44; including availability of different technical resources and ethical issues&#46; This base is necessary when we intend to compare different studies&#46;</p><p id="para210" class="elsevierStylePara elsevierViewall">This investigation describes the sample collection methods from different segments of the digestive tract&#46; This methodology is characterized by the following characteristics&#58; &#40;i&#41; it is innocuous for patients&#59; &#40;ii&#41; it allows material to be collected from restricted sites&#44; avoiding contamination&#59; &#40;iii&#41; it uses available materials with accessible prices&#44; and &#40;iv&#41; it is easily reproducible&#46;</p><p id="para220" class="elsevierStylePara elsevierViewall">Material sampling from the mouth<a class="elsevierStyleCrossRefs" href="#bib18"><span class="elsevierStyleSup">18&#44;31&#44;32</span></a> and esophagus<a class="elsevierStyleCrossRef" href="#bib33"><span class="elsevierStyleSup">33</span></a> was done by modifying previously validated methods already described in the literature&#46; For the stomach&#44; duodenum&#44; jejunum &#40;proximal and distal&#41;&#44; and proximal ileum&#44; similar methods were used&#46;<a class="elsevierStyleCrossRefs" href="#bib19"><span class="elsevierStyleSup">19&#8211;22</span></a> Finally&#44; samples from the distal ileum&#44; colon&#44; and rectum were collected using a new method developed by the authors&#46;<a class="elsevierStyleCrossRef" href="#bib28"><span class="elsevierStyleSup">28</span></a></p><p id="para230" class="elsevierStylePara elsevierViewall">The oral cavity presented very diverse microbiota due to the different anatomical sites and constant exposure to the external environment&#46; The method of collecting saliva without using chewing gum or paraffin tablets gave better results than in previous studies&#44;<a class="elsevierStyleCrossRefs" href="#bib34"><span class="elsevierStyleSup">34&#8211;38</span></a> suggesting that the technique used in this study is more sensitive and causes fewer alterations to indigenous flora&#46; Results from the back of the tongue were similar to those of other studies&#46;<a class="elsevierStyleCrossRefs" href="#bib35"><span class="elsevierStyleSup">35&#8211;38</span></a></p><p id="para240" class="elsevierStylePara elsevierViewall">Periodontal Gracey curettes were preffered for sampling from the supra- and subgingival biofilm&#46; Our results were similar to those reported in the literature&#44;<a class="elsevierStyleCrossRefs" href="#bib32"><span class="elsevierStyleSup">32&#44;38&#44;39</span></a> validating this method&#46;</p><p id="para250" class="elsevierStylePara elsevierViewall">From a microbiological point of view&#44; the esophagus has always been considered to be a saliva secretion passageway with transitory microbiota similar to the mouth and of little interest in research&#46; However&#44; when alimentary stasis occurs&#44; as in neoplasia or achalasia&#44;<a class="elsevierStyleCrossRefs" href="#bib40"><span class="elsevierStyleSup">40&#44;41</span></a> there is an excessive increase in bacterial growth&#44; with the risk of serious infections after surgery or endoscopy&#46;<a class="elsevierStyleCrossRefs" href="#bib42"><span class="elsevierStyleSup">42&#44;43</span></a></p><p id="para260" class="elsevierStylePara elsevierViewall">Sample collection for studying the microbiota of the esophagus cannot be performed with catheters that pass through the mouth because of the risk of contamination during their insertion&#46; The use of sterile catheters that pass through the working channel of an endoscope is expensive and does not permit aspiration of sufficient thick material from an esophagus with stasis&#46;</p><p id="para270" class="elsevierStylePara elsevierViewall">Gagliardi et al<a class="elsevierStyleCrossRef" href="#bib33"><span class="elsevierStyleSup">33</span></a> developed a similar collection method to that used in our study&#46; However&#44; by taking the samples before endoscopic examination&#44; we avoided possible contamination during the introduction or removal of the endoscopic device&#46; This small technical modification enabled us to obtain fewer positive cultures &#40;40&#37; vs 66&#37;&#41; with similar strains of bacteria&#44; with predominantly Gram positive aerobes and without Gram negative aerobes&#44; as described by Gagliardi in 13&#37; of cases&#46;</p><p id="para280" class="elsevierStylePara elsevierViewall">The samples obtained from the stomach for microbiological study presented no problems because of the ease of access&#44; and because gastric pH is responsible for the destruction of most swallowed bacteria&#44; all of which facilitates the isolation of the appropriate microorganisms&#46;<a class="elsevierStyleCrossRef" href="#bib19"><span class="elsevierStyleSup">19</span></a></p><p id="para290" class="elsevierStylePara elsevierViewall">In the stomach&#44; there was a predominance of <span class="elsevierStyleItalic">Lactobacillus</span> sp&#44; <span class="elsevierStyleItalic">Veillonella</span> sp&#44; and <span class="elsevierStyleItalic">Clostridium</span> sp&#44; which are all resistant to the acid environment&#44; demonstrating potential residual microflora that could develop down to the lower regions of the digestive tract&#46;</p><p id="para300" class="elsevierStylePara elsevierViewall">Other species such as <span class="elsevierStyleItalic">Escherichia coli&#44; Peptococcus</span> sp&#44; <span class="elsevierStyleItalic">Klebisiella</span> sp&#44; <span class="elsevierStyleItalic">Bacteroides</span> sp &#40;npg&#41; start an ascending curve of growth or &#8220;re-population&#8221; of the lower sites of the digestive tract&#44; being dormant in the stomach because of the acidic environment&#46;</p><p id="para310" class="elsevierStylePara elsevierViewall">Sample collection from