Original article
Epidemiology of Aeromonas spp. isolated from stool in a tertiary hospital in Cantabria, Northern Spain, in the last five years
Epidemiología de Aeromonas spp. aisladas de heces en un hospital terciario en Cantabria, norte de España, en los últimos 5 años
Carlos Ruiz de Alegría-Puig
, Marta Fernández-Martínez, Ana De Malet Pintos-Fonseca
Corresponding author
Microbiology Service, University Hospital Marqués de Valdecilla-IDIVAL, Santander, Spain
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array:1 [ "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Seasonal distribution of <span class="elsevierStyleItalic">Aeromonas</span> spp. in children and adults.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">The genus <span class="elsevierStyleItalic">Aeromonas</span> belongs to the <span class="elsevierStyleItalic">Aeromonadaceae</span> family and comprises a group of Gram-negative bacteria widely distributed in aquatic environments, but its great capacity for adaptation also makes <span class="elsevierStyleItalic">Aeromonas</span> species able to colonize terrestrial environments, so these microorganisms can be identified from different sources, such as soils, plants, fruits, vegetables, birds, reptiles, amphibians, among others.<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">1</span></a> The genus <span class="elsevierStyleItalic">Aeromonas</span> comprises of two different groups of bacteria. One is non-motile psychrophilic <span class="elsevierStyleItalic">Aeromonas salmonicida</span> and the other group comprising of three mesophilic motile spp. <span class="elsevierStyleItalic">Aeromonas hydrophila</span>, <span class="elsevierStyleItalic">Aeromonas caviae</span>, and <span class="elsevierStyleItalic">Aeromonas sobria</span>.<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">2</span></a> Some species of <span class="elsevierStyleItalic">Aeromonas</span> are known to be pathogenic in both mammals and reptiles or fish, particularly in humans, Aeromonads, are known to cause gastroenteritis and extraintestinal diseases such as septicemia, skin, eye, wound and respiratory tract infections.<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">3</span></a> It has not always been easy to identify <span class="elsevierStyleItalic">Aeromonas</span> spp. by traditional biochemical tests in clinical microbiology laboratories. Today, thanks to the new technologies used such as mass spectrometry, which is increasingly used because it is faster, simpler and with high precision with respect to traditional methods, make it easier identifying them. Some <span class="elsevierStyleItalic">Aeromonas</span> species are found forming part of the human gastrointestinal microbiota, varying the rates of frequency from 0% to 4% in persons with no disease to 0.8–7.4% in persons with diarrheal illness.<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">4</span></a> The prevalence in case of diarrhea in pediatric age is around 4.6%<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">5</span></a> and also it has been described as a co-pathogen at 1.9–57.7% in pediatric age.<a class="elsevierStyleCrossRefs" href="#bib0105"><span class="elsevierStyleSup">6,7</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">The objective of this study was to know the epidemiological distribution of <span class="elsevierStyleItalic">Aeromonas</span> spp. in our health area, to determine the most significant symptom associated with Aeromonas, frequency of association as co-pathogen, identification of existing species as well as age of distribution or existence of seasonal association in our environment.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Material and methods</span><p id="par0015" class="elsevierStylePara elsevierViewall">Retrospective descriptive study, through the laboratory information system (SIL), of isolates of <span class="elsevierStyleItalic">Aeromonas</span> spp. in stool between 2016 and 2020 in the Microbiology Department of the University Hospital Marqués de Valdecilla, Santander, that serves a total of 313.040 census population. The protocol for these isolates included inoculated on Yersinia Selective Agar (CIN Agar; BD, Heidelberg, Germany) and incubated at 37<span class="elsevierStyleHsp" style=""></span>°C for 24<span class="elsevierStyleHsp" style=""></span>h. Identification was performed by MALDI-TOF system (Vitek-MS®, BioMerieux) and most of them were confirmed by multiplex PCR developed by Perssons S et al.<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">8</span></a> The statistical analysis was performed by Fisher statistical test with SPSS program.</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Results</span><p id="par0020" class="elsevierStylePara elsevierViewall">A total of 366 isolates of <span class="elsevierStyleItalic">Aeromonas</span> spp. were analyzed. It was 1.1% of the total of coprocultures analyzed and 15.8% of all enteropathogens identified in the years under study, behind <span class="elsevierStyleItalic">Campylobacter</span> spp. (57.8%) and <span class="elsevierStyleItalic">Salmonella enterica</span> (25.2%), but at the same time far ahead of other genera such as <span class="elsevierStyleItalic">Yersinia enterocolitica</span> (1.3%) or <span class="elsevierStyleItalic">Shigella</span> spp. (0.5%). <span class="elsevierStyleItalic">A. caviae</span> was the most prevalent species (78.5%), at a large distance from other species such as <span class="elsevierStyleItalic">A. sobria/veronii</span> (9.0%) or <span class="elsevierStyleItalic">A. hydrophila</span> (2.4%). Without taking into account the enteropathogenic <span class="elsevierStyleItalic">Escherichia coli</span> serotypes that are identified at the express request of the clinician.</p><p id="par0025" class="elsevierStylePara elsevierViewall">No significant differences were found in sex distribution (190; 52.0% women) nor in the frequency of infection in adults (>16 years) with respect to pediatric age (185; 50.5%), with a mean age of infection of 34 years (range 0–98 years). Diarrhea was found as the most common referred symptom (162;44.0%), followed by acute gastroenteritis (78; 21.3%). A total of 58 co-infections were identified (15.93%), being significantly more frequent in pediatric ages (49;84.5%) (<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.05) and mostly associated with <span class="elsevierStyleItalic">Campylobacter</span> spp. (75.9% of the total co-infections and 75.5% in pediatric age). <span class="elsevierStyleItalic">A. caviae</span> (51, 87.9%) was the most frequently isolated species as a copathogen regardless of age.</p><p id="par0030" class="elsevierStylePara elsevierViewall">Antimicrobial sensitivity to the most commonly used antibiotics showed good activity to cotrimoxazole (92.9%), ciprofloxacin (86.1%) and cefepime (98.9%).</p><p id="par0035" class="elsevierStylePara elsevierViewall">The 52.0% of the studied samples were requested from health centers, followed by emergency service for both pediatric 12.6% and adult age 10.9%. The most frequently observed symptom was diarrhea 44.2%, being bloody in 4.6% of cases, followed by acute gastroenteritis in 21.3%.</p><p id="par0040" class="elsevierStylePara elsevierViewall">In the cases accumulated by months, there is a clear increase in the incidence in summer, especially in the month of August (15.8%), being significant this increase for adults (<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.02) and children (<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.04) (see <a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>).</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Discussion</span><p id="par0045" class="elsevierStylePara elsevierViewall"><span class="elsevierStyleItalic">Aeromonas</span> spp. ranks third in terms of incidence of enteropathogenic bacteria in our area of influence, as opposed to other series in the 1990s, possibly due to the fact that in those years it was not yet considered a primary pathogen. But in more recent series this enteropathogen does not appear possibly because it is not included in the molecular syndromic panels of recent massive introduction in clinical diagnostic laboratories.<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">9</span></a> It is true that its finding in association with another enteropathogen,<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">7</span></a> as well as its known role as part of the usual intestinal microbiota<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">10</span></a> or doubts about its possible pathogenicity mechanism,<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">11</span></a> relegate it to the identification of classical enteropathogens. Even more in case of isolation of <span class="elsevierStyleItalic">A. caviae</span> in pediatric age where it is not given much attention, although published series show that <span class="elsevierStyleItalic">A. caviae</span> is the most frequently isolated species<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">12</span></a> a fact that coincides with our population.</p><p id="par0050" class="elsevierStylePara elsevierViewall">In the present study, <span class="elsevierStyleItalic">Campylobacter</span> spp. showed a significant association with <span class="elsevierStyleItalic">Aeromonas</span> spp. particularly in the younger age group, as other studies in our country.<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">13</span></a> Is reported <span class="elsevierStyleItalic">Aeromonas</span> spp. as a part of a polymicrobial infection, which raises the question of whether it is behaving as a nonpathogenic “co-traveler”, perhaps acquired from the same source as the true pathogen, or is interacting with other agents to cause disease. The almost exclusive appearance of the species <span class="elsevierStyleItalic">A. caviae</span> and its lower virulence can indicate its appearance in feces as a colonizer. Pathogens commonly reported in literature to coexist with <span class="elsevierStyleItalic">Aeromonas</span> are rotavirus, <span class="elsevierStyleItalic">Shigella</span>, <span class="elsevierStyleItalic">Campylobacter</span>, and <span class="elsevierStyleItalic">Escherichia coli</span> O157:H7.<a class="elsevierStyleCrossRefs" href="#bib0135"><span class="elsevierStyleSup">12,14</span></a> This feature in identifying <span class="elsevierStyleItalic">Aeromonas</span> can help the microbiologist and pediatrician be alert to a possible primary enteropathogen.</p><p id="par0055" class="elsevierStylePara elsevierViewall">But the pathogenicity is clear both by its association with diarrhea, as in this and other works and by the identification of virulence genes especially in species such as <span class="elsevierStyleItalic">Aeromonas hydrophila</span> or <span class="elsevierStyleItalic">Aeromonas sobria</span>.