small intestine segments is technically more difficult because of difficulties relating to access and to the standardization of specific locations&#46; Nevertheless&#44; it is of major interest because of the range of diseases associated with alterations in its microbiota&#46;<a class="elsevierStyleCrossRefs" href="#bib44"><span class="elsevierStyleSup">44&#44;45</span></a></p><p id="para320" class="elsevierStylePara elsevierViewall">Shiner<a class="elsevierStyleCrossRef" href="#bib46"><span class="elsevierStyleSup">46</span></a> developed a stainless steel capsule that only opens at collection time to aspirate the contents of the jejunum&#59; this avoids contamination during its passage&#44; but it is very complex to use&#46; Kalser et al<a class="elsevierStyleCrossRef" href="#bib6"><span class="elsevierStyleSup">6</span></a> developed a double lumen polyvinyl catheter with a mercury weight on the distal end for taking samples starting 75 cm from Treitz&#8217;s ligament to near the distal ileum and cecal valve&#46; However&#44; there was no mechanism to protect from contamination&#46; Their results were very similar to those of Shiner&#46;<a class="elsevierStyleCrossRef" href="#bib46"><span class="elsevierStyleSup">46</span></a></p><p id="para330" class="elsevierStylePara elsevierViewall">This method was tested in our midst by Machado et al&#44;<a class="elsevierStyleCrossRef" href="#bib19"><span class="elsevierStyleSup">19</span></a> who collected samples of the jejunum liquid in patients suffering from Chagasic achalasia&#46; It was also used by Quintanilha et al<a class="elsevierStyleCrossRefs" href="#bib20"><span class="elsevierStyleSup">20&#44;21</span></a> for qualitative evaluation of microbiota alterations in the proximal jejunum of patients with Chagasic megacolon&#44; both before and after surgery&#46;</p><p id="para340" class="elsevierStylePara elsevierViewall">A similar method has been used by different authors in the study of bacterial translocation in critical patients&#46; Belov et al<a class="elsevierStyleCrossRef" href="#bib47"><span class="elsevierStyleSup">47</span></a> evaluated sepsis mediators &#40;TNF and IL-1&#41; using jejunal aspiration in septic shock patients&#46; Pardo et al<a class="elsevierStyleCrossRef" href="#bib16"><span class="elsevierStyleSup">16</span></a> demonstrated a reduction in bacterial overgrowth and translocation in cirrhotic patients using cisapride&#46; Bernhardt et al<a class="elsevierStyleCrossRef" href="#bib48"><span class="elsevierStyleSup">48</span></a> studied <span class="elsevierStyleItalic">Candida</span> sp colonization in digestive tracts of critical patients under long-term antibiotic treatment&#46;</p><p id="para350" class="elsevierStylePara elsevierViewall">In this study&#44; the method of collecting mucus from the upper digestive tract was used to evaluate healthy volunteers with the aim of establishing a normal pattern that could serve as a control in studies of microbiotic changes in disease states&#46; Even though the sample group was small&#44; we obtained similar results to those described by Kalser<a class="elsevierStyleCrossRef" href="#bib6"><span class="elsevierStyleSup">6</span></a> and Shiner&#46;<a class="elsevierStyleCrossRef" href="#bib46"><span class="elsevierStyleSup">46</span></a></p><p id="para360" class="elsevierStylePara elsevierViewall">It must be said that sample collection from the jejunum and proximal ileum is an uncomfortable procedure for the patient&#46; Therefore&#44; recruiting healthy volunteers is not easy&#59; this makes it difficult for researchers to recruit control groups for their studies&#46;</p><p id="para370" class="elsevierStylePara elsevierViewall">The study of lower digestive tract microbiota is a major challenge because of the high concentration and variety of microorganisms pertaining to the indigenous and transitory microbiota&#46;<a class="elsevierStyleCrossRef" href="#bib49"><span class="elsevierStyleSup">49</span></a> In early trials in which researchers attempted to study the microbiology of dregs&#44;<a class="elsevierStyleCrossRefs" href="#bib4"><span class="elsevierStyleSup">4&#44;5</span></a> they were unable to differentiate indigenous from transitory microbiota or determine the different levels of bacteria in the different segments of the lower digestive tract&#46; Studies that have employed sample collection during laparotomy<a class="elsevierStyleCrossRef" href="#bib50"><span class="elsevierStyleSup">50</span></a> have not respected the physiological conditions of the patient&#44; because the quantitative study was prejudiced due to dilution of mucus during collection&#46;</p><p id="para380" class="elsevierStylePara elsevierViewall">The need for more precise and reliable methods motivated us to develop a special catheter to collect adequate volume of undiluted mucus from specific regions of the lower digestive tract during colonoscopy using an aseptic technique&#46; This is an efficient method as shown by the large variety of aerobic&#44; anaerobic&#44; microaerophile&#44; and facultative microorganisms&#44; and yeasts obtained&#46; The results show a stable increase in anaerobic microorganisms &#40;<span class="elsevierStyleItalic">Veillonella</span> sp&#44; <span class="elsevierStyleItalic">Peptococcus</span> sp&#44; and <span class="elsevierStyleItalic">Fusobacterium</span> sp&#41; with the capacity to digest amino acids but with little ability to ferment carbohydrates&#46; These and other similar microorganisms comprise a distinct metabolism group in the large intestine&#46;<a class="elsevierStyleCrossRef" href="#bib4"><span class="elsevierStyleSup">4</span></a></p><p id="para390" class="elsevierStylePara elsevierViewall">There was also the constant presence of other bacteria with average concentrations of 10<span class="elsevierStyleSup">5</span> such as <span class="elsevierStyleItalic">Clostridium</span> sp &#40;gel-&#41; <span class="elsevierStyleItalic">Corynebacterium</span> sp&#44; <span class="elsevierStyleItalic">E&#46; coli&#44; Enterobacter</span> sp&#44; <span class="elsevierStyleItalic">Klebisiella</span> sp&#44; <span class="elsevierStyleItalic">Lactobacillus</span> sp&#44; <span class="elsevierStyleItalic">Propionibacterium</span> sp&#44; <span class="elsevierStyleItalic">Proteus</span> sp&#44; and <span class="elsevierStyleItalic">Veillonella</span> sp&#59; there were others at lower concentrations&#46;</p><p id="para400" class="elsevierStylePara elsevierViewall">Bacterial types were characterized colonizing restricted areas of the lower digestive tract with average concentrations of 10<span class="elsevierStyleSup">5</span> &#40;<a class="elsevierStyleCrossRef" href="#tbl5">Table 5</a>&#41;&#59; the following could be interpreted as &#8220;biological markers&#8221; of health&#58; <span class="elsevierStyleItalic">Fusobacterium</span> sp in the rectum&#59; <span class="elsevierStyleItalic">Peptococcus</span> sp in the sigmoid&#59; and <span class="elsevierStyleItalic">Enterococcos</span> sp in the transverse colon&#46; <span class="elsevierStyleItalic">Bacteroides</span> sp tend to reside in the more proximal regions&#44; gradually decreasing in prevalence in the sigmoid and rectum&#46;</p></span><span id="cesec70" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle180">CONCLUSION</span><p id="para410" class="elsevierStylePara elsevierViewall">The presented sampling collection methods are safe and efficient for obtaining suitable samples of mucus for qualitative and quantitative microbiologic studies&#44; revealing an environment of low oxidation-reduction &#40;redox&#41; potential&#46;</p><p id="para420" class="elsevierStylePara elsevierViewall">These results open the possibility for many other studies in this area&#44; using low-risk and highly reliable methodology&#44; to define the role of microbiota in the other gastrointestinal diseases as well as for standardization of future prophylactic treatment<a class="elsevierStyleCrossRefs" href="#bib50"><span class="elsevierStyleSup">50&#44;51</span></a> in gastroenterology&#46;</p></span><span id="cesec80" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle190">ACKNOWLEDGMENTS</span><p id="para430" class="elsevierStylePara elsevierViewall">The authors thank Ulysses Ribeiro Junior for his helpful suggestions&#46;</p><p id="para440" class="elsevierStylePara elsevierViewall">This study was supported by financial aid of FAPESP &#40;Funda&#231;&#227;o de Amparo &#224; Pesquisa do Estado de S&#227;o Paulo&#41;&#46;</p></span><span id="cesec90" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle200">ERRATA</span><p id="para450" class="elsevierStylePara elsevierViewall">CLINICS 2007&#59;62&#40;1&#41;&#58;47-54</p><p id="para460" class="elsevierStylePara elsevierViewall">Page 52&#44; 1&#176; Column&#44; Line 22</p><p id="para470" class="elsevierStylePara elsevierViewall">Replace&#58; Quintanilha et al<a class="elsevierStyleCrossRefs" href="#bib20"><span class="elsevierStyleSup">20&#44;21</span></a> for Quintanilha et al<a class="elsevierStyleCrossRefs" href="#bib21"><span class="elsevierStyleSup">21&#8211;22</span></a></p><p id="para480" class="elsevierStylePara elsevierViewall">Page 52&#44; Tables 4 e 5</p><p id="para490" class="elsevierStylePara elsevierViewall"><elsevierMultimedia ident="tbl4"></elsevierMultimedia><elsevierMultimedia ident="tbl5"></elsevierMultimedia></p></span></span>"
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            0 => "Bacteria Anaerobic"
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        "resumen" => "<span id="ceabs10" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle10">PURPOSE&#58;</span><p id="spara110" class="elsevierStyleSimplePara elsevierViewall">The aim of this study was to standardize the methods of sample collection of mucus from the digestive tract and to determine the microbiota in healthy volunteers from Brazil&#44; collecting samples from the mouth&#44; esophagus&#44; stomach&#44; duodenum&#44; jejunum&#44; ileum&#44; colon&#44; and rectum&#46;</p></span> <span id="ceabs20" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle20">METHODS&#58;</span><p id="spara120" class="elsevierStyleSimplePara elsevierViewall">Microbiota of selected healthy volunteers from the oral cavity &#40;n&#61;10&#41;&#44; the esophagus &#40;n&#61;10&#41;&#44; the upper digestive tract &#40;n&#61;20&#41;&#44; and the lower digestive tract &#40;n&#61;24&#41; were evaluated through distinct collection methods&#46; Collection methods took into account the different sites&#44; using basic scraping and swabbing techniques&#44; stimulated saliva from the oral cavity&#44; irrigation-aspiration with sterile catheters especially designed for the esophagus&#44; a probe especially designed for upper digestive tract&#44; and a special catheter for the lower digestive tract&#46;</p></span> <span id="ceabs30" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle30">RESULTS&#58;</span><p id="spara130" class="elsevierStyleSimplePara elsevierViewall">&#40;i&#41; Mixed microbiota were identified in the oral cavity&#44; predominantly Gram-positive aerobic and anaerobic cocci&#59; &#40;ii&#41; transitional flora mainly in the esophagus&#59; &#40;iii&#41; <span class="elsevierStyleItalic">Veillonella</span> sp&#44; <span class="elsevierStyleItalic">Lactobacillus</span> sp&#44; and <span class="elsevierStyleItalic">Clostridium</span> sp in the stomach and duodenum&#59; &#40;iv&#41; in the jejunum and upper ileum&#44; we observed <span class="elsevierStyleItalic">Bacteroides</span> sp&#44; <span class="elsevierStyleItalic">Proteus</span> sp&#44; and <span class="elsevierStyleItalic">Staphylococcus</span> sp&#44; in addition to <span class="elsevierStyleItalic">Veillonella</span> sp&#59; &#40;v&#41; in the colon&#44; the presence of &#8220;nonpathogenic&#8221; anaerobic bacteria <span class="elsevierStyleItalic">Veillonella</span> sp &#40;average 10<span class="elsevierStyleSup">5</span> UFC&#41; indicates the existence of a low oxidation-reduction potential environment&#44; which suggests the possibility of adoption of these bacteria as biological markers of total digestive tract health&#46;</p></span> <span id="ceabs40" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle40">CONCLUSIONS&#58;</span><p id="spara140" class="elsevierStyleSimplePara elsevierViewall">The collection methods were efficient in obtaining adequate samples from each segment of the total digestive tract to reveal the normal microbiota&#46; These procedures are safe and easily reproducible for microbiological studies&#46;</p></span>"
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        "resumen" => "<span id="ceabs50" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle60">OBJETIVO&#58;</span><p id="spara150" class="elsevierStyleSimplePara elsevierViewall">Padronizar os m&#233;todos de coleta do muco do trato digestivo e determinar a microbiota&#44; em volunt&#225;rios saud&#225;veis no Brasil&#44; coletando amostras da boca&#44; es&#244;fago&#44; est&#244;mago&#44; duodeno&#44; jejunos e &#237;leo&#44; c&#243;lons e reto&#46;</p></span> <span id="ceabs60" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle70">M&#201;TODOS&#58;</span><p id="spara160" class="elsevierStyleSimplePara elsevierViewall">A microbiota de volunt&#225;rios saud&#225;veis foi avaliada atrav&#233;s de diferentes m&#233;todos de coleta&#58; cavidade oral &#40;n&#61;10 volunt&#225;rios&#41;&#44; do es&#244;fago &#40;n&#61;10&#41;&#44; do trato digestivo alto &#40;n&#61;20&#41; e do trato digestivo baixo &#40;n&#61;24&#41;&#46; M&#233;todos de coleta foram adotados em cada s&#237;tio restrito&#44; usando derramar saliva&#44; t&#233;cnica de esfregar a mucosa e saliva estimulada da cavidade oral&#44; irriga&#231;&#227;o-aspira&#231;&#227;o&#44; cateteres espec&#237;ficos designados para o es&#244;fago&#44; sonda especial para o trato digestivo alto e cateteres especiais para o trato digestivo baixo&#46;</p></span> <span id="ceabs70" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle80">RESULTADOS&#58;</span><p id="spara170" class="elsevierStyleSimplePara elsevierViewall">Identificados&#58; &#40;i&#41; na cavidade oral&#44; microbiota mista&#44; predominando cocos aer&#243;bios e anaer&#243;bios Gram positivos&#59; &#40;ii&#41; no es&#244;fago&#44; flora transit&#243;ria&#59; &#40;iii&#41; no est&#244;mago e duodeno&#44; <span class="elsevierStyleItalic">Veillonella</span> sp&#44; <span class="elsevierStyleItalic">Lactobacillus</span> sp and <span class="elsevierStyleItalic">Clostridium</span> sp&#59; &#40;iv&#41; no jejuno e &#237;leo proximal&#44; <span class="elsevierStyleItalic">Bacter&#243;ides</span> sp&#44; <span class="elsevierStyleItalic">Proteus</span> sp and <span class="elsevierStyleItalic">Staphilococcus</span> sp&#44; al&#233;m da <span class="elsevierStyleItalic">Veillonella</span> sp&#59; &#40;v&#41; no colon&#44; foi revelada a presen&#231;a &#8220;n&#227;o patog&#234;nica&#8221; da bact&#233;ria anaer&#243;bica <span class="elsevierStyleItalic">Veillonella</span> sp numa concentra&#231;&#227;o m&#233;dia de 10<span class="elsevierStyleSup">5</span> unidades formadoras de col&#244;nia&#44; indicando um meio de baixo potencial de oxi-do-redu&#231;&#227;o e a possibilidade de se conceituar esta bact&#233;ria como um marcador biol&#243;gico do trato digestivo total em sadios&#46;</p></span> <span id="ceabs80" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="cestitle90">CONCLUS&#195;O&#58;</span><p id="spara180" class="elsevierStyleSimplePara elsevierViewall">Estes m&#233;todos de coleta foram considerados eficientes para obten&#231;&#227;o adequada de amostra em cada segmento do trato digestivo total para caracterizar a microbiota normal&#46; Estes procedimentos s&#227;o seguros e facilmente reprodut&#237;vel para estudo microbiol&#243;gico&#46;</p></span>"
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                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">40&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \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" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">Lactobacillus</span> sp&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">90&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">50&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">30&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \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" 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"><span class="elsevierStyleItalic">Neisseria</span> sp&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
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="center" valign="\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="left" valign="\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">Neisseria</span> sp&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\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  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">40&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \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" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">Peptostreptococcus</span> sp&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">50&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">20&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  " align="left" valign="\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">Propionibacterium</span> sp&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">20&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">30&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">60&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">30&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  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Staphylococcus</span> sp &#40;coag-&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">50&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">30&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="center" valign="\n