<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">15</span></a></p><p id="par0060" class="elsevierStylePara elsevierViewall">We can conclude that <span class="elsevierStyleItalic">Aeromonas</span> spp. is an enteropathogen that appears very frequently in the feces of patients with digestive symptoms both in our health area and in other published case series. Circumstance that should be taken into account when deciding to diagnose patients with gastrointestinal pathology with syndromic panels in which <span class="elsevierStyleItalic">Aeromonas</span> spp is not included.</p><p id="par0065" class="elsevierStylePara elsevierViewall">The appearance of <span class="elsevierStyleItalic">Aeromonas</span> spp. in feces of patients at an early age, in many cases, is associated with the appearance of a classic primary copathogen, in our case <span class="elsevierStyleItalic">Campylobacter</span> spp. This finding could alert in the active search by molecular techniques for primary pathogens if they are not isolated by stool culture, especially in those cases that are associated with diarrhea, bloody diarrhea or acute gastroenteritis.</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Transparency declarations</span><p id="par0070" class="elsevierStylePara elsevierViewall">All authors have nothing to declare. This study has not been financially supported by any Diagnostic/Pharmaceutical company.</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Ethical approval</span><p id="par0075" class="elsevierStylePara elsevierViewall">Not applicable.</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Funding</span><p id="par0080" class="elsevierStylePara elsevierViewall">This study was supported by <span class="elsevierStyleGrantSponsor" id="gs1">Plan Nacional de I+D+i 2013–2016</span>, <span class="elsevierStyleGrantSponsor" id="gs2">Instituto de Salud Carlos III</span>, <span class="elsevierStyleGrantSponsor" id="gs3">Subdirección General de Redes y Centros de Investigación Cooperativa</span>, <span class="elsevierStyleGrantSponsor" id="gs4">Ministerio de Economía y Competitividad</span>, <span class="elsevierStyleGrantSponsor" id="gs5">Spanish Network for Research in Infectious Diseases</span> (<span class="elsevierStyleGrantNumber" refid="gs5">REIPI RD16/0016/0007</span>).</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Conflict of interest</span><p id="par0085" class="elsevierStylePara elsevierViewall">The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:13 [ 0 => array:3 [ "identificador" => "xres1877919" "titulo" => "Abstract" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Introduction" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Methods" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Results" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Discussion" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec1628842" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres1877918" "titulo" => "Resumen" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0025" "titulo" => "Introducción" ] 1 => array:2 [ "identificador" => "abst0030" "titulo" => "Métodos" ] 2 => array:2 [ "identificador" => "abst0035" "titulo" => "Resultados" ] 3 => array:2 [ "identificador" => "abst0040" "titulo" => "Discusión" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec1628841" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:2 [ "identificador" => "sec0010" "titulo" => "Material and methods" ] 6 => array:2 [ "identificador" => "sec0015" "titulo" => "Results" ] 7 => array:2 [ "identificador" => "sec0020" "titulo" => "Discussion" ] 8 => array:2 [ "identificador" => "sec0025" "titulo" => "Transparency declarations" ] 9 => array:2 [ "identificador" => "sec0030" "titulo" => "Ethical approval" ] 10 => array:2 [ "identificador" => "sec0035" "titulo" => "Funding" ] 11 => array:2 [ "identificador" => "sec0040" "titulo" => "Conflict of interest" ] 12 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2021-06-17" "fechaAceptado" => "2021-09-14" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1628842" "palabras" => array:3 [ 0 => "<span class="elsevierStyleItalic">Aeromonas</span> spp." 1 => "Diarrhea" 2 => "MALDI-TOF" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec1628841" "palabras" => array:3 [ 0 => "<span class="elsevierStyleItalic">Aeromonas</span> spp." 1 => "Diarrea" 2 => "MALDI-TOF" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:3 [ "titulo" => "Abstract" "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Introduction</span><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">The role of <span class="elsevierStyleItalic">Aeromonas</span> species in gastrointestinal disease is controversial. The aim of this study was to know the epidemiological distribution of <span class="elsevierStyleItalic">Aeromonas</span> spp. isolated from stool in our health area, determine the existence of diarrhea as a significant symptom, identification of existing species in our environment and association as co-pathogen.</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Methods</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">It was a retrospective descriptive study of isolates of <span class="elsevierStyleItalic">Aeromonas</span> spp. in feces (2016–2020). The protocol for these isolates included coproculture, identification by MALDI-TOF (Vitek-MS®, BioMerieux) and confirmation by multiplex PCR.</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">A total of 366 <span class="elsevierStyleItalic">Aeromonas</span> spp. isolates were analyzed being <span class="elsevierStyleItalic">Aeromonas caviae</span> the most prevalent species (289, 78.7%). A total of 58 (15.8%) co-infections were identified, being more frequent in pediatric age (49;84.5%) (<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0.01) and mostly associated with <span class="elsevierStyleItalic">Campylobacter</span> spp.