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                  \t\t\t\t">10&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="center" 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" 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"><span class="elsevierStyleItalic">Streptococcus</span> sp &#40;alpha- hemolytic&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">100&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">90&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">90&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">80&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  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Streptococcus</span> sp &#40;gamma- hemolytic&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">20&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" 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><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" 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" 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"><span class="elsevierStyleItalic">Veillonella</span> sp&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">100&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">60&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">80&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">70&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
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      5 => array:7 [
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                  <table border="0" frame="\n
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                  \t\t\t\t" scope="col">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col">Frequency &#40;&#37;&#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">Concentration &#40;ufc&#47;mL&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Staphylococcus</span> sp&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\ttop\n
                  \t\t\t\t">20&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
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                  \t\t\t\t">10<span class="elsevierStyleSup">2</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Corynebacterium</span> sp&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">10&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
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                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Lactobacillus</span> sp&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" 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><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">10<span class="elsevierStyleSup">2</span>&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
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                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Peptococcus</span> sp&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" 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><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">10<span class="elsevierStyleSup">1</span>&nbsp;\t\t\t\t\t\t\n
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          "leyenda" => "<p id="spara100" class="elsevierStyleSimplePara elsevierViewall">MC &#61; mean concentration &#40;UFC&#47;log<span class="elsevierStyleInf">10</span>&#41;&#59; &#37; &#61; prevalence&#59; sp &#61; species&#59; npg &#61; nonpigmented&#59; gel&#43; &#61; gelatinase positive&#59; gel- &#61; gelatinase negative&#59; npg &#61; nonpigmented&#59; coag- &#61; coagulase negative</p>"
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                0 => """
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                  \t\t\t\t" scope="col">Site&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " colspan="2" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col">STOMACH</th><th class="td" title="\n
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                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col">DUODENUM</th><th class="td" title="\n
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                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col">JEJUNUM</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " colspan="2" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col">ILEUM</th></tr><tr title="table-row"><th class="td" title="\n
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                  \t\t\t\t" scope="col">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t" scope="col">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t" scope="col">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " colspan="2" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col">Proximal</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " colspan="2" align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col">Distal</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " colspan="2" align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col">Proximal</th></tr><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">Microorganisms&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
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                  \t\t\t\t" scope="col">MC&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t" scope="col">&#37;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col">MC&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t" scope="col">&#37;&nbsp;\t\t\t\t\t\t\n
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                  \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">MC&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">&#37;&nbsp;\t\t\t\t\t\t\n
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                  \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">MC&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">&#37;&nbsp;\t\t\t\t\t\t\n
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                  \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">MC&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
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                  \t\t\t\t" scope="col">&#37;&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" 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"><span class="elsevierStyleItalic">Bacillus</span> sp&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">9&#46;1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t  " align="" valign="\n
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                  \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"><span class="elsevierStyleItalic">Bacteroides</span> sp&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t">&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">2&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">9&#46;1&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">3&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="center" valign="\n
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                  \t\t\t\t">9&#46;1&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="" valign="\n
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                  \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"><span class="elsevierStyleItalic">Bacteroides</span> sp &#40;npg&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\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\ttable-entry\n
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                  \t\t\t\t">16&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\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">9&#46;1&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">3&#46;5&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">36&#46;4&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">3&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">45&#46;5&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">3&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">9&#46;1&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">9&#46;1&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"><span class="elsevierStyleItalic">Candida</span> sp&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">3&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">18&#46;2&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">Clostridium ramosum</span>&nbsp;\t\t\t\t\t\t\n
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                  """
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">3&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">8&#46;3&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="" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&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="" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&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="" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&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="" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&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="" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&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="" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&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  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Veillonella sp</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="center" 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><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">90&#46;5&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">2&#46;5&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">83&#46;3&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="center" 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><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">70&#46;8&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="center" 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><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">62&#46;5&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="center" 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><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">75&#46;0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" 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><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">95&#46;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="center" 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><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">90&#46;0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
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          "en" => "<p id="spara190" class="elsevierStyleSimplePara elsevierViewall">Mean Concentration and Prevalence &#40;&#37;&#41; of Microorganisms in each Site of the LDT</p>"
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      8 => array:7 [
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          "leyenda" => "<p id="spara220" class="elsevierStyleSimplePara elsevierViewall">sp &#61; species&#44; &#42;<span class="elsevierStyleItalic">p</span> &#60; 0&#44;05 or &#60; 5&#37;</p>"
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            0 => array:1 [