</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Discussion</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleItalic">Aeromonas</span> spp. prove to be a gastrointestinal pathogen more frequently associated with co-infections in pediatric age, evidencing its appearance especially with <span class="elsevierStyleItalic">Campylobacter</span> spp.</p></span>" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Introduction" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Methods" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Results" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Discussion" ] ] ] "es" => array:3 [ "titulo" => "Resumen" "resumen" => "<span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Introducción</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">El papel de las especies de <span class="elsevierStyleItalic">Aeromonas</span> en la enfermedad gastrointestinal es muy controvertido. El objetivo de este estudio fue conocer la distribución epidemiológica de <span class="elsevierStyleItalic">Aeromonas</span> spp. aislada de heces en nuestra área de salud, determinar la existencia de diarrea como síntoma significativo, la identificación de especies existentes en nuestro entorno y la asociación como copatógeno.</p></span> <span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Métodos</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Se trata de un estudio descriptivo retrospectivo de aislados de <span class="elsevierStyleItalic">Aeromonas</span> spp. en heces (2016-2020). El protocolo para estos aislamientos incluía coprocultivo, la identificación por MALDI-TOF (VITEK®MS, bioMérieux) y la confirmación por PCR multiplex.</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Se analizaron un total de 366 aislados de <span class="elsevierStyleItalic">Aeromonas</span> spp., siendo <span class="elsevierStyleItalic">Aeromonas caviae</span> la especie más prevalente (289; 78,7%). Se identificaron un total de 58 (15,8%) coinfecciones, siendo significativamente más frecuentes en edades pediátricas (49; 84,5%) (p<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>0,01) y asociadas principalmente con <span class="elsevierStyleItalic">Campylobacter</span> spp.</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Discusión</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleItalic">Aeromonas</span> spp. resulta ser un patógeno gastrointestinal que se asocia con mayor frecuencia a coinfecciones en la edad pediátrica, evidenciando su aparición especialmente con <span class="elsevierStyleItalic">Campylobacter</span> spp.</p></span>" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0025" "titulo" => "Introducción" ] 1 => array:2 [ "identificador" => "abst0030" "titulo" => "Métodos" ] 2 => array:2 [ "identificador" => "abst0035" "titulo" => "Resultados" ] 3 => array:2 [ "identificador" => "abst0040" "titulo" => "Discusión" ] ] ] ] "multimedia" => array:1 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 2849 "Ancho" => 2500 "Tamanyo" => 235537 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Seasonal distribution of <span class="elsevierStyleItalic">Aeromonas</span> spp. in children and adults.</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0015" "bibliografiaReferencia" => array:15 [ 0 => array:3 [ "identificador" => "bib0080" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "The genus <span class="elsevierStyleItalic">Aeromonas</span>: a general approach" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:6 [ 0 => "R.B. 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Gutiérrez-Ferández" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1016/j.ram.2019.03.003" "Revista" => array:6 [ "tituloSerie" => "Rev Argent Microbiol" "fecha" => "2020" "volumen" => "52" "paginaInicial" => "22" "paginaFinal" => "26" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/31248693" "web" => "Medline" ] ] ] ] ] ] ] ] 13 => array:3 [ "identificador" => "bib0145" "etiqueta" => "14" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Prevalence, serotype distribution, antibiotic susceptibility and genetic profiles of mesophilic <span class="elsevierStyleItalic">Aeromonas</span> species isolated from hospitalized diarrhoeal cases in Kolkata, India" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:6 [ 0 => "S. Sinha" 1 => "T. Shimada" 2 => "T. Ramamurthy" 3 => "S.K. Bhattacharya" 4 => "S. Yamasaki" 5 => "Y. Takeda" ] ] ] ] ] "host" => array:1 [ 0 => array:2 [ "doi" => "10.1099/jmm.0.05269-0" "Revista" => array:6 [ "tituloSerie" => "J Med Microbiol" "fecha" => "2004" "volumen" => "53" "paginaInicial" => "527" "paginaFinal" => "534" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/15150333" "web" => "Medline" ] ] ] ] ] ] ] ] 14 => array:3 [ "identificador" => "bib0150" "etiqueta" => "15" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Genetic diversity and virulence potential of clinical and environmental <span class="elsevierStyleItalic">Aeromonas</span> spp. isolates from a diarrhea outbreak" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:6 [ 0 => "L.C.A.D. Silva" 1 => "T.C. Leal-Balbino" 2 => "B.S.T. Melo" 3 => "C.L. Mendes-Marques" 4 => "A.M. Rezende" 5 => "A.M.P. 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| Year/Month | Html | Total | |
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| 2024 November | 2 | 1 | 3 |
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| 2024 February | 6 | 0 | 6 |
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