              "tabla" => array:1 [
                0 => """
                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
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                  \t\t\t\t" scope="col">Microbiota&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
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                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col">Lower Digestive Tract site&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" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">Klebisiella</span> sp&#44; <span class="elsevierStyleItalic">Clostridium</span> sp &#40;gel-&#41;&#44; <span class="elsevierStyleItalic">Veillonella</span> sp&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="center" valign="\n
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                  \t\t\t\t">All sites&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"><span class="elsevierStyleItalic">Enterobacter</span> sp&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Sigmoid&#42;&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  " align="left" valign="\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">C&#226;ndida</span> sp&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="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Sigmoid and Rectum&#42;&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
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Enterococcus</span> sp e <span class="elsevierStyleItalic">Lactobacillus sp</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">Rectum&#42;&nbsp;\t\t\t\t\t\t\n
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                  """
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          "en" => "<p id="spara210" class="elsevierStyleSimplePara elsevierViewall">Association between microorganisms&#47;sites of the lower digestive tract</p>"
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      "titulo" => "REFERENCES"
      "seccion" => array:1 [
        0 => array:2 [
          "identificador" => "cebibsec10"
          "bibliografiaReferencia" => array:51 [
            0 => array:3 [
              "identificador" => "bib1"
              "etiqueta" => "1"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:1 [
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:1 [
                            0 => """
                              E Metchnikoff \n
                              \t\t\t\t\t\t\t\t
                              """
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "LibroEditado" => array:4 [
                        "titulo" => "Sur la Flore du corps humain"
                        "paginaInicial" => "1"
                        "paginaFinal" => "38"
                        "serieFecha" => "1901"
                      ]
                    ]
                  ]
                ]
              ]
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            1 => array:3 [
              "identificador" => "bib2"
              "etiqueta" => "2"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "The normal microbial flora"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:1 [
                            0 => """
                              PA Mackrowiak \n
                              \t\t\t\t\t\t\t\t
                              """
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1056/NEJM198207083070203"
                      "Revista" => array:6 [
                        "tituloSerie" => "N Engl J Med&#46;"
                        "fecha" => "1982"
                        "volumen" => "307"
                        "paginaInicial" => "83"
                        "paginaFinal" => "93"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/6806656"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            2 => array:3 [
              "identificador" => "bib3"
              "etiqueta" => "3"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Studies on the intestinal flora&#46; I&#46; the bacterial flora of the gastrointestinal tract in healthy and achlorhydric persons"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:3 [
                            0 => """
                              BS Drasar \n
                              \t\t\t\t\t\t\t\t
                              """
                            1 => """
                              M Shiner \n
                              \t\t\t\t\t\t\t\t
                              """
                            2 => """
                              GM McLeod \n
                              \t\t\t\t\t\t\t\t
                              """
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:6 [
                        "tituloSerie" => "Gastroenterology&#46;"
                        "fecha" => "1969"
                        "volumen" => "56"
                        "paginaInicial" => "71"
                        "paginaFinal" => "79"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/4885396"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            3 => array:3 [
              "identificador" => "bib4"
              "etiqueta" => "4"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Interactions between mechanisms controlling the Intestinal microflora"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:1 [
                            0 => """
                              R Freter \n
                              \t\t\t\t\t\t\t\t
                              """
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1093/ajcn/27.12.1409"
                      "Revista" => array:6 [
                        "tituloSerie" => "Am J Clin Nutr&#46;"
                        "fecha" => "1974"
                        "volumen" => "27"
                        "paginaInicial" => "1409"
                        "paginaFinal" => "1416"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/4611192"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            4 => array:3 [
              "identificador" => "bib5"
              "etiqueta" => "5"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Human colonic microbiota&#58; ecology&#44; physiology and metabolic potential of intestinal bacteria"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:2 [
                            0 => """
                              GT Macfarlane \n
                              \t\t\t\t\t\t\t\t
                              """
                            1 => """
                              S Macfarlane \n
                              \t\t\t\t\t\t\t\t
                              """
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:1 [
                      "Revista" => array:6 [
                        "tituloSerie" => "Scand J Gastroenterol&#46;"
                        "fecha" => "1997"
                        "volumen" => "222"
                        "numero" => "Suppl"
                        "paginaInicial" => "3"
                        "paginaFinal" => "9"
                      ]
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                ]
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            5 => array:3 [
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              "etiqueta" => "6"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Normal bacterial population of the intestine and their relation to intestinal function"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:1 [
                            0 => """
                              RM Donaldson Jr \n
                              \t\t\t\t\t\t\t\t
                              """
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1056/NEJM196404302701806"
                      "Revista" => array:6 [
                        "tituloSerie" => "N Engl J Med&#46;"
                        "fecha" => "1964"
                        "volumen" => "270"
                        "paginaInicial" => "938"
                        "paginaFinal" => "945"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/14114115"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            6 => array:3 [
              "identificador" => "bib7"
              "etiqueta" => "7"
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                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Normal viral and bacterial flora of the human small and large intestine"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => true
                          "autores" => array:6 [
                            0 => """
                              MH Kalser \n
                              \t\t\t\t\t\t\t\t
                              """
                            1 => """
                              R Cohen \n
                              \t\t\t\t\t\t\t\t
                              """
                            2 => """
                              I Arteaga \n
                              \t\t\t\t\t\t\t\t
                              """
                            3 => """
                              E Yawn \n
                              \t\t\t\t\t\t\t\t
                              """
                            4 => """
                              L Mayoral \n
                              \t\t\t\t\t\t\t\t
                              """
                            5 => """
                              W Hofeert \n
                              \t\t\t\t\t\t\t\t
                              """
                          ]
                        ]
                      ]
                    ]
                  ]
                  "host" => array:1 [
                    0 => array:2 [
                      "doi" => "10.1056/NEJM196603102741006"
                      "Revista" => array:6 [
                        "tituloSerie" => "N Engl J Med&#46;"
                        "fecha" => "1966"
                        "volumen" => "274"
                        "paginaInicial" => "558"
                        "paginaFinal" => "563"
                        "link" => array:1 [
                          0 => array:2 [
                            "url" => "https://www.ncbi.nlm.nih.gov/pubmed/5325049"
                            "web" => "Medline"
                          ]
                        ]
                      ]
                    ]
                  ]
                ]
              ]
            ]
            7 => array:3 [
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              "etiqueta" => "8"
              "referencia" => array:1 [
                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Rapid identification of bacteria from positive blood cultures by fluorescence-based PCR-single-strand conformation polymorphism analysis of the 16S rRNA gene"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:5 [
                            0 => """
                              CY Turene \n
                              \t\t\t\t\t\t\t\t
                              """
                            1 => """
                              E Witwicki \n
                              \t\t\t\t\t\t\t\t
                              """
                            2 => """
                              DJ Hoban \n
                              \t\t\t\t\t\t\t\t
                              """
                            3 => """
                              JA Karlowsky \n
                              \t\t\t\t\t\t\t\t
                              """
                            4 => """
                              AM Kabani \n
                              \t\t\t\t\t\t\t\t
                              """